American Journal of Forensic Medicine and Pathology - Vol 32, No. 2, June 2011

ORIGINAL ARTICLE

Virtual Casting of Stab Wounds in Cartilage Using MicroYComputed Tomography Derrick J. Pounder, FRCPA and Louise J. Sim, BMSc

Abstract: In homicidal stabbings using a serrated knife, stab wounds involving costal cartilage leave striations on the cut surface of the cartilage from the serration points on the blade edge. Class characteristics of the serrated blade can be determined from the striation marks, and individualizing characteristics may be seen also. The traditional method for recording the striation marks involves the pernickety technique of casting with dental impression material. We assessed the potential utility of microYcomputed tomography scanning of the stab track as a technique for nondestructive recording of striation patterns and virtual casting of them. Stab tracks in porcine cartilage, produced with a coarsely serrated blade, were scanned with a bench-top microYcomputed tomography scanner. The typical irregularly regular striation pattern could be demonstrated, and the images manipulated, using proprietary software to produce a virtual cast. Whether the technology will have sufficient resolution to image not only class characteristic tool marks but also the much finer individualizing tool marks remains to be evaluated, but the technology shows considerable promise. Key Words: micro-CT, stab wounds, forensic microradiology, serrated knives (Am J Forensic Med Pathol 2011;32: 97Y99)

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n many jurisdictions, stabbing is a common method of homicide, with the weapon often one of opportunity in the home.1 In a domestic kitchen, serrated knives are increasingly common, as is their use in homicides.2 There is a high frequency of anterior thorax wounds in homicidal stabbings,3 and stab wounds from serrated knives involving costal cartilages leave striations on the cut surface of the cartilage from the serration points on the blade edge.4,5 Class characteristics of the serrated blade can be determined from the striation marks on cartilage,5 and individualizing characteristics may be seen also in both serrated and nonserrated blades.6Y9 Examination of tool marks on cartilage currently requires casting with dental impression material and examination of the casts.5,6 The purpose of this experimental study, using porcine cartilage, was to assess the potential utility of microYcomputed tomography (CT) scanning of the stab track as a technique for nondestructive recording of striation patterns and virtual casting of them.

MATERIALS AND METHODS A left-side-ground(scalloped), straight-spine, coarsely serrated knife, purchased from a department store, was used to stab Manuscript received September 20, 2010; accepted October 8, 2010. From the Centre for Forensic and Legal Medicine, University of Dundee, Dundee, Scotland, UK. Reprints: Derrick Pounder, FRCPA, Centre for Forensic and Legal Medicine, University of Dundee, Dundee, Scotland, UK DD1 4HN. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0097 DOI: 10.1097/PAF.0b013e3182186f37

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porcine cartilage using a previously published experimental setup.5 The stab wound was trimmed to less than 1.5  3cm to fit a bench-top micro-CT, a SkyScan 1072 (SkyScan, Kontich, Belgium). Scans of closed stab tracks were compared with scans following 3 different preparatory techniques intended to facilitate imaging: introducing an osmium tetroxide solution into the stab track as a contrast stain, opening one end of the stab track slightly to maintain an air gap between the stab track walls, and opening the stab track fully by bisecting it as would be done before casting with dental impression material.5 Images were obtained at 50 kV and 197 KA with no filter. For each specimen, a series of images were obtained with a rotation of 0.6750 degrees between each image through 180 degrees using a magnification of 15 (pixel size, 19.098 Km). Best results were obtained when the reconstruction duration per slice was extended to between 0.7 and 0.96 seconds. The knife blade tip was removed and scanned using adjusted parameters of 70 kV and 142 KA and using a 1-mm Al filter. From the series of images, a stack of 2-dimensional sections was reconstructed, stored in .bmp format using NRecon software (version 1.6.1.3; SkyScan N.V), points on the specimen selected for reconstruction, and then 3-dimensional (3D) analysis and modeling achieved using both CTAn (CT Analyser (version 1.10.0.2; SkyScan N.V) and CTVol (3D visualization, version 2.1.0.0; SkyScan). Data were stored in CTM format. Before creating the 3D model, smoothing and despeckled plug-ins were used to add or remove pixels from the surface and to remove ‘‘noise’’ to improve the image quality. CTVol was used to create an animated movie, as well as allowing viewing of multiple models simultaneously. Models were viewed also in stereo mode, which, with the use of 3D glasses, enables the viewer to see the model in true 3D.

RESULTS AND DISCUSSION On naked-eye examination, striations present on the stab track walls of the cartilage had the characteristic pattern described in the literature,4,5 representing class characteristic tool marks from the serration points of the blade. Knives can either be left- or right side-ground (scalloped), and the knife used in this experiment was left-side ground. With scalloping on the left side of the blade, the scalloping creates broad ridges on the left wall of the wound with narrow striation valleys corresponding to the serration points. The right wall of the wound is a mirror image, with broad valleys and narrow ridges.5 Casting the stab track wall with dental impression material reverses the image (Fig. 1). Micro-CT scanning allows visualization of the stab track walls and also virtual casting of the stab track by computer program selection of the air gap between the opposing walls of the stab track, producing a cast-like reverse image of the stab track walls (Figs. 2 and 3). Computed tomographic scans of 12 stab tracks were obtained. Scans obtained from closed stabs were not satisfactory because the air gap between the 2 walls of the stab track was incomplete. The best scans were produced when the stab wound was opened up slightly or fully, but the latter technique required

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FIGURE 3. Three-dimensional virtual cast of stab track in cartilage from a left-side-ground, serrated blade. This side represents the virtual cast of the right wall and therefore shows broad ridges and narrow valleys.

FIGURE 1. Dental impression material cast of cartilage stab track wall together with serrated blade, illustrating the irregularly regular pattern of striations produced by the serrations.

virtual cast and the knife blade models to be demonstrated side by side so that it is possible to illustrate for presentational purposes how the stab track striation pattern was produced by the blade serration pattern (Fig. 4). The use of micro-CT has practical advantages in that there is no special specimen preparation, it is rapid and nondestructive, it does not require complete separation of the 2 walls of the stab track, and it does away with the time-consuming and pernickety technique of casting with dental impression material. Its disadvantages lie in the availability of the equipment and of personnel experienced in scanning cartilage and manipulating of the data. It remains to be seen whether current technology will have sufficient resolution to image not only class characteristic

care in marking the 2 halves to prevent confusion as to their relative orientation. Staining with osmium tetroxide also produced good-quality 3D pictures. Osmium tetroxide has been the most commonly used contrast stain for micro-CT imaging of soft tissues, because osmium has electron-binding energies favorable for strong x-ray absorption. However, osmium tetroxide is very toxic and expensive and does not stain well if samples have been stored in alcohol.10 The 3D models created using micro-CT demonstrated the striations on the surface of the cartilage, so that the characteristic striation pattern expected from serrated blades could be seen (Figs. 2 and 3). Scanning the blade allows both the stab track

FIGURE 2. Three-dimensional virtual cast of stab track in cartilage from a left-side-ground, serrated blade. This side represents the virtual cast of the left wall and therefore shows broad valleys and narrow ridges.

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FIGURE 4. Three-dimensional model of cartilage with striations produced by the blade serrations together with the knife tip (compare with Fig. 1). * 2011 Lippincott Williams & Wilkins

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Virtual Casting of Stab Wounds Using Micro-CT

tool marks5 but also the much finer individualizing tool marks.6Y9,11 However, it seems likely that the technology will sooner or later be up to the task.

4. Bonte W. Tool marks in bones and cartilage. J Forensic Sci. 1975; 20(2):315Y325. 5. Pounder DJ, Cormack L, Broadbent E, et al. Class characteristics of serrated knife stab wounds to cartilage [published online ahead of print]. Am J Forensic Med Pathol. doi:10.1097/PAF.0b013e3181db7ee4. Accessed September 7, 2010.

ACKNOWLEDGMENTS The authors thank Mr Kevin Mackenzie, Microscopy and Imaging Facility, Institute of Medical Sciences, University of Aberdeen, for assisting in the use of the SkyScan 1072 micro-CT scanner.

6. Rao V, Hart R. Tool mark determination in cartilage of stabbing victim. J Forensic Sci. 1983;28(3):794Y799. 7. Ernest RN. Toolmarks in cartilage revisited. AFTE J. 1991;23(4): 958Y959.

REFERENCES

8. Mikko D, Hornsby BJ. On the cutting edge IIVan identification involving a knife. AFTE J. 1995;27(4):293.

1. Ormstad K, Karlsson T, Enkler L, et al. Patterns in sharp force fatalitiesVa comprehensive forensic medical study. J Forensic Sci. 1986;31(2):529Y542. 2. Hanzlick R, Graham M. Sharp Force Injury, Forensic Pathology in Criminal Cases. 2nd ed. Charlottesville, VA: Lexis; 2000:211Y221. 3. Karlsson T. Homicidal and suicidal sharp force fatalities in Stockholm Sweden. Orientation of entrance wounds in stabs gives information in the classification. Forensic Sci Int. 1998;93:21Y32.

9. Thompson E, Wyant R. Knife identification project (KIP). AFTE J. 2003;35(4):366Y370. 10. Metscher BD. MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues, BMC Physiol. 2009;9:11. doi:10.1186/1472-6793-9-11. 11. Wong DT. Preservation and examination of tool marks on cartilage and bone. AFTE J. 2007;39(4):265Y280.

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ORIGINAL ARTICLE

Minimum Velocity Necessary for Nonconventional Projectiles to Penetrate the Eye An Experimental Study Using Pig Eyes John W. Marshall, BSc (Hons), Dean B. Dahlstrom, BSc, and Kramer D. Powley, BSc Abstract: To satisfy the Criminal Code of Canada’s definition of a firearm, a barreled weapon must be capable of causing serious bodily injury or death to a person. Canadian courts have accepted the forensically established criteria of ‘‘penetration or rupture of an eye’’ as serious bodily injury. The minimal velocity of nonconventional ammunition required to penetrate the eye including airsoft projectiles has yet to be established. To establish minimal threshold requirements for eye penetration, empirical tests were conducted using a variety of airsoft projectiles. Using the data obtained from these tests, and previous research using ‘‘air gun’’ projectiles, an ‘‘energy density’’ parameter was calculated for the minimum penetration threshold of an eye. Airsoft guns capable of achieving velocities in excess of 99 m/s (325 ft/s) using conventional 6-mm airsoft ammunition will satisfy the forensically established criteria of ‘‘serious bodily injury.’’ The energy density parameter for typical 6-mm plastic airsoft projectiles is 4.3 to 4.8 J/cm2. This calculation also encompasses 4.5-mm steel BBs. Key Words: airsoft, BB, pellet, eye penetration (Am J Forensic Med Pathol 2011;32: 100Y103)

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ection 2 of the Canadian Criminal Code defines a firearm as ‘‘a barrelled weapon from which a bullet or projectile can be discharged and that is capable of causing serious bodily injury or death to a person.’’1 Although ‘‘serious bodily injury’’ has not been defined by the Canadian courts, the penetration of an eye has been accepted by the Canadian Judicial System as the minimum criterion for serious bodily injury (R. v. Cripps, 2006 CanLII 29523 [ON S.C.], R. v. B.[E.], 2007 ONCJ 518 [CanLII]). A previous study establishing the V50 (defined as the velocity at which 50% of test projectiles will penetrate and 50% will not) for threshold velocity for penetration of an eye by a BB at 75 m/s (246 ft/s) has been widely accepted.2 With the recent development and importation into Canada of a variety of nonconventional firearm/ammunition combinations, typically airsoft, it is necessary to determine the penetration threshold for a variety of airpropelled projectiles. This information will assist the courts in the legal classification of these items. One previous study3 compiled information from tests involving the shooting of 13 pig and 14 humans eyes with 0.11-g 6-mm plastic airsoft pellets. There were no reported globe ruptures for the pig eyes occurring at a velocity range of 67.22 to 115.63 m/s. Only 1 reported rupture of a human eye occurred within the velocity range of 73.03 to 117.80 m/s; it occurred at 109.44 m/s. Manuscript received September 2, 2008; accepted April 11, 2009. From the Forensic Laboratory Services Y Firearms Section, Royal Canadian Mounted Police, Regina, Saskatchewan, Canada. Reprints: John W. Marshall, Forensic Laboratory Services Y Firearms Section, Royal Canadian Mounted Police, Regina, Saskatchewan, Canada. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0100 DOI: 10.1097/PAF.0b013e31820c2be2

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Research has attempted to determine the threshold velocity required for penetration of human skin by both conventional and nonconventional air-propelled ammunition.4Y10 The purposes of the current study were (1) to determine the minimum threshold velocities of specific projectiles to penetrate the eye, most which are ‘‘airsoft,’’ and (2) to determine whether an ‘‘energy density’’ calculation parameter may be used to determine the threshold for eye penetration of untested ammunition. Energy density formula, defined as energy per unit area (E/a), has been previously calculated for typical air-propelled ammunition (BBs and lead pellets) in a number of previous studies examining threshold penetration of human skin.4Y6,10 This formula uses the weight, diameter, and velocity of a projectile required to penetrate an object. We hypothesize that this formula may also be used to calculate the variables required for projectiles to penetrate the eye. If verified, this formula will allow the evaluation of previously untested ammunition to determine eye rupture potential.

MATERIALS AND METHODS Previous research examining threshold penetration values using air-propelled ammunition has included the recorded velocity measurements of individual shots. Close-range firing during this research prevented the recording of individual projectile velocities related to impact damage. This departure from previous studies was due to the inaccuracy of soft air projectiles fired at a distance. To determine velocity, a series of tests were initially fired to establish a velocity range. A Doppler radar chronograph was used to measure these velocities. These test velocities were recorded, and a subsequent series of tests shots were fired into pigs’ eyeballs. Penetrations were recorded. A new eyeball was used for each shot. All eyeballs were shot from a distance of 2 inches, a distance guaranteeing near-muzzle velocity and accurate shot placement. Each recorded shot hit the cornea at 90 degrees (Fig. 1). The pig eyes were fresh, received within 48 hours of butchering, refrigerated, and packed in water to ensure hydration. Before firing, each eyeball was placed in a cavity formed in a Styrofoam block simulating the orbit and secured by a clamp on the optic nerve, applying slight pressure. Two complete series of tests were conducted, using eyes from different shipments. A minimum of 5 shots was recorded for each test event.

RESULTS The results are summarized in Table 1, with only penetrations of the cornea recorded. Damage less than rupture was disregarded for the purpose of this research. Owing to the inaccuracy of the gun/projectile combination, specific velocities of the airsoft projectiles that penetrated could not be recorded. An accurate V50 could not be determined. With a high-speed videocamera, the velocity of individual shots could be calculated to determine V50. Am J Forensic Med Pathol

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Minimum Velocity Necessary to Penetrate the Eye

TABLE 2. New Research on Spheres (Projectiles Designed for Soft Air Guns)

Composition Metal* Plastic Plastic Plastic

Diameter, mm 6 6 6 8

Lowest Recorded Velocity Causing Weight, Eye Penetration, E/a, m/s J/cm2 g 0.30 0.11 0.25 0.34

101 (pig) 123 (pig) 99 (pig) 113.6 (pig)

5.4 2.9 4.3 4.3

All raw data for each series of tests are available on request. *Unknown type of metal.

FIGURE 1. Penetration of pigs’ eyes with 6-mm plastic airsoft pellet.

In the first series of 5 shots with the 0.25-g projectiles, 1 penetration occurred. The velocities ranged from 99 to 104 m/s (325Y341 ft/s). One penetration occurred during the second series of tests, with velocities ranging from 99 to 110 m/s (325Y361 ft/s). It is the authors’ opinion that the velocities recorded encompass the minimum threshold for penetration of the pigs’ eyes. The 0.11-g 6-mm projectile penetrated the eye once in the first series of tests where velocities were recorded between 105 and 123 m/s (344Y403 ft/s). There were no penetrations recorded at velocities between 94 and 110 m/s (308Y361 ft/s). These limited data may indicate that the threshold may be encompassed within the velocity parameters closer to the high end of the range. Further testing is required to validate this assumption. These findings are similar to the results documented by Kennedy et al.3 Eye penetrations occurred for all shots within the 6-mm metal and 8-mm plastic projectile tests. This suggests that these velocities exceed the minimal threshold penetration requirements. E/a values calculated for this new data are shown in Table 2. Using the data listed in Table 2 and the calculated E/a values for spheres based on existing research (Table 3), an E/a range of 4.3 to 4.8 J/cm2 can be used as an acceptable threshold for eye penetration of spheres. Further testing with a larger database is required to validate the minimal threshold velocity for penetration and the associated calculations for E/a. However, using 4.3 to 4.8 J/cm2 as the threshold standard for spherical penetration, the velocities have been calculated and are reported in Table 4. The theoretical data are verified by the recorded data from the 6-mm projectile tests. The calculated E/a as tested for the 0.11-g plastic 6-mm projectile is 2.9 J/cm2 using the highest recorded velocity. This may have occurred as a result of a velocity or penetration anomaly. TABLE 1. Results for Airsoft Projectile Tests Projectile Type

No. Ruptures Recorded Velocity Range (out of 5 Shots)

6-mm plastic 0.25 g 99Y104 m/s (325Y341 ft/s) 6-mm plastic 0.25 g 99Y110 m/s (325Y361 ft/s) 6-mm plastic 0.11 g 105Y123 m/s (344Y403 ft/s) 6-mm plastic 0.11 g 94Y110 m/s (308Y361 ft/s) 6-mm metal 0.30 g 101Y106 m/s (331Y348 ft/s) 8-mm plastic 0.34 g 113Y126 m/s (371Y413 ft/s)

1 1 1 0 5 5

Appendix 1 is the E/a formula. Appendix 2 is a summary of calculated E/a for skin penetration previously reported. To expand on the eye penetration data collected from test shots within the body of this research, the theoretical threshold velocities for eye penetration for both 4.5- and 5.6-mm lead pellets were calculated, and these are presented in Table 5. These penetration velocities were calculated using the existing skin penetration velocities and comparing them to tested data for both skin and eye penetration of 4.5-mm BBs. These calculations were formulated on the assumption that skin-to-eye penetration threshold ratios would be consistent for the 5.6-mm lead pellet as well as the 4.5-mm BB and lead pellet. This assumption was verified by collecting penetration velocity test data from the 4.5-mm lead pellet. Appendix 3 is an example of this calculation. These calculations were also used to convert the data of Williams and Stewart11 from the reported V50 to the lowest penetrating velocities. Data collected within this current study are concerned only with the breach of tissue (rupture of the eye) and not the perforation. The calculations for E/a in skin by previous authors seem to have a wide variance. This may be a result of the previous authors’ interpretation of penetration and perforation. Rathman’s10 article, in particular, discusses the importance of projectile shape in the advancement of the projectile through the tissue. The E/a for penetration of pellets is higher than the E/a values for spheres and remains constant for plastic, steel, and lead. This suggests that shape (cross section of the nose) is a significant factor in E/a calculations.

DISCUSSION Airsoft guns capable of discharging 6-mm plastic projectiles at velocities in excess of 99 m/s (325 ft/s) may be considered capable of causing ‘‘serious bodily injury.’’ This is a requirement within the definition of a firearm, Section 2 of the Criminal Code of Canada.1 E/a, defined as impact energy per unit area, has been calculated to determine the threshold value for human skin penetration by a sphere in numerous previous studies.9,10 Calculation of E/a for the threshold penetration value for eyes by a sphere can be determined from the data presented in this article as well as previous data presented on BB penetration of the eye.2 The calculated E/a threshold values for an eye by a sphere has been experimentally determined to be from 4.3 to 4.8 J/cm2 for both steel BBs and 0.25-g plastic 6-mm projectiles. Further research will be conducted to validate the E/a threshold value for an eye using a variety of projectiles varying in shape. It will be necessary that a method for controlling projectile velocity be

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TABLE 3. Existing Research on Spheres (Standard BBs for Air Guns) Research

Composition

Diameter, mm

Steel Lead Steel Steel

4.5 4.5 4.5 4.5

2

Powley et al Williams and Stewart11 Williams and Stewart11 Tillet et al12

Weight, g

Lowest Recorded/Reported Velocity at Eye Penetration, m/s

0.36 0.51 0.34 0.345

65.2 (pig) 66 (rabbit)* 56 (rabbit)* 65 (rabbit)

E/a, J/cm2 4.8 5 4.6 4.5

*Calculated data are based on V50 values from original research.

TABLE 4. Calculated Values to Determine the Threshold Velocity for Eye Penetration Composition

Diameter, mm

Weight, g

Velocity (m/s) to Achieve an E/a of 4.3 J/cm2

Velocity (m/s) to Achieve an E/a of 4.8 J/cm2

6 6

0.30 0.11

90 149

95 157

Metal* Plastic *Unknown type of metal.

TABLE 5. New Research on Pellets (Standard Pellets for Air Guns) Composition Lead* Lead† Lead†

Diameter, mm

Weight, g

4.5 4.5 5.6

0.53 0.53 1.06

Lowest Recorded/Calculated Velocity at Eye Penetration, m/s 61 (pig) 63.1 51.33

E/a, J/cm2 6.2 6.6 5.7

*Raw data for this testing are available on request. †Information was theoretically calculated based on eye and skin penetration of 4.5-mm caliber BBs and skin penetration of 4.5- and 5.6-mm pellets; diameters and weights were taken from average pellets.

developed to enable more consistent tests. This will also allow for the calculation of V50 for airsoft projectiles. Author’s supplementary comments: After the original study, a different method using a highspeed videocamera and quantitative software allowing for individual velocity calculations was performed. This subsequent research more precisely defines the E/a threshold parameters for an eye using a soft air projectile and also enables the calculation of V50 for airsoft projectiles. Thirty-one pig eyeballs were shot following the same procedure as previously recorded; however, all results were recorded on a Vision Research Phantom V 7.3 high-speed digital videocamera. The velocity of the soft air projectiles was measured using Track Eye Motion Analysis Software (TEMA) combined with a correction factor for scaling, enabling the recording of individual shots. The scaling factor allows for correction of quantitative analysis when the scale is behind the plane of the projectile. All of the projectiles discharged in the study were 0.20-g 6-mm plastic soft air projectiles. The results confirmed the original finding of the research. The calculated V50 is 366 ft/s. The lowest recorded penetrator is 325 ft/s. The calculated E/a using the calculated V50 is 4.4 J/cm2. The calculated E/a using the lowest recorded penetrator is 3.5 J/cm2. REFERENCES 1. Martin’s Annual Criminal Code. Ontario, Canada: Canada Law Book; retrieved on June 11, 2008. Available at: http://laws.justice.gc.ca/en/C-46/index.html.

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2. Powley KD, Dahlstrom DB, Atkins VJ, et al. Velocity necessary for a BB to penetrate the eye: an experimental study using pig eyes. Wound Ballistics Rev. 1997;3(1):10Y12. 3. Kennedy EA, Ng TP, McNally C, et al. Risk functions for human and porcine eye rupture based on projectile characteristics of blunt objects. Stapp Car Crash J. 2006;50:651Y671. 4. DiMaio VJ. Penetration and perforation of skin by bullets and missiles: a review of the literature. Am J Forensic Med Pathol. 1981;2(2):107Y110. 5. DiMaio VJ, Copeland AR, Besant-Matthews PE, et al. Minimal velocities necessary for perforation of skin by air gun pellets and bullets. J Forensic Sci. 1982;27(4):894Y898. 6. Haag MG. Skin penetration and skin simulants. AFTE J. 2002;34(3):268Y286. 7. Journee C. Rapport entre force vive des balles et la gravite des blessures qu’elles peuvent causer. Rev d’Artillerie. 1907;70:81Y120. 8. MacPherson D. Bullet Penetration: Modelling the Dynamics and the Incapacitation Resulting From Wound Trauma. El Segundo, CA: Ballistic Publications; 1994:221Y243. 9. Mattoo BN, Wani AK, Asgekar MD. Casualty criteria for wounds from firearms with special reference to shot penetrationVpart II. J Forensic Sci. 1974;19(3):585Y589. 10. Rathman GA. The effect of shape on BB and pellet penetration. AFTE J. 1987;19(4):426Y431. 11. Williams RL, Stewart GM. Ballistic studies in eye protection. Am J Ophthalmol. 1964;58:453Y464. 12. Tillet CW, Rose HW, Herget C. High-speed photographic study of perforating ocular injury by the BB. Am J Ophthalmol. 1962;5:675Y688.

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APPENDIX 1 Energy density (or ‘‘E/a’’) equation (as reported in Rathman10).

Lead Pellet (Flat Nose) Diameter, Weight, Velocity at Skin E/a, mm g Penetration, m/s J/cm2

Research

2

E=a ¼

Minimum Velocity Necessary to Penetrate the Eye

2wv Pd 2

Missliwetz et al* DiMaio et al5† Rathman10‡ DiMaio et al5† Rathman10‡

w = weight (kg) v = velocity (m/s) d = diameter (cm)

4.5 4.5 4.5 5.6 5.6

0.49 0.53 0.53 1.06 1.06

136 T 17 101 75

28.3 18.2 29.9 12.8 39

*As reported in Haag’s6 article. †Nose design not stated in research, assumed it was flat nosed by description. ‡Weight of pellets not stated in research, assumed similar to standard pellets.

APPENDIX 2

Lead Pellet (Pointed Nose)

Skin Penetration Blank spaces indicate unreported information within the individual research articles. When the missing information was required to calculate the E/a value, an explanation is given as to where the figures were derived from.

Diameter, Weight, Velocity at Skin E/a, mm g Penetration, m/s J/cm2

Research Rathman10 Missliwetz et al† Rathman10

4.5 4.5 5.6

Diameter, Weight, Velocity at Skin E/a, mm g Penetration, m/s J/cm2

Missliwetz et al* MacPherson8 Rathman10 MacPherson8

4 4.34 4.5 9

0.26 0.34 0.36† 2.9

126 T 14 101 T 9 82 T 21

13 11.8 18 15.4

*As reported in Haag’s6 article. †Weight of BB not stated in research, assumed similar to standard BB.

Lead BB

Missliwetz et al* Mattoo et al9 Journee7

25 20.9 26

APPENDIX 3 Sample Calculation of Theoretical Velocity for Eye Penetration For the 4.5-mm caliber pellet: From p227 in MacPherson8: Lowest velocity value at which 4.5-mm air gun pellet penetrated skin = 290 ft/s Lowest velocity value at which 4.5-mm steel BB penetrated skin = 300 ft/s From Powley et al2: Lowest velocity value at which 4.5-mm steel BB penetrated eye = 214 ft/s

Diameter, Weight, Velocity at Skin E/a, mm g Penetration, m/s J/cm2

Research

109 T 12

*Weight of pellets not stated in research, assumed similar to standard pellets. †As reported in Haag’s6 article.

Steel Sphere (BB) Research

0.53* 0.49 1.06

4.5 8.5 11.25

0.54 4.5 8.5

110 T 12 70 70

½4:5<mm pellet skin penetration
290 ft=s ½4:5<mm BB skin penetration
300 ft=s

20.7 20.2 20.9

*As reported in Haag’s6 article.

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¼ x¼

½4:5<mm pellet eye penetraton
x ½4:5<mm BB eye penetraton
214 ft=s

290 ft=s  214 ft=s ¼ 207 ft=s ð63:1 m=sÞ 300 ft=s

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ORIGINAL ARTICLE

Agonal Sequences in 14 Filmed Hangings With Comments on the Role of the Type of Suspension, Ischemic Habituation, and Ethanol Intoxication on the Timing of Agonal Responses Anny Sauvageau, MD, MSc,* Romano LaHarpe, MD,Þ David King, MD,þ Graeme Dowling, MD,* Sam Andrews, MD,§ Sean Kelly, MD,¶ Corinne Ambrosi, MD,¶ Jean-Pierre Guay, PhD,|| and Vernon J. Geberth, MS, MPS for the Working Group on Human Asphyxia Abstract: The Working Group on Human Asphyxia has analyzed 14 filmed hangings: 9 autoerotic accidents, 4 suicides, and 1 homicide. The following sequence of agonal responses was observed: rapid loss of consciousness in 10 T 3 seconds, mild generalized convulsions in 14 T 3 seconds, decerebrate rigidity in 19 T 5 seconds, beginning of deep rhythmic abdominal respiratory movements in 19 T 5 seconds, decorticate rigidity in 38 T 15 seconds, loss of muscle tone in 1 minute 17 seconds T 25 seconds, end of deep abdominal respiratory movements in 1 minute 51 seconds T 30 seconds, and last muscle movement in 4 minutes 12 seconds T 2 minutes 29 seconds. The type of suspension and ethanol intoxication does not seem to influence the timing of the agonal responses, whereas ischemic habituation in autoerotic practitioner might decelerate the late responses to hanging. Key Words: hanging, asphyxia, video recording, pathophysiology, human, ethanol (Am J Forensic Med Pathol 2011;32: 104Y107)

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anging is a form of asphyxia characterized by a constriction of the neck by a ligature tightened by the gravitational weight of the body or part of the body.1 Death has traditionally been attributed to 3 possible mechanisms: closure of the blood vessels of the neck, compression of the air passages, and vagal stimulation by pressure on the baroreceptors in the carotid sinuses and the carotid body.2Y4 This explanation of the mechanism of death is largely based on old writings and experimentation from the end of the 19th century and beginning of the 20th.5 Apart from a few animal studies that gave very limited information on the pathophysiology of hanging in human,6 there was slight new development on this issue until the recent studies on filmed hangings by the Working Group on Human Asphyxia.7,8 In a series of 8 filmed hanging, it was demonstrated that all cases demonstrated deep rhythmic abdominal respiratory movements.8 These respiratory movements were not only visuManuscript received June 7, 2010; accepted June 22, 2010. From the *Office of the Chief Medical Examiner, Edmonton, Alberta, Canada; †Centre Universitaire Romand de Me´decine Le´galeVSite Gene`ve, Unite´ de Me´decine Forensique, Geneva, Switzerland; ‡Regional Forensic Pathology Unit, Hamilton General Hospital, Hamilton, Ontario, Canada; §Office of the Chief Medical Examiner, Calgary, Alberta, Canada; ¶Office of the Chief Medical Examiner, Jamaica, NY; ||School of Criminology, Faculty of Arts and Sciences, University of Montre´al and Montreal Philippe-Pinel Institute, Montreal, Quebec, Canada; and **P.H.I. Investigative Consultant Inc, Garnerville, NY. Reprints: Anny Sauvageau, MD, MSc, Office of the Chief Medical Examiner, 7007, 116 St, Edmonton, Alberta T6H 5R8, Canada. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0104 DOI: 10.1097/PAF.0b013e3181efba3a

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alized but were also clearly audible. This fact strongly challenges the theory of the obstruction of the air passage as a mechanism of death in hanging. It could be argued, however, that hearing breath sounds does not eliminate the possibility of a partial airway obstruction. Although it is now clear that tracheal occlusion is not complete in some hangings, it would be premature to totally exclude some implication of partial airways obstruction in the mechanism of death in all hangings. Besides the presence of clear audible respiration in some cases, the study of filmed hangings has also documented the sequence of agonal responses in these deaths8: a rapid loss of consciousness after 8 to 18 seconds, closely followed by convulsions at 10 to 19 seconds, then a complex pattern of decerebrate rigidity and decorticate rigidity, a loss of muscle tone after 1 minute 38 seconds to 2 minute 15 seconds, and isolated body movements until the last movements between 1 minute 2 seconds and 7 minute 31 seconds. The description of this agonal sequence constitutes a major advance in the understanding of the pathophysiology of human hanging. Nevertheless, additional cases are needed before we can pretend to fully grasp the agonic sequence in hanging deaths and appreciate its variability. This fact was recently emphasized by the report of an unusual case of hanging without decerebrate or decorticate rigidity.9 In this film of a hanging with complete suspension of the body, a 52-year-old man stepped off a stool and the movement of the body stepping off the stool created a rotary movement around the ceiling_s ring. Apart from the rolling around the ceiling_s ring, the body stayed motionless for the duration of the movie, without any evidence of decerebrate or decorticate rigidity. A possible elucidation of this singularity was proposed: the particular revolving movement of the body around the ceiling_s ring created a vestibular stimulation that interfered with the development of the decerebrate rigidity.9 Here we present 5 additional filmed hangings, raising the number of filmed hangings studied to 14.

MATERIALS AND METHODS For each video, we evaluated the time frame of the following body responses: loss of consciousness, convulsions, decorticate rigidity, decerebrate rigidity, loss of muscle tone, last muscle movement, and respiratory responses. All recording were evaluated jointly by at least 2 judges, one of the judges having seen all the videos.

RESULTS The Working Group on Human Asphyxia has compiled and analyzed 14 filmed hangings: 9 autoerotic accidents, 4 suicides, and 1 homicide. All victims were adults. Most were white males, with the exception of an Asiatic male (case 9) and a white female (case 11). A brief description of each case and the observed agonal sequence are presented in Table 1. The time to the various Am J Forensic Med Pathol

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Autoerotic

Suicide

8

9‡

Homicide||

Autoerotic

7

12¶

Autoerotic

6

Suicide

Autoerotic

5

11

Autoerotic Suicide

3 4*

Autoerotic

Autoerotic

2

Toxicology

No intoxication

Nd

Nd

Nd

No intoxication No intoxication

No intoxication

No intoxication

Ethanol 10 mg/100 mL in the femoral blood Seems incomplete; No intoxication feet probably on the ground Incomplete; feet No intoxication on the ground Incomplete, feet Ethanol on the ground 156 mg/100 mL in the femoral blood**; THC 6.5 ng/mL in the femoral blood

Incomplete; Feet on the ground Incomplete; feet on the ground Complete Incomplete; kneeling on the ground Incomplete; almost completely lying down in a prone position Incomplete; feet on the ground Incomplete, feet on the ground Incomplete; feet on the ground Complete

9s

8s

8s

Nd

12 s

10 s

8s

10 s

18 s Nd

Nd

13 s

Nd

11 s

12 s

Nd

14 s

10 s

11 s

13 s

19 s 18 s

14 s

15 s

Nd

43 s

Nd§ 16 s

24 s

V

31 s

26 s

33 s

59 s

1 min 00 s Nd

1 min 08 s

21 s

20 s

V

20 s

11 s

31 s

1 min 19 s

21 s Nd

19 s

19 s

Nd

57 s

39 s (and 1 min 55 s)

V

Nd

1 min 25 s

2 min 45 s

V

Nd

16 s

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Nd

End

Nd

1 min 15 s

2 min 37 s

Nd

Nd†

Nd†

1 min 02 s

2 min 05 s

2 min 04 s Nd

2 min 03 s

2 min 00 s

(Continued on next page)

Nd

3 min 15 s 32 s

7 min 35 s 16 s

V

Nd†

Nd† V

13 s

1 min 02 s 19 s Nd†

V

V

7 min 31 s 13 s

Nd†

1 min 52 s

V

3 min 01 s 22 s Nd 24 s

2 min 47 s 21 s

4 min 10 s 20 s

Last Muscle Movement Start

34 s

2 min 04 s Nd

2 min 15 s

1 min 38 s

Loss of Muscle Tone

1 min 04 s Nd

1 min 32 s

1 min 11 s

Decorticate Rigidity 2 (and 3)

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Suicide

Loss of Decerebrate Decorticate Consciousness Convulsions Rigidity Rigidity 1

Movement Responses

Respiratory Responses (Very Deep Respiratory Attempt)

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1

No. Circumstances

Type of Suspension

TABLE 1. Agonal Responses in 14 Filmed Hangings

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*The film obtained from a surveillance camera was not of optimal quality and several responses are difficult to assess. † A few copies of films have been cut to early to allow evaluation of the late responses. ‡ There was no decerebrate or decorticate rigidities in this case (the case was published as a case report,9). § At the beginning of the hanging, both arms are bent with the fingers slide between the ligature and the neck. The decerebrate rigidity is not seen probably because of this restriction limb movement. Later, the right fingers slip from the ligature and decorticate rigidity is seen. ¶ Several body responses are difficult to assess because the victim is in the shadow. || An erotic asphyxia practitioner asked for the help of his spouse in his practice. He was hanging himself and indicating her when to stop the process. On a filmed hanging, she was seen to ignore his sign to stop the hanging and let him die. **The victim is seen consuming several beers at the beginning of the film, before the hanging. †† The respiratory attempt are seen but the timing was difficult to assess because of the angle of the camera. Nd indicates no data; V, not observed.

1 min 43 s Nd†† 17 s Nd†† Nd Nd† 1 min 53 s 1 min 42 s 50 s (and 57 s) 45 s (and 53 s) 39 s 35 s 22 s 14 s 15 s 11 s Complete Incomplete, feet on the ground Autoerotic Autoerotic 13 14

No. Circumstances

TABLE 1. (Continued)

Type of Suspension

Nd Nd

Toxicology

10 s 8s

End Last Muscle Movement Start Decorticate Rigidity 2 (and 3) Decerebrate Decorticate Convulsions Rigidity Rigidity 1 Loss of Consciousness

Movement Responses

Loss of Muscle Tone

Respiratory Responses (Very Deep Respiratory Attempt)

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responses is assessed considering time zero to represent the onset of the final hanging. In case 14, however, the victim tied the ligature very tightly 2 seconds before the hanging and in this case, the time estimates were done considering time 0 to be the tightening of the ligature. Loss of consciousness was largely assessed by a close examination of the victim_s face, voluntary movements, and body tonus. In 3 cases (cases 2, 4, and 9), loss of consciousness was not possible to evaluate: in case 2, the victim_s face was masked with underwear; in case 4, image quality from the surveillance camera was not optimal enough to estimate this issue adequately; in case 9, the onset of the loss of consciousness and of convulsions was not clearly identifiable. In all the other cases, a rapid loss of consciousness was observed in 8 to 18 seconds (average, 10 T 3 seconds). The loss of consciousness was closely followed by mild generalized, tonic-clonic convulsions in 10 to 19 seconds (average, 14 T 3 seconds). Decerebrate rigidity then followed. This postural attitude of marked extensor rigidity is characterized by a full extension of the upper and lower limbs, with extension of the hips and knees, adduction of the legs, internal rotation of the shoulders, extension of the elbows, hyperpronation of the distal parts of the upper limbs with finger extension at the metacarpophalangeal joints, and flexion at the interphalangeal joints. This extensor posturing was observed in 11 seconds to 1 minute 19 seconds (average, 25 T 19 seconds). If we exclude the only case in which decorticate rigidity preceded decerebrate rigidity (case 5), the posturing occurred in an average of 19 T 5 seconds. After the decerebrate rigidity, a decorticate rigidity occurred: this postural attitude is characterized by marked extensor rigidity of the legs, identical to the one observed in decerebrate rigidity, but combined with rigidity of the flexors of the arms: the arms are flexed and bent on the chest, with the hands clenched into fists. A first phase of decorticate rigidity was relatively sudden and quick. It was generally followed by a second and sometimes a third phases of decorticate rigidity, these subsequent ones developing more slowly and being more sustained. The first decorticate rigidity appeared in 21 seconds to 1 minute 8 seconds (average, 40 T 16 seconds). If we exclude case 5, the posturing first begins in an average of 38 T 15 seconds. Between 1 minute 38 seconds and 2 minutes 45 seconds (average, 1 minute 17 seconds T 25 seconds), the body lost its muscle tone and became progressively flaccid. Subsequently, isolated body movements were observed from time to time, the last one occurring between 1 minute 2 seconds and 7 minutes 35 seconds (average, 4 minutes 12 seconds T 2 minutes 29 seconds). As for the respiratory responses, deep rhythmic abdominal respiratory movements were seen These respiratory movements, with rhythmic rocking of the body by the contraction of the TABLE 2. Agonal Sequence in Hanging Average Time Loss of consciousness Convulsions Decerebrate rigidity Stat of deep rhythmic abdominal respiratory movements Decorticate rigidity Loss of muscle tone End of deep rhythmic abdominal respiratory movements Last muscle movement

10 T 3 s 14 T 3 s 19 T 5 s 19 T 5 s 38 T 15 s 1 min 17 s T 25 s 1 min 51 s T 30 s 4 min 12 s T 2 min 29 s

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diaphragm, started between 13 and 32 seconds (average, 19 T 5 seconds) and stopped between 1 minute 2 seconds and 2 minutes 37 seconds (average, 1 minute 51 seconds T 30 seconds). It is worth emphasizing that these respiratory movements were not only seen but also heard when sound was available, confirming the passage of air in the airways despite the hanging process.

DISCUSSION Despite the great diversity of hangings included in this study, the similarity between most cases is striking. The agonic sequence observed in hanging is summarized in Table 2. This study provides a comprehensive portrait of the pathophysiology of human hanging.

The Role of the Type of Suspension on the Timing of Agonal Responses A comparison of time delay for agonal responses in complete suspension (cases 3 and 13) and incomplete suspension (cases 1Y2, 4Y8, 10Y12, 14) do not reveal impressive differences. However, the small number of cases in the complete suspension group precludes statistical analyses. These preliminary results suggest that the type of suspension may not be an important factor in the timing of agonal responses and therefore in the time to irreversible damage and death. Further cases are needed to assess the validity of this observation. In the present study, most cases of incomplete hangings were in an upright position with feet on the ground, with only 1 case of incomplete hanging in a kneeling position (case 4) and one case of incomplete hanging lying down (case 5). By comparing the timing of responses in these cases, there is no evidence that the position of the incomplete suspension interferes with the time delay. Further cases are needed to assess the validity of this preliminary statement. It should be pointed out, however that the only case with an inversion of the sequence of decerebrate and decorticate rigidity is the case in a lying down position (case 5). It is unknown at this time if this position plays a role in this inversion of the sequence.

Agonal Sequences in 14 Filmed Hangings

TABLE 3. Timing of the Agonal Responses: Comparison of Autoerotic Hangings Versus Nonautoerotic Hangings Autoerotic Hangings

Nonautoerotic Hangings

Loss of consciousness 11 T 3 s 10 T 3 s Convulsions 13 T 3 s 15 T 4 s Decerebrate rigidity 20 T 6 s 18 T 2 s Stat of deep rhythmic 17 T 3 s* 25 T 6 s* abdominal respiratory movements Decorticate rigidity 40 T 16 s 32 T 16 s Loss of muscle tone 2 min 5 s T 23 s* 1 min 31 s T 9 s* End of deep rhythmic 1 min 56 s T 31 s 1 min 38 s T 32 s abdominal respiratory movements Last muscle 4 min 23 s T 2 min 59 s 3 min 42 s T 39 s movement *Comparisons between both groups using Mann-Whitney U were significant at P G 0.05.

victim, alleging that ethanol is a respiratory depressant. We could not find any animal or human studies to support or refute this theory. In the present study, 1 victim was intoxicated with ethanol (case 12). This intoxication state does not seem to have accelerated the timing of agonal responses. It would be interesting to further evaluate the effect of ethanol on the timing of agonal responses to hanging on the animal model of hanging previously proposed by Boghossian et al.6 REFERENCES 1. Sauvageau A, Boghossian E. Classification of asphyxia: the need for standardization. J Forensic Sci. 2010;55:1259Y1267.

The Role of Ischemic Habituation on the Timing of Agonal Responses

2. DiMaio VJ, DiMaio D. Asphyxia Forensic Pathology. 2nd ed. Boca Raton, FL: CRC Press; 2001:229Y277.

Considering that autoerotic practitioners might develop over time a certain ischemic habituation, it is theoretically possible that these cases present a deceleration of the sequence. In contrast, as they often play for a longer period with the hanging process before the final hanging, it could be argue that on the contrary, their hanging sequence will be accelerated. A comparison of the timing of agonal responses in autoerotic hangings versus nonautoerotic hangings is presented in Table 3. Overall, the time delays for the early responses to hanging seem to be relatively similar between both groups, with the exception of an accelerated start of deep abdominal respiratory movements in the autoerotic practitioners. As for the late responses to hanging, they seem to be decelerated in autoerotic practitioners. Statistical analysis confirmed a significant difference between both groups for 2 variables: the start of the deep abdominal respiratory abdominal movement occurred significantly faster in autoerotic practitioner whereas the loss of muscle tone was significantly delayed. Further research is needed to determine whether and under which circumstances ischemic habituation plays a role on the agonal sequences.

3. Spitz WU. Asphyxia. In: Spitz WU, Spitz DJ, eds. Spitz and Fisher_s Medicolegal Investigation of Death: Guidelines for the Application of Pathology to Crime Investigation. 4th ed. Springfield, IL: Charles C Thomas Publisher LTD; 2006:783Y845.

The Role of Ethanol Intoxication on the Timing of Agonal Responses An expert-witness recently stated that a victim intoxicated by ethanol will die more quickly from strangulation than a sober * 2011 Lippincott Williams & Wilkins

Copyright © 2011 by the American Psychosomatic Society.

4. Saukko P, Knight B. Suffocation and BAsphyxia.[ In: Saukko P, Knight B, eds. Knight_s Forensic Pathology. 3rd ed. London, England: Arnold Publishers; 2004:352Y367. 5. Clement R, Redpath M, Sauvageau A. Mechanism of death in hanging: a historical review of the evolution of pathophysiological hypotheses. J Forensic Sci. 2010;55:1268Y1271. 6. Boghossian E, Clement R, Sauvageau A. Respiratory, circulatory and neurological responses to asphyxia by hanging: a review of animal models. J Forensic Sci. In press. 7. Sauvageau A. Agonal sequences in four filmed hangings: analysis of respiratory and movement responses to asphyxia by hanging. J Forensic Sci. 2009;54:192Y194. 8. Sauvageau A, LaHarpe R, Geberth VJ; The Working Group on Human Asphyxia. Agonal sequences in eight filmed hangings: analysis of respiratory and movement responses to asphyxia by hanging. J Forensic Sci. 2010;55:1278Y1281. 9. Sauvageau A, Kelly S, Ambrosi C. A filmed hanging without decerebrate and decorticate rigidity: a case report and pathophysiological considerations. Am J Forensic Med Pathol. In press.

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ORIGINAL ARTICLE

What Is the Lethal Concentration of Hydrocodone? A Comparison of Postmortem Hydrocodone Concentrations in Lethal and Incidental Intoxications D. Kimberley Molina, MD and Veronica M. Hargrove, MS, FTS-ABFT

Abstract: Hydrocodone is a semisynthetic opioid medication that is widely used as an analgesic and antitussive. Since 2004 it has been the most commonly prescribed drug in the United States and is often misused as a drug of abuse. Hydrocodone is frequently encountered in the postmortem setting, both as a cause of death and incidentally. Unfortunately, information regarding the concentrations of hydrocodone found with chronic high-dose use is lacking, and interpretation of postmortem concentrations can be difficult. A retrospective review of postmortem and BDriving under the Influence[ (DUI) cases in Bexar County Texas in which hydrocodone was present was conducted. The cases were included in the study if they fit the criteria of belonging to 1 of 3 categories: the hydrocodone either caused or was the main contributor to death; the hydrocodone was incidental and definitively did not cause or contribute to death; and the DUI cases. The average hydrocodone concentration in the cases where the hydrocodone caused death was 0.47 mg/L (median, 0.38 mg/L). The average hydrocodone concentration in cases where it was incidental to death was 0.15 mg/L (median, 0.08 mg/L). The average hydrocodone concentration in the DUI cases was 0.09 mg/L (median, 0.08 mg/L). Analysis showed the possibility of postmortem redistribution as well as significant overlap of the concentrations noted in the different groups. Given that no definitive lethal concentration could be delineated, it is recommended that each hydrocodone case encountered be assessed individually to include a thorough medical record review to accurately interpret hydrocodone concentrations. It has also been shown that concentrations as high as 0.3 mg/L peripherally and 1.4 mg/L centrally can be present and not result in death. In addition, further research into hydrocodone concentrations with chronic use and hydrocodone metabolism is necessary. Key Words: forensic toxicology, hydrocodone, hydromorphone, fatal, lethal, death (Am J Forensic Med Pathol 2011;32: 108Y111)

H

ydrocodone is a semisynthetic opioid first derived from codeine in the 1920s as an analgesic and antitussive. It shows 2 to 8 times the potency of codeine and is currently a Schedule II medication.1 Hydrocodone is most commonly found in preparations combined with acetaminophen (Vicodin, Norco, Lorcet, and Lortab), although it can also be combined with ibuprofen (Vicoprofen) or guaifenesin (Hycotuss). Since 2004 it has been prescribed more each year than any other medication in the United States.2 It is widely used to treat both acute and chronic pain as well as being commonly misused as a drug of abuse.

Manuscript received February 25, 2010; accepted March 9, 2010. From the Bexar County Medical Examiner’s Office, San Antonio, TX. Reprints: D. Kimberley Molina, MD, Bexar County Medical Examiner’s Office, 7337 Louis Pasteur, San Antonio, TX. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0108 DOI: 10.1097/PAF.0b013e3181dd5a75

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Hydrocodone has a volume of distribution of 3.3 to 4.7 L/kg and a half-life of 3.5 to 6.2 hours.1,3,4 Peak concentrations, averaging 0.02 to 0.05 mg/L, are achieved 60 to 100 minutes after acute dosing.1,3 Hydrocodone is metabolized by the CYP450 system and is a minor metabolite of codeine, although it is often seen only in urine after codeine use. The main active metabolite of hydrocodone, hydromorphone, is created via CYP2D6 by O-demethylation of the parent molecule. Hydromorphone has been shown to have an approximately 30 times greater affinity for the K-opioid receptor than hydrocodone.5 Norhydrocodone is the other major metabolite of hydrocodone and its creation though N-demethylation is catalyzed by CYP3A4. Approximately 40% of hydrocodone is metabolized through other pathways including reduction at the 6-keto position and fecal, biliary, intestinal, and renal elimination.5 Unfortunately, even though hydrocodone use is so prevalent, data regarding its pharmacokinetic properties with chronic use are lacking. Many clinicians do not consider hydrocodone tolerance a concern since they feel acetaminophen is the doselimiting component of long term hydrocodone use (Eckmann M, personal communication, August 18, 2009). Ackermann and Ahmad studying the effects of cigarette smoking on hydrocodone concentrations,6 and Jannetto and Bratanow7 reviewing the pharmacogenomics of hydrocodone found hydrocodone concentrations in chronic users to be comparable to those found in the acute setting with concentrations ranging from 0.004 to 0.04 mg/L. Forensic studies, however, have shown that postmortem concentrations can be as high as 2.56 mg/L in individuals where hydrocodone was not considered a factor in the death.8 This conflicting information makes the interpretation of postmortem hydrocodone results difficult. In addition, hydrocodone_s relatively high volume of distribution suggests it could possibly undergo significant postmortem redistribution, making interpretation even more difficult.

MATERIALS AND METHODS A retrospective review was performed to identify all cases in which hydrocodone was detected at the Bexar County Medical Examiners Office (BCMEO) between January 1998 and September 2009. The cases were further reviewed to ascertain those cases where hydrocodone definitely did not cause or contribute to death and those cases where hydrocodone was the cause or main contributor to death. In addition, the BCMEO performs blood testing on suspected BDriving Under the Influence[ cases for the local police agencies, and those cases were reviewed for the presence, and concentration, of hydrocodone. For each case, the concentrations of both hydrocodone and acetaminophen were analyzed. The source of each sample was categorized as central (heart or subclavian), peripheral (femoral), cavity, and unknown. The data analysis performed regarding the specimen source compared only known peripheral versus central samples as defined; the unknown and cavity samples as well as any potentially contaminated specimens were not included in the Am J Forensic Med Pathol

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TABLE 1. Summary of Hydrocodone Concentrations in Cases Where Hydrocodone Caused or Was Main Contributor to Death (Group 1)

No. cases Average Median Range

Lethal Concentration of Hydrocodone

TABLE 3. Summary of Causes of Death in Cases Where Hydrocodone Did Not Cause or Contribute to Death (Group 2)

All Cases

Peripheral Blood

Central Blood

Cause of Death

39 0.47 mg/L 0.38 mg/L 0.07Y2.1 mg/L

24 0.49 mg/L 0.39 mg/L 0.14Y0.32 mg/L

11 0.42 mg/L 0.29 mg/L 0.07Y0.9 mg/L

Gunshot wound(s) Blunt force injuries Stab wounds Other Total cases

All cases = peripheral, central, cavity, and unknown sample sites; peripheral = femoral; central = heart and subclavian sample sites.

analysis. Statistical analysis was performed using the MannWhitney U test.

RESULTS A total of 97 medical examiner cases and 16 driving under the influence cases were identified that met inclusion parameters for the study. Of these, 39 cases were found where hydrocodone was believed to have either caused or have been the main contributor of death and 58 cases were found where hydrocodone was present but was believed to not have caused or contributed to death. A detailed summary of the case types follows.

Group 1: Hydrocodone Caused or Was Main Contributor to Death There were a total of 39 cases found which met the criteria that hydrocodone either caused or was the main contributor to death. The average hydrocodone concentration was 0.47 mg/L (median, 0.38 mg/L; range, 0.07Y2.1 mg/L). The average acetaminophen concentration was 60.3 mg/L (median, 37.9 mg/L; range, 0Y311.5 mg/L). The majority (75%) of cases had hydrocodone concentrations greater than 0.07 mg/L. The central and peripheral blood concentrations did not show a statistically significant difference (Table 1). In 32 cases (82%), at least one additional drug, other than acetaminophen, was present and in 15 cases (38.5%) two or more drugs were present. In only three cases, however, was the other drug present at a significant enough concentration that it was believed to contribute to death. In all three cases, the additional drug present was ethanol and the concentrations ranged from 0.15 to 0.26 g/dL. The prevalence of the other drugs found is summarized in Table 2. Anxiolytics and antidepressants were the most common drug types found in combination with hydrocodone, followed by antihistamines and ethanol.

TABLE 2. Type and Frequency of Other Drugs Found in Cases Where Hydrocodone Caused or Was Main Contributor to Death (Group 1) Type of Drug Antidepressant Anxiolytic Antihistamine Ethanol Opiate/opioid (not hydrocodone) Cardiac Stimulant/sympathomimetic Other

No. Cases (% of Cases) 18 (46%) 17 (44%) 5 (13%) 5 (13%) 2 (5%) 1 (3%) 1 (3%) 4 (10%)

No. Cases 32 19 3 4 58

Seven cases (18%) had no other drugs present. In these cases, the average hydrocodone concentration was 0.46 mg/L (median, 0.53 mg/L; range, 0.19Y0.83 mg/L), with an average acetaminophen concentration of 91.2 mg/L (median, 42 mg/L; range, 0Y311.5 mg/L). Analysis failed to show a statistically significant difference between the hydrocodone concentrations in the Bpure[ cases versus those with other drugs present (P = 0.96).

Group 2: Hydrocodone Did Not Cause or Contribute to Death There were a total of 58 cases found in which hydrocodone was present but did not cause or contribute to death. A summary of the causes of death in these cases is shown in Table 3. Gunshot wounds were the most common cause of death, followed by blunt force injuries. Stab wounds, pulmonary emboli, cardiac tamponade (2 cases), and dissecting aortic aneurysm accounted for the remaining cases. The hydrocodone concentrations found in cases where the hydrocodone did not cause or contribute to death is summarized in Table 4. The average hydrocodone concentration was 0.15 mg/L (median, 0.08 mg/L; range, 0.02Y1.4 mg/L). The average acetaminophen concentration was 18.7 mg/L (median, 14.7 mg/L; range, 0Y112.8 mg/L). The majority (75%) of cases had hydrocodone concentrations less than 0.16 mg/L. Statistical analysis showed a significant difference between the peripheral and central blood hydrocodone concentrations within this group (P = 0.01). In 49 cases (84.5%), at least one additional drug, besides acetaminophen, was present and in 25 cases (43%) two or more drugs were present. The prevalence of the other drugs found is summarized in Table 5. Anxiolytics, antidepressants, and other opiates/opioids were the most common drug types found in combination with hydrocodone, followed by stimulants/ sympathomimetics and ethanol. Eight cases (14%) had no other drugs present. In these cases, the average hydrocodone concentration was 0.12 mg/L (median, 0.08 mg/L; range, 0.02Y0.33 mg/L). Accurate analysis

TABLE 4. Summary of Hydrocodone Concentrations in Cases Where Hydrocodone Did Not Cause or Contribute to Death (Group 2)

No. cases Average Median Range

All Cases

Peripheral Blood

Central Blood

58 0.15 mg/L 0.08 mg/L 0.02Y1.4 mg/L

17 0.08 mg/L 0.06 mg/L 0.02Y0.32 mg/L

36 0.19 mg/L 0.1 mg/L 0.03Y1.4 mg/L

All cases = peripheral, central, cavity, and unknown sample sites; peripheral = femoral; central = heart and subclavian sample sites.

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Copyright © 2011 by the American Psychosomatic Society.

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TABLE 5. Type and Frequency of Other Drugs Found in Cases Where Hydrocodone Did Not Cause or Contribute to Death (Group 2) Type of Drug

No. Cases (% of Cases)

Anxiolytic Opiate/opioid (not hydrocodone) Antidepressant Ethanol Stimulant/sympathomimetic Antihistamine Cardiac Other

21 (36%) 15 (26%) 13 (22%) 13 (22%) 10 (17%) 7 (12%) 2 (3%) 4 (7%)

regarding the acetaminophen concentrations in these cases could not be performed. In two cases, acetaminophen was not detected. In one case, testing for acetaminophen was not performed. In four cases acetaminophen was present but not quantified and in one case the concentration was found to be 11.4 mg/L. Analysis failed to show a statistically significant difference between the hydrocodone concentrations in the Bpure[ cases versus those with other drugs present (P = 0.64).

Group 3: DUI Cases Review of the DUI cases performed at the BCMEO revealed 16 cases where hydrocodone was present. The hydrocodone concentration data are summarized in Table 6. The average hydrocodone concentration was 0.09 mg/L (median, 0.08 mg/L; range, 0.03Y0.17 mg/L). Unfortunately, the presence or absence of other drugs could not be analyzed for this group because full toxicologic screening was not necessarily performed on every case. However, in no case where full toxicology was performed was hydrocodone the only drug present (ie, additional intoxicants were always present when testing was performed).

Comparison of Groups Statistical analysis showed a significant difference between the hydrocodone concentrations of group 1 when compared with both groups 2 and 3 (P G 0.001). Analysis also showed a significant difference between the acetaminophen concentrations between group 1 when compared with groups 2 and 3 (P G 0.001). Analysis comparing the hydrocodone concentrations of groups 2 and 3 failed to show a significant difference (P = 0.49).

DISCUSSION As stated previously, hydrocodone concentrations are believed to be of little use in the clinical setting, as the usefulness of high-dose hydrocodone therapy is considered to be limited by the acetaminophen component. However, in the forensic setting, elevated concentrations of hydrocodone are often found in cases of traumatic death where hydrocodone could not have contributed to death. In this study, the median hydrocodone concentration found in traumatic deaths, 0.08 mg/L, was 12 times greater than the upper limit of the therapeutic range for hydrocodone. This leaves the forensic pathologist questioning how then should elevated hydrocodone concentrations be interpreted. This study highlights that the specimen source is one variable which may affect interpretation. Hydrocodone may undergo significant postmortem redistribution as evidenced by the statistically significant difference between the central and peripheral blood concentrations in group 2. Although this same finding was not evident in group 1, it may have been a result of the small number of centrally drawn samples in this group.

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Both this study and previous studies have shown considerable overlap between hydrocodone concentrations that cause death and those where it did not contribute. This study found an average and median concentration of hydrocodone in cases where the hydrocodone caused death to be 0.47 and 0.38 mg/L, respectively, with a range of 0.07 to 2.1 mg/L. This is consistent with Spillers study where he found, in 17 individuals dying from intoxication with hydrocodone, the average hydrocodone concentration to be 0.53 mg/L with a median of 0.4 mg/L and a range of 0.12 to 1.6 mg/L.9 He also found that the majority of cases (65%) had hydrocodone concentrations greater than or equal to 0.5 mg/L,9 which is significantly higher than the 0.07 mg/L majority found in this study. Baker and Jenkins (2008), in their study addressing postmortem hydrocodone concentrations, reviewed 54 cases where hydrocodone caused or contributed to death and found that hydrocodone concentrations ranged from 0.012 to 1.66 mg/L with 42% of cases being 90.2 mg/L.8 In addition, they had seven cases where no other drugs were present, and the concentration of hydrocodone ranged from 0.07 to 1.66 mg/L,8 a broader range than that seen in this study. For cases where hydrocodone neither caused nor contributed to death, this study found an average hydrocodone concentration of 0.15 mg/L with a median of 0.08 mg/L and a range of 0.02 to 1.4 mg/L. This is comparable to the study performed by Baker and Jenkins that analyzed 115 cases where hydrocodone was present incidentally and was not believed to cause death.8 In their study, the mean hydrocodone concentration was 0.09 mg/L with a range from 0.01 to 2.56 mg/L.8 Baker and Jenkins also reported that 20 cases had concentrations 90.2 mg/L and 2 cases had concentrations 91 mg/L.8 In this study, 25 cases were Q0.1 mg/L and 12 were 90.2 mg/L. Hydrocodone is metabolized by the CYP450 enzyme system, specifically 2D6 and 3A4. Both of these enzymes have shown genetic variability which can affect the metabolizer status of an individual (ie, poor vs. extensive metabolizers). Poor metabolizers may develop higher concentrations of hydrocodone when taken chronically allowing for tolerance to develop and a relative resistance to these concentrations. In addition, extensive metabolizers may create increased concentrations of hydromorphone, which has been shown to have greater activity than hydrocodone, resulting in death at decreased hydrocodone concentrations. Otton et al4 and Jannetto and Bratanow7 have both studied the issue of hydrocodone metabolizer status as it pertains to CYP2D6. Jannetto and Bratanow found no significant difference in the hydrocodone concentrations of extensive and intermediate metabolizers but the data was limited (only four extensive metabolizers, three intermediate, and no poor metabolizers) and markedly skewed.7 Like Janetto and Bratanow, Otton et al failed to find a significant difference between hydrocodone concentrations of extensive versus poor metabolizers, although, a significant difference between the hydromorphone concentrations was found.4 However, Otton et al_s study was again limited by number (only five extensive metabolizers and

TABLE 6. Summary of Hydrocodone Concentrations in DUI Cases (Group 3) DUI Cases No. cases Average Median Range

16 0.09 mg/L 0.08 mg/L 0.03Y0.17 mg/L

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six poor metabolizers) and the data analysis was performed using a method which appears to have been inappropriate for the data given. This study, in combination with both Spillers, and Baker and Jenkins, illustrates the variability in postmortem hydrocodone concentrations and the overlap between those concentrations which may result in death and those which may not. This study has shown that concentrations of hydrocodone can be as high as 1.4 mg/L centrally and 0.32 mg/L peripherally and not cause death. Concentrations as high as 0.17 mg/L were also seen in individuals operating motor vehicles, although how well the vehicle was being operated is not known. In the majority of cases where the hydrocodone resulted in death, concentrations were 90.1 mg/L; although, 42% of cases where hydrocodone did not cause death had concentrations Q0.1 mg/L. Thus, a thorough death investigation including a complete autopsy and review of the decedent_s medical history should be undertaken before interpreting the significance of hydrocodone concentrations and determining whether hydrocodone caused or contributed to death. In addition, further research should be conducted into the possible role of pharmacogenetics in this variability. REFERENCES 1. Physician_s Desk Reference. 61st ed. Montvale, NJ: Thomson PDR; 2007:535Y536.

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Lethal Concentration of Hydrocodone

2. IMS Health. Top-line Industry Data: 2008 US Sales and Prescription Information. IMS Health Web site. Available at: http://www.imshealth.com/portal/site/imshealth/menuitem. a46c6d4df3db4b3d88f611019418c22a/?vgnextoid= 85f4a56216a10210VgnVCM100000ed152ca2RCRD&cpsextcurrchannel=1. Accessed 3 December, 2009. 3. Barnhart JW, Caldwell WJ. Gas chromatographic determination of hydrocodone in serum. J Chromatogr. 1977;130:243Y249. 4. Otton SV, Schadel M, Cheung SW, et al. CYP2D6 phenotype determines the metabolic conversion of hydrocodone to hydromorphone. Clin Pharmacol Ther. 1993;54:463Y472. 5. Hutchinson MR, Menelaou A, Foster DJ, et al. CYP2D6 and CYP3A4 involvement in the primary oxidative metabolism of hydrocodone by human microsomes. Br J Clin Pharmacol. 2003;57:287Y297. 6. Ackerman W, Ahmad M. Effect of cigarette smoking on serum hydrocodone levels in chronic pain patients. J Ark Med Soc. 2007;104:19Y21. 7. Jannetto PJ, Bratanow NC. Utilization of pharmacogenomics and therapeutic drug monitoring for opioid pain management. Pharmacogenomics. 2009;10:1157Y1167. 8. Baker DD, Jenkins AJ. A comparison of methadone, oxycodone and hydrocodone related deaths in northeast Ohio. J Anal Toxicol. 2008;32:165Y171. 9. Spiller HA. Postmortem oxycodone and hydrocodone blood concentrations. J Forensic Sci. 2003;48:429Y431.

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ORIGINAL ARTICLE

Advancement in the Examination of the Human Cardiac Sinus Node An Unexpected Architecture and a Novel Cell Type Could Interest the Forensic Science Tiziana Balbi, MD,* Claudio Ghimenton, MD,Þ Gianandrea Pasquinelli, MD,* Laura Foroni, PhD,þ Marco Grillini, BD,§ and Giovanni Pierini, BD§

Abstract: We have investigated the morphology of the sinus node of the human cardiac conduction system. Until today the sinus node (SN) is described as a heterogeneous system composed of 2 types of cells, namely, P or pale and Tor transitional cells which are immersed in the matrix around the sinus nodal artery. T cells are said to share characteristics of P cells and of peripheral working atrial myocardial cells. This study was carried out on autoptic and explanted specimens using histochemical, immunohistochemical, and electron microscopic methods. Our investigations show that SN tissue has a quite different cellular composition, ie, spherical and/or star-shaped cells organized in clusters with long cytoplasmic processes (type P), transitional cells, similar to myocytes but with a reduced number of sarcomeres (type T) and, finally, as yet not described in the literature, fibroblast-like cells with long bitripolar extensions contacting cells. Interestingly, SN is squared by connective and elastic fibers geometrically arranged. Immunohistochemistry shows that the 3 cell types of the SN node express mesenchymal markers revelatory of their embryological origin. Innervation appears to be more complex than previously thought; we identified a system of synaptophysin-positive cholinergic vesicles dependent on the sympathetic system and parasympathetic fibers expressing S100 protein. Overall results indicate that the SN has an unexpected, systematic architecture. Key Words: sinus node, forensic sciences, scanning and transmission electron microscopy (Am J Forensic Med Pathol 2011;32: 112Y118)

O

ur research was aimed at the in-depth study of the morphology of the sinus node (SN), or the Keith-Flack node, in the human cardiac conduction system. The SN is a 1 to 2 cm long cigar-shaped structure in the subepicardium of the right atrium, posterior to the terminal crest and lateral to the superior vena cava ostium (sulcus terminalis),1,2 even though a variability in its location has been described.3 The

Manuscript received February 14, 2009; accepted June 24, 2009. From the *Institute of Surgical Pathology, S. Orsola-Malpighi Hospital, Bologna; †Department of Pathology, Borgo Trento Hospital, Verona; ‡Department of Anestesiological and Specialistic Surgical Sciences, University of Bologna; and §Legal Medicine Institute, University of Bologna, Bologna, Italy. Our research was conducted in the year 2008 at Department of Legal Medicine, Bologna University, Italy, without grants or fundings from National Institute of Health (NIH), Wellcom Trust; Howard Hughes Medical Institute (HHMI), and other public or private institutions. Reprints: Giovanni Pierini, BD, Department of Legal Medicine, Via Irnerio 49, 40126 Bologna, Italy. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0112 DOI: 10.1097/PAF.0b013e3181ce9f23

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nodal artery which originates from both the right and the left coronary arteries in approximately equal percentages passes through the center of the SN, in some cases eccentric to this location.4 A disproportion between the dimensions of the artery and the tissue mass of the SN has also been hypothesized, leading us to hypothesize aspects of superior functionality different from those which are only nutritional.5 Over the course of many years, scientific research has been aimed towards the detailed study of the anatomy and the morphologic and pathologic variants of the atrioventricular conduction system. However, not the same can be said of the SN, described by many authors as adjacent to the artery of the SN3 and made up of a zonal representation of pale cells (or P cells) and by other transitional cells towards the working muscles of the contractile tissue (T cells, idem). The P cells are described as spherical, with long cytoplasmatic extensions, and grouped in clusters without specific intercellular junctions while those of the transitional type are more similar to cardiac cells and are more frequently found towards the periphery of the SN and at times outside it. Both cellular types appear Bpale[ with respect to the muscular tissue of the atrium.6 The aspect of the P cells has also been described as primitive and/or embryonal.7,8 The variability of the morphology of the SN and its random distribution is considered essential by many authors for the functionality of the depolarization signal which is causally restored to the autonomous depolarization of pacemaker cells.9 Some authors propose the introduction of a third cellular type isolated in the matrix and similar to a mature myocyte.8 With respect to the innervation of the SN, the prevalent supply is the parasympathetic system (nervous fibers and ganglia of the vagus) while there is doubt as to whether there is also a sympathetic adrenergic component (only observed in mammals). Therefore we carried out studies aimed at investigating the phenotypic expression of cells of the SN, as yet not documented in the literature, thinking, by analogy, of the function of the regulation of motility on the part of the pacemaker cells, well-documented in the gastroenteric tract,10 near the plexus of Auerbach, in the digestive system,11Y13 in the genitourinary tract,14,15 in vascular and lymphatic systems.16 Furthermore, fibroblast-like cells have recently been observed in the adventitia of the aorta, even if their function remains uncertain.17 But the results furnished different and unexpected evidence with respect to the expectations which question regarding the morphology of the tissue of the SN.

MATERIALS AND METHODS Twenty-five autoptic cases in which neither pathologic modifications of the conduction system nor dysplastic modifications of the SN artery were present were chosen. The SN was examined according to the procedure suggested by Gulino3; the Am J Forensic Med Pathol

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FIGURE 1. A, Spherical and/or star-shaped cells (type P) are organized in clusters; the cells have long cytoplasmatic processes (hematoxylin-eosin [HE], 400). B, A type P cell at higher magnification. The toluidine blue stain evidences cytoscheletal filaments (toluidine blue, 800). C, Transitional and immature myoid cells (type T) (HE, 400). D, Fibroblast-like cells with long bipolar extensions (HE, 800).

specimens were sectioned perpendicular to the terminal crest and fixed in FineFix18 (Milestone, Bergamo, Italy) and microwave processed (ATP1, Kaltek, Italy). The tissues were paraffin-embedded. For histology, staining with hematoxylin-eosin and Luxol fast blue was carried out, observations were conducted with direct and polarized light; for histochemistry, toluidine blue and orcein were used (all reagents from Histo-line, Milano, Italy). For immunohistochemistry, c-kit (CD117), vimentin, S100, a-tubulin, synaptophysin, neurofilaments, calretinin, desmin, calcitonin, and Ck AE1-AE3 were tested as were the following neuroendocrine markers: serotonine, somatostatin, chromogranin, and neuronspecific enolase, (all reagents from NBL Int). For scanning electron microscopy (SEM), fixed material was dehydrated in an alcohol-ascending series for preliminary drying, then critical point dried and finally gold-coated (50 A

thickness).19 A SEM Philips 505 equipped with a backscattered detector and digital image recording was used. For transmission electron microscopy (TEM), sinoatrial tissue was carefully recovered from paraffin blocks; the samples were dewaxed in xylene and rehydrated; after fixation with 1% buffered osmium tetroxide (Histo-line, Milano, Italy), the samples were dehydrated in alcohol and embedded in epoxy resin; 60 to 80 nm thick sections were stained with uranyl acetate, lead citrate and examined under a Philips 400T transmission electron microscope (reagents from C.Erba, Milano, Italy).

RESULTS Spherical cells with long cellular processes containing filaments and with an evident nucleus (P cells) were seen around

FIGURE 2. A, Sinus node (SN) architecture. At left the SN artery, elastic fibers geometrically arrange to form contiguous compartments (orceine, 400). B, C, SN architecture. Compartments suggest a structure which is oriented orthogonally (orceine, 450) at the edge of myocyte mature working cells (orceine, 450). Orceine stain highlights the elastic fiber network. * 2011 Lippincott Williams & Wilkins

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FIGURE 3. A, B, Sections parallel to the SN artery. Connective and elastic fibers squared walls, and evidence of twisted connective stuctures (HE, 450). C, Sections transverse to the SN artery. Cross-sectioned ‘‘helical’’ connective structures in respect to the SN artery (Luxol fast blue, 400). Luxol fast blue stain reveals thin elastic fibers (blue stained) in complex cellular matrices (cells are stained in pale red, myocytes in violet). D, Same field seen in polarized light (HE, 250). Polarized light analysis enhances the presence and the twisting of collagen fibers, in bright yellow.

FIGURE 4. A, Immunohistochemistry c-kit (CD117) weak-positive type P cell (immersion oil, 1000). C-kit is a transmembrane protein kinase involved in cell development. B, Immunohistochemistry, SN overview. Lateral working myocytes immunostained by desmin (counterstaining with toluidine blue), in the center immature SN muscular fibers (250). Desmin immunostaining evidences myoid origin of cells. C, Immunohistochemistry of S-100 positive neural fibers, at the bottom the SN node arterial wall (400). S-100 stains parasympathetic fibers. D, Immunohistochemistry of synaptophysin-positive (dot-like) nerve endings contacting a SN muscular cell (400). Synaptophysin stains sympathetic fibers.

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FIGURE 5. A, Immunohistochemistry. Double-immunofluorescence labeling for S-100 and synaptophysin: the simultaneous presence of presynaptic cholinergic vesicles belonging to the parasympathetic system and fibers of the sympathetic system is seen. Green (*mark), S100 positivity; red (+mark) dot-spot synaptophysin positivity (400). B, Immunohistochemistry. Double-immunofluorescence labeling for desmin and synaptophysin: red (+mark), desmin positivity; green (*mark), synaptophysin positivity (500).

the SN artery (Fig. 1, A and B). Thin elongated cells with a myoid aspect (transitional T cells), smaller with respect to the mature atrial myocytes and alternating with the other cell types were also observed (Fig. 1C); in addition to these cell types which have already been described, we identified spindle cells with extremely thin long cytoplasmatic extensions and a needle-shaped hyperchromic nucleus; these cells, resembling fibroblasts, were hereafter called Bfibroblast-like[ cells (Fig. 1D). These cells were immersed in a loose collagen matrix, rich in elastic fibers which showed a nonrandom orientation, suggesting an organization made up of orthogonal layers, as revealed by the orcein stain (Fig. 2, AYC). In sections both transverse and parallel to the SN artery, the connective and elastic bands define quadrangular spaces. P cells, thin muscular T cells, and fibroblast-like cells are located within these connective elastic walls. The walls of the

connective cage intersect at right angles. In the middle of the quadrangular spaces helicoidal structures of connective nature can be seen; interestingly, these structures are regularly twisted in the sections parallel to the SN artery plane, whereas in the transverse sections they appear as circular whirlwinds (Fig. 3, A and B). Moreover, a thin capillary channel was always seen at their center, surrounded by thin elastic fibers (Fig. 3C). This architecture was also evident when samples were analyzed under polarized light (Fig. 3D). The immunohistochemical profile of the P cells demonstrated a weak positivity for c-kit (Fig. 4A) and a constant negativity for neuroendocrine markers, including NSE, serotonin, synaptophysin, somatostatin, chromogranin. Transitional T cells expressed desmin exclusively (Fig. 4B). The fibroblast-like cells were positive for vimentin and negative for desmin thus revealing a primitive mesenchymal nature. Consonant with their connective

FIGURE 6. Scanning electron microscopy. A, SN tissue squared by the walls of the connective and elastic fibers (B, C) type P cells with long cytoplasmatic processes (*) (C) ie, along the SN artery (D) transversal section of cellular processes of a T type cell; (E) fibroblast-like cell; (F) ‘‘helical’’ or twisted connective structures. * 2011 Lippincott Williams & Wilkins

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nature the twisted helicoidal structures were unreactive with all the monoclonal and polyclonal antibodies investigated here. According to the immunohistochemical results SN cells cannot be therefore believed to be a tissue-specific pacemaker cell and hence be considered as a human interstitial cell of Cajal, currently regarded as pacemaker cells of the gastrointestinal tract counterpart. Indeed they were faintly positive to c-kit (CD117) and the neuroendocrine profile was constantly negative. The SN is richly innervated. The innervation is represented by a 2-fold system: a network of positive S100 fibers, seen both in the SN area and in the functioning myocytes (Fig. 4C), and a dot-like immunoreactivity for synaptophysin in the same areas (Fig. 4D). This 2-fold system of SN innervation was shown by double immunofluorescence detection of S100 and synaptophysin which showed the simultaneous presence of presynaptic cholinergic vesicles belonging to the parasympathetic system and fibers of the sympathetic system (Fig. 5, A and B). As described in the TEM section, however, there was no direct con-

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tact between the nervous fibers and the SN cells (P cells, T cells, and myocytes).

Electron Microscopy: SEM At low magnification, the architectural partition of the SN tissue into quadrangular compartments was evident, both along the axis of the SN artery and transversally to it; SEM analysis confirmed that connective and elastic tissue bands outlined the periphery of individual compartment (Fig. 6A). Inside these circumscribed areas, in a more homogeneous matrix rich in small fibers, isolated cells, some with a polygonal shape, with an evident spherical nucleus, a cytoplasm rich in vesicles and thin filaments identifiable as type P were observed (Fig. 6B). The sections parallel to the SN artery were like P cells and had long extensions (Fig. 6C). Moreover, transitional T cells with an elongated nucleus were noted (Fig. 6D). Along the connective partitions, thin fibroblast-like cells, smaller but having thin, long, and elaborated extensions were found (Fig. 6E).

FIGURE 7. Transmission electron microscopy. A, Fibroblast-like cell (*) with thin cytoplasmic processes (**); (B) detail on a thin cell processes contacting a round P cell (arrows); (C) detail on a thin cell process (arrows) interconnecting a T cell with a small capillary (*); (D) at higher magnification the contact between T cell and fibroblast-like cell cytoplasm processes is linked by a thin long-spaced collagen fiber (arrows).

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Inside the compartments delimited by the connective and elastic fibers, the helicoidal structures previously seen at light microscopy were also found: in the sections obtained on a plane transverse to the SN artery, they appeared as concentric spirals of flattened cells, with a thin central capillary channel having a thin ring of elastic fibers. As expected, in the sections longitudinal to the SN artery, these connective structures appeared helicoidal (Fig. 6F); in these fields the regularity of the spiralization was particularly evident (twisting interval of approximately 25 Km).

Electron Microscopy: TEM TEM analysis was focused on the extracellular space of the SN tissue; apart from collagen fibers and elastic lamellae, we observed numerous slender fibroblast-like cells which were characterized by the presence of long, thin, and sinuous bitripolar cytoplasmic processes. The processes which run quite distant from the main cell body (Fig. 7A) characteristically encircled both P cells (Fig. 7B), blood vessels, and transitional T cells (Fig. 7C), which had very few sarcomeres, therefore revealing an immature phenotype. Interestingly, bands of fibrous long spaced collagen of the compact type were seen along the main axis of the cell processes; this unusual type of collagen, which is commonly found in benign growths of supporting nerve cells, was also seen between the surfaces of the fibroblast-like processes and the basal lamina of the transitional cells (Fig. 7D). The intimate relationship between the SN cells and the connective matrix was seen as a direct contact between the P cells basal membrane and the broadband compact type collagen fibers under TEM. The fibroblast-like cells showed clear, empty cytoplasmic zones originally rich, most likely, of glycogen; these cells connected, through elaborated cell projections, the capillary vessels with T cells and broadband compact type connective tissue. Nerve endings were seen; however, no direct connection to either P or T cells was observed.

Advanced Examination of Human Cardiac Sinus Node

DISCUSSION Our observations document the presence of 3 different cellular types in the human SN tissue, delimited into contiguous geometric areas by connective and elastic walls; the walls intersect themselves at right angles, thus designing an ordered architecture in opposition to the precedent vision of SN as a chaotic structure. The cellular population is characterized by 3 type of cells: type P, or Bpale,[ star-shaped and with globular nucleus; type T or Btransitional,[ and a novel type as yet not described in the literature and defined by us, on the basis of their morphology and mesenchymal phenotype, to be fibroblast-like. This novel type is characterized by a hyperchromic nucleus and very long and thin bi-tripolar extensions which are associated with the above described cells and the capillary network, extending to all layers. This type of relationship appears to be supported by broadband dense connective tissue. Moreover, in the spaces delimited by this architecture, we find helicoidal structures of connective tissue, that were oriented parallel to the SN artery plane, centered by thin capillaries and surrounded by thin elastic fiber rings. The particularity of the spiral connective is that it has a constant twisting interval of approximately 25 Km. Overall, the tissue of the SN had immature embryonal type characteristics, also as regards the structure of the connective matrix, even if we are dealing with adult subjects. At immunohistochemistry, the cellular population shows a pattern of reactivity which points to a mesenchymal phenotype for the 3 cellular types. The innervation is both parasympathetic, along the layers which delimit the cells, and sympathetic in the form of a network which also extends towards the areas of the functioning myocytes; however, there is no direct connection to either P or T cellular elements. These findings are consequent to our observations by double immunofluorescence (S100 and synaptophysine), and are the first evidence that the SN also posses a double innervation, as the heart has. In conclusion, our study documents that SN is characterized by a systematic architecture, a double innervation and that a novel cell type is present. Regarding the significance of this architecture, (Fig. 8), even if the various cellular types does not express a specific immunophenotypic pattern, nevertheless they are thought to play an important role as components of a highly systematic, geometric structure, probably with the aim of coordinate complex activities, such as cardiac rhythm synchronization. This encourages, we hope, further research in pathology and forensic sciences. REFERENCES 1. Anderson RH, Ho SY. The architecture of the sinus node, the atrioventricular conduction axis, and the internodal atrial myocardium. J Cardiovasc Electrophysiol. 1998;9:1233Y1248. 2. Anderson KR, Ho Y, Anderson RH. Location and vascular supply of sinus node in human heart. Br Heart J. 1979;41:28Y32. 3. Gulino SP. Examination of the cardiac conduction system: forensic application in cases of sudden cardiac death. Am J Forensic Med Pathol. 2003;24:227Y236. 4. Davies MJ, Anderson RH, Becker AE. The Conduction System of the Heart. London, United Kingdom: Butterworths; 1983.

FIGURE 8. Art picture: the connective network and the elastic fibers plan defining the orthogonal layers which form the architecture of the contiguous chambers in our rendering of the SN tissue. * 2011 Lippincott Williams & Wilkins

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5. James TN. Anatomy of the human sinus node. Anat Rec. 1961;141:109Y139. 6. James TN, Sherf L, Fine G, et al. Comparative ultrastructure of the sinus node in man and dog. Circulation. 1966;34:139Y163.

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7. Leonelli F, Richey M, Beheiry S, et al. Tridimensional mapping: guided modification of the sinus node. J Cardiovasc Electrophysiol. 2007;9:1214Y1217. 8. Lowe JE, Hartwich T, Takla M, et al. Ultrastructure of electrophysiologically identified human sinoatrial nodes. Basic Res Cardiol. 1988;83:401Y409. 9. Boyett MR, Honjo H, Kodama I. The sinoatrial node, a heterogeneous pacemaker structure. Cardiovasc Res. 2000;47:658Y687. 10. Hinescu ME, Popescu LM, Gherghiceanu M, et al. Interstitial Cajal-like cells in rat mesentery: an ultrastructural and immunohistochemical approach. J Cell Mol Med. 2008;12:260Y270. 11. Faussone Pellegrini MS, Cortesoni C. Ultrastructural features and localisation of the interstitial cells of Cajal in the smooth muscle coat of human esophagus. J Submicrosc Cytol. 1985;17:187Y197. 12. Komuro T. The interstitial cells in the colon of the rabbit: scanning and transmission electron microscopy. Cell Tissue Res. 1982;222:41Y51. 13. Kyung-Whan M, Sook Seo I. Interstitial cells of Cajal in the human

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small intestine: immunochemical and ultrastructural study. Ultrastruct Pathol. 2003;27:67Y68. 14. McCloskey KD, Gurney AM. C-kit positive cells in the guinea pig bladder. J Urol. 2002;168:832Y836. 15. Sergeant GP, Hollywood MA, McCloskey KD, et al. Specialized pacemaking cells in the rabbit urethra. J Physiol. 2000;526:359Y366. 16. Pezzone MA, Watkins SC, Alber SM, et al. Identification of c-kit-positive cells in the mouse ureter: the interstitial cells of Cajal of the urinary tract. Am J Physiol Renal Physiol. 2003;284:F925YF929. 17. Pasquinelli G, Tazzari PL, Vaselli C, et al. Thoracic aortas from multiorgan donors are suitable for obtaining resident angiogenic mesenchymal stromal cells. Stem Cells. 2007;25:1627Y1634. 18. Iesurum A, Balbi T, Vasapollo D, et al. Microwave processing ethanol-based fixation in forensic pathology. Am J Forensic Med Pathol. 2006;27:178Y182. 19. Pierini G, Balbi T, Grillini P, et al. Forensic Pathology by Scanning Electron Microscopy. Bologna, Italy: CLUEB; 2009.

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ORIGINAL ARTICLE

Neonatal Freshwater Drowning After Birth in the Bathroom Jan Dressler, MD,* Uwe Schmidt, MD,* Uwe Hanisch, MD,* Guc ter Demmler, MD,* Axel Riehn, MD,Þ and Stefan Pollak, MDþ

Abstract: The macroscopic and microscopic findings in neonatal freshwater drowning are demonstrated on the basis of 3 exemplary cases of birth in the bathroom after concealed pregnancy. If the newborn is expelled under water and remains there until death, the lungs cannot be ventilated with air. In case of incomplete or only temporary submersion, aeration of the lungs may develop in the immediate postpartum period. The morphologic criteria of separate existence are critically discussed with respect to the presented findings. Key Words: underwater birth, separate existence, drowning, neonaticide (Am J Forensic Med Pathol 2011;32: 119Y123)

the newborn due to swallowing after delivery, air in the middle ears, food in the stomach and vital reaction in the stump of the umbilical cord. Underwater births make assessment more difficult: Due to the aspiration of water instead of air inhalation the appearance of the lungs may resemble a stillbirth and the lung flotation test can be negative even though the infant performed respiratory movements postpartum. In cases of intentional underwater delivery, the newborn is usually removed from the water immediately after expulsion and with the first cry the infant starts to breathe. However, in home births without the presence of a midwife it cannot be ruled out that the newborn may be submerged for a longer period, resulting in drowning. The following case reports from the forensic autopsy material demonstrate the findings that can be encountered in neonatal deaths from freshwater drowning.

N

eonaticide committed by the mother soon after the child_s birth has become rare in developed countries, but it still occurs sporadically. As in the past, deliberate killing of the newborn is always a challenge for the medicolegal expert. Although the frequency and the social background of neonaticide have changed over the decades, some of its characteristic features have stayed the same: concealment of pregnancy and delivery, preference of suffocation as the most common mode of killing the newborn, and clandestine disposal of the body. The general term Bsuffocation[ includes different methods of commitment such as smothering, manual and ligature strangulation, choking, and drowning. It goes without saying that homicidal drowning must be differentiated from disposing of an already dead infant by submersion in open water (pond, river, lake, open sea), from where the body may be recovered sometime later. Drowning of a child born alive can take place in a toilet (lavatory pan) or in other household receptacles, such as bathtub, bowl, or bucket. Up to the middle of the 20th century, in rural areas many newborns were dropped into the cesspool where they drowned in the liquid manure. The question of whether an infant was alive after delivery, that is, whether natural respiration began or the heart or umbilical cord pulsated, is to be regarded as the most important question in the forensic or pathologic postmortem examination of newborns. If none of these vital signs are evident, thenV depending on the birth weightVit is a case of stillbirth or miscarriage. However, if there are signs of separate existence, it may be a case of infanticide if, for example, there is evidence of suffocation, other forms of violence, hypothermia, or neglect. The main criteria of postnatal survival are ventilation of the lungs, the presence of air in the stomach (and intestine) of

From the Departments of *Legal Medicine, and †Gynecology and Obstetrics, Technical University, Dresden, Germany; and ‡Institute of Legal Medicine, Albert Ludwig University, Feiburg, Germany. Reprints: Jan Dressler, MD, Department of Legal Medicine, Technical University, Fetscherstrasse 74, D-01307 Dresden, Germany. E-mail: Jan.Dressler)tu-dresden.de. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0119 DOI: 10.1097/PAF.0b013e318187dff9

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CASE REPORTS Case 1 The 15-year-old mother (weight: 48 kg) said in a statement to the police that she had not noticed her pregnancy and had been surprised by the birth of the child. On the day of the delivery, she had felt severe abdominal pain and therefore took a bath. When lying in the water-filled bathtub she noticed amniotic fluid and blood. After approximately 1 hour in which the abdominal pain had constantly intensified, she realized the baby in the bathwater and cut the umbilical cord with scissors. She then tapped the child on the back to see if it was alive, but the infant did not react. After the delivery she went to bed together with the newborn. 10 months before, the young mother had had an abortion.

Forensic Medical Findings In the postmortem examination of the mature female newborn (weight: 2640 g, length: 49 cm, occipitofrontal head circumference: 29.5 cm) no evidence was found of any intrauterine disorder or fetal deformity. The child was developed in such a way as to be viable. The degree of maturity corresponded to an age of 36 T 2 weeks of gestation.1 There was no maceration (evidence of intrauterine death of the fetus). The hydrostatic test of the lung tissue in all lobes and the gastrointestinal hydrostatic test were negative. The sharp cut through the umbilical cord had been made directly adjacent to the abdominal wall, and in the periumbilical abdominal skin there was microscopic evidence of fresh bleeding into the muscle and connective tissue without inflammatory demarcation. A retroplacentary hematoma (11  8  2 cm) covered approximately 50% of the surface of the organ. Lamellate section through the placenta (lateral insertion of the umbilical cord) did not reveal any evidence of earlier circulatory disturbances, such as white infarct or pseudoinfarct. Histologic investigation showed the degree of the infant_s gestational development to correspond to full term.

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All the pulmonary lobes were subjected to histologic investigation in a series of sections (Fig. 1, A and B). There was deep aspiration of amniotic fluid components, such as squamous epithelium and horny squames (Fig. 2, A and B). Optically empty spaces in the interstitium were also visible.

Cause of Death Rapid Drowning After Underwater Birth.

Case 2 After having concealed her pregnancy and the delivery, a 21-year-old woman was taken to hospital by ambulance with severe genital bleeding. Her condition showed evidence of having shortly before given birth without medical assistance. According to the landlord, she had been in the bathroom for a long time. She stated that she had collapsed after taking a hot bath and was unaware of the whereabouts of the newborn. It

FIGURE 2. Squamous epithelium aspirated into the alveoli (A), cross-section of a bronchiolus with formed amniotic fluid components (B), (H&E, 125).

turned out that the child had been born into the water of the bathtub. Later, the police found the body of a male newborn infant in the freely accessible basement of the building where she lived.

Forensic Medical Findings

FIGURE 1. Pulmonary parenchymatous tissue, overall view (A), (H&E, 50), subpleural pulmonary parenchymatous tissue (B), (H&E, 125) expanded pulmonary parenchymatous tissue with fresh intra-alveolar bleeding. The lung tissue appears mature (stage VYVI)2Vno fetal atelectasis, no pulmonary hyaline membranes, and no indication of neonatal pneumonia. Optically empty tissue spaces in the interstitium resemble aeration although the lung had not been ventilated.

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A mature male infant (weight: 2700 g, length: 50.5 cm, head circumference: 33.5 cm) was brought in for autopsy in a plastic bag smeared with blood. The body was covered with vernix caseosa, the umbilical cord was 54 cm long; it had been cut with a sharp instrument and was tied in a simple knot. The infant showed several petechial hemorrhages in the eyelids and conjunctivae. The placenta had been fixed already in formaldehyde solution by the hospital. The autopsy was performed 1 day after birth. The caput succedaneum in the parietooccipital region indicated cephalic presentation. No deformities were found. The lungs were dark, small, and liver-like; their texture was rubbery without any crepitation at the margins. Petechial hemorrhages were found under the pleura visceralis. The hydrostatic lung and gastrointestinal tests gave negative results (Fig. 3). In spite of the short postmortem interval * 2011 Lippincott Williams & Wilkins

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FIGURE 3. Negative hydrostatic gastrointestinal test. The whole gastrointestinal tract did not contain air and sank to the bottom of the water-filled basin.

of only 1 day, a hemolytic supernatant was found after centrifugation of the blood. Microscopic examination revealed the aspiration of amniotic fluid components (horny scales, lanugo hairs, meconium) in the nonexpanded alveoli. Inside the vessels and also in the alveoli deformed erythrocytes and hemolytic residual erythrocytes were discernible (Fig. 4). The strong hemolysis indicated aspiration of hypotonic fluid (bath water) with osmotic diffusion into the circulatory system.

Cause of Death Drowning After Underwater Birth.

Case 3 After concealing her pregnancy, an 18-year-old schoolgirl gave birth to a mature male child while standing under the running water in the shower. The infant fell into the shower tray where it was exposed to splash water for several minutes. Due to the precipitate delivery the umbilical cord was torn close to the navel. The placenta was expelled later while the mother was still

Neonatal Freshwater Drowning After Birth

FIGURE 5. Skin navel with dried remains of the torn umbilical cord.

in the shower. She then wrapped the infant, which she allegedly believed to be dead, into a towel and put it into a drawer in her room. As she complained about severe abdominal pain, her mother took her to the hospital, where a perineal tear had to be sutured. She was not prepared to make a statement as to the whereabouts of the newborn, so that the police searched the flat and found the hidden child.

Forensic Medical Findings A mature male newborn (weight: 2886 g, length: 50.5 cm, head circumference: 35 cm) was brought in for autopsy in a bloodstained terry towel. Indications that the infant was a newborn were meconium smears on the skin, a caput succedaneum over the left parietal bone, and residual vernix caseosa. In an accompanying plastic bag was a placenta weighing 380 g and a 77 cm long umbilical cord with central insertion. The umbilical cord was torn irregularly close to the infant_s navel (Fig. 5). The lungs were pink and fully expanded with rounded and crepitant edges (Fig. 6). Signs of separate existence were positive results of the hydrostatic lung and gastrointestinal tests. The trachea and bronchi contained fine froth as typically seen in victims of drowning. The large intestine was filled with meconium.

Cause of Death Drowning due to splash water during birth in the shower.

FIGURE 4. Deformed and hemolytic erythrocytes in the lung tissue (Lectin histochemistry for PNA-binding sites, approximately 660).

FIGURE 6. Lungs with acute emphysema.

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TABLE 1. Comparison of Case Characteristics Characteristics

Case 1

Case 2

Case 3

Age of the mother 15 yr 21 yr 18 yr Mother_s occupation School girl School girl Previous abortions Yes Type of underwater birth Bath tub Bath tub Shower Gender of infant F M M Degree of maturity Mature Mature Mature Hydrostatic lung test j j + Hydrostatic gastrointestinal test j j + Tardieu spots + + j Aspiration of amniotic fluid + + + Aspiration of meconium + + j

In the following, these cases (Table 1) will be compared with reports in the literature (Table 2).

DISCUSSION The greatest problem in suspicious deaths of newborn infants is the proof of live birth, that is, that the child had a separate existence and had lived after the complete extrusion of its body from that of its mother. Histology is not as helpful as might be expected in the problem of demonstrating the onset of breathing.9 Autopsy of the fully developed infant in Case 1 did not reveal any evidence of pre-existing (intrauterine) disorders or deformity of the child. The newborn infant displayed signs of maturity at full term and was developed in such a way as to be viable; there was no maceration and no evidence of infection in the placenta or in the lungs of the child. The placenta showed slight immaturity and a retroplacentary hematoma. The negative result of the hydrostatic lung test was compatible with the mother_s statement that she had given birth under water. Histologic examination revealed foreign material corresponding to amniotic fluid components. In view of the retroplacentary hematoma it seems possible that the fetus suffered from intrauterine asphyxia resulting in an early respiratory impulse with consecutive aspiration of amniotic fluid containing meconium. After being born into the bath water, the infant

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probably died very rapidly from a combination of intrauterine asphyxia and subsequent drowning. Such a rapid death after expulsion would be consistent with the statement of the mother that the child was lifeless when she lifted it out of the bath water.10 The blood extravasation in the umbilical cord may be regarded as a sign of vitality, indicating that there was circulation when the umbilical cord was cut through. The absence of any cellular reaction (no granulocytes) suggested a very short survival time. In summary, the autopsy findings could not disprove the statement of the mother that the child did not breathe when she took it out of the water. As a result, the investigation proceedings were dropped. In Case 2 it was found that hypotonic fluid, obviously bath water, had been aspirated. This fluid diffused into the pulmonary vessels causing strong hemolysis. These findings justified the assumption that the newborn died of drowning in freshwater after extrusion of the body. As the child had remained under water until death, the hydrostatic tests of the lung and intestinal tract gave negative results. The hydrostatic lung test can give false negative results if the child, having been born alive, gets under water directly after birth and therefore Bbreathes[ liquid instead of air.11 The case was discontinued by the competent court in accordance with article 153 a of the German Code of Criminal Proceedings against payment of a fine. Case 3 deals with a precipitate delivery while the mother was standing under the shower in the course of which the child fell to the ground thus tearing the umbilical cord close to the navel. In the shower tray, the newborn was exposed to splash water and finally drowned. The fine froth found in the airways with acute alveolar and interstitial emphysema together with strong hemolysis could be regarded as typical signs of drowning. In this case the hydrostatic lung and gastrointestinal tests gave a positive result, as the newborn had inhaled both water and air. The mother was found guilty of involuntary manslaughter according to article 222 German Penal Code.

CONCLUSION In the cases reported here, the infants were born in the mother_s home without medical assistance and drowned in bath or shower water. Under such circumstances, a negative hydrostatic lung test does not rule out the possibility of the child having been born alive.

TABLE 2. Overview of Literature About the Most Common Complications After Underwater Birth Authors

Respiration (n)

Gilbert and Tookey3

Rosenthal4

Nguyen et al5 Wilson et al6 Rosser7 Zimmermann et al8

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Lung edema (9) Aspiration (4) Drowning (1) Lung edema (8) Aspiration of meconium (1) Near drowning (4) Aspiration of water (1) Drowning (2) Drowning (1)

Infection (n)

Streptococcal meningitis (1)

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Hyperthermia, Tachycardia (n)

Cerebral Hypoxia (n)

Hyponatremia (n)

(5)

(1)

(1)

(1)

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REFERENCES

the evidence or missing the point? Pediatrics. 2003;12: 972Y973.

1. Finnstro¨m O. Studies on maturity in newborn infants. IX. Further observations on the use of external characteristics in estimating gestational age. Acta Paediatr Scand. 1977;66:601.

7. Rosser J. Is water birth safe? The facts behind the controversy. Midwifery Dig. 1994;4:4Y6.

2. Vogel M. Atlas der Morphologischen Plazentadiagnostik. 2 Auflage. Berlin, NY: Springer-Verlag; 1996.

8. Zimmermann R, Huch A, Huch R. Water birthVis it safe? J Perinat Med. 1993;21:5Y11.

3. Gilbert RE, Tookey PA. Perinatal mortality and morbidity among babies delivered in water: surveillance study and postal survey. BMJ. 1999;319:483Y487.

9. Saukko P, Knight B. Knight_s Forensic Pathology. 3rd ed. London: Arnold; 2004:439Y450.

4. Rosenthal M. Warm-water immersion in labor and delivery. Female Patient. 1991;16:35Y46. 5. Nguyen S, Kuschel C, Teele R. Water birth: a near drowning experience. Pediatrics. 2002;110:411Y413. 6. Wilson B, Bowden K, Kessler D, et al. Underwater birth: missing

10. Johnston BM, Gluckmann PD. Respiratory Control and Lung Development in the Fetus and Newborn. Ithaca, NY: Perinatology Press; 1986. 11. Rauch E, Madea B. Kindsto¨tung. In: Brinkmann B, Madea B, eds. Handbuch Gerichtliche Medizin. Heidelberg, NY: Springer-Verlag; 2004:921Y938.

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ORIGINAL ARTICLE

Survival of Anesthetized Sus scrofa After Cycling (7-Second On/3-Second Off) Exposures to an Electronic Control Device for 3 Minutes James R. Jauchem, PhD,* Ronald L. Seaman, PhD,Þ and David A. Fines, BSÞ

Abstract: Electronic control devices (ECDs) may eventually be deployed by the military in a manner resulting in longer exposures than those encountered during law-enforcement operations. In a previous study, 18 repeated cycling (5-second on/5-second off) exposures (within a 3-minute period) of anesthetized swine to an ECD (TASER International’s Advanced TASER X26 device) resulted in leg muscle contraction, acidosis, and increases in blood electrolytes. In the current study, experiments were performed to examine effects of exposures to a different cycling rate (7-second on/3-second off), from a modified X26 ECD, on 10 swine (Sus scrofa), maintained on propofol anesthesia. In contrast with the previous study, a large number of animals (6/10) died immediately after the exposures. There were no major differences in preexposure blood factors from survivors versus nonsurvivors, with the exception of hematocrit and 2 isoenzymes of lactate dehydrogenase. It is doubtful that these factors would be useful in predicting survival after ECD exposure. Blood pH was significantly decreased after exposure, but (in animals that survived) subsequently returned to baseline levels. On the basis of the overall survival rate, further development of useful ECDs (for long-term incapacitation during military operations) may require consideration of longer pauses between repeated exposures over a 3-minute period.

toward baseline. In a subsequent study of only 3 repeated exposures,2 pH and lactate were significantly changed, but to a lesser degree than in the previous study. Electronic control devices may eventually be deployed regularly by the military in a manner resulting in longer exposures.3 Law-enforcement activities have included exposure to an ECD continuously for almost 3 minutes.4 It is possible that 5 seconds of ‘‘rest’’ between activation periods of the ECD (as in the previous experiments) would allow conscious subjects to take action to deactivate the device (eg, remove the probes, twist body to break the connection, etc). Therefore, the present experiments were performed to investigate the effects of 3 minutes of a different on/off cycling time (7-second on/3-second off) of the X26 device. To facilitate measurement of muscle contraction and changes in blood factors, anesthetized swine were used in this study, rather than conscious animals. The experiments were designed for comparison with the previous 5-second-on/5-second-off study of ECD exposure cycles.

MATERIALS AND METHODS Animal Model

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Ten male domestic swine (Sus scrofa domestica), ranging in weight from 49 to 70 kg (mean T SEM, 59 T 7 kg), were used for these studies. The pig model was selected for several reasons, including similarities to humans in terms of chemical and physical characteristics of blood, respiratory parameters, and responses to muscular exercise.1,2

S

Anesthesia and Experimental Setup

Key Words: conducted electrical weapon, electronic control device, TASER, electromuscular disruption

everal reports of TASER electronic control device (ECD) (alternatively referred to as ‘‘conducted electrical weapon,’’ ‘‘electromuscular disruption device,’’ or ‘‘electromuscular incapacitating device’’) use by law-enforcement personnel have involved repeated shots to a single individual in a short period. (X26 is a trademark of TASER International, Inc. TASER is a registered trademark of TASER International, Inc, Scottsdale, Ariz.) Jauchem et al1 published the first study of blood factor changes after such exposures in an animal model (swine). Blood pH was significantly decreased for 1 hour after 18 repeated TASER X26 ECD exposures (cycles of 5-second on/5-second off), but subsequently returned toward a normal level. All animals survived. Lactate was highly elevated, with a slow return

Manuscript received August 29, 2007; accepted December 6, 2007. From the *Directed Energy Bioeffects Division, Human Effectiveness Directorate, US Air Force Research Laboratory; and †Advanced Information Engineering Services (A General Dynamics Company), San Antonio, TX. The views, opinions, and/or findings contained in this report are those of the authors and should not be construed as an official Department of Defense position, policy, or decision. Reprints: James R. Jauchem, PhD, AFRL/HEDR, 8262 Hawks Rd, San Antonio, TX 78235. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0124 DOI: 10.1097/PAF.0b013e3182186d5d

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Details of the techniques of animal preparation, anesthesia, physiological measurements, blood sampling, and analysis of blood factors have been presented previously.1,2 After administration of tiletamine HCl, zolazepam HCl, and buprenorphine, anesthesia was maintained with 100 to 125 Kg/kg per minute (or to anesthetic effect) of propofol. Aspects of propofol relevant to these experiments, compared with other anesthetics, have been discussed previously.1,2 Levels of whole-blood factors and of myoglobin, creatine phosphokinase (CPK), and lactate deyhydrogenase (LDH) in serum samples (and their isoenzymes) were measured as described previously.1,2 When levels of blood lactate were above the limit of the analyzer, serum samples were prepared for further analysis. Techniques that were different from those previously reported1,2 are as follows. The outputs of force sensors attached to the limbs were amplified by differential input DC amplifiers (model 56-1340-00; Gould, Cleveland, Ohio) and recorded by an MP150 system (MP150 hardware and Acqknowledge v3.7.3 software; BIOPAC Systems, Santa Barbara, Calif ). Electrocardiogram (ECG) monitoring electrodes (model 9300-032-50; Mortara Instrument, Milwaukee, Wis) were attached to the limbs and connected to an ECG/Biotach unit (model 20-4615-52; Gould). The ECG unit was protected from high voltages by a Am J Forensic Med Pathol

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Zener diode connected to ground on each electrode connection. A voltage signal was derived from a respiration sensor (HESKA, Loveland, Colo) with a custom circuit to indicate inflow and outflow of respiratory air. The signal provided a continuous record of respiratory activity that was recorded by the MP150 system. Mean colonic temperatures of all animals were between 36.1-C and 37.2-C, with no significant changes over time.

Electronic Control Device Exposures The probes of the X26 ECD were inserted into each pig at a standard position (30 cm apart) subcutaneously.1 Swine were then exposed to the output of the X26 device for 3 minutes at a cycling rate of 7 seconds on, followed by ‘‘rest’’ periods of 3 seconds off, repeatedly (ie, for total of 18 cycles), with blood samples taken afterward. (The device was modified to allow for longer periods of applied power than the standard 5 seconds.) The heart continued to exhibit organized QRS electrical activity after exposure; apnea was therefore considered to represent the lethal end point. If an animal exhibited apnea (defined here as no more than 3 regular chest movements per minutes) for 10 minutes, the animal was considered to have died; pentobarbital was administered, and after cessation of heartbeat, the experiment was terminated.

Statistical Analyses Blood, serum, and physiological data were studied using analysis of variance (ANOVA). Analysis of variance was performed on pre-exposure and immediate postexposure levels with repeated measures on time (pre and post) with and without survival status in the ANOVA model (2-way and 1-way, respectively). For survivors, 1-way ANOVA was performed with repeated measures on the time points across 3 hours with a linear contrast for each of the 7 postexposure values with the preexposure value. Heart rate, respiration rate, oxygen saturation, and body temperature analyses included linear contrasts with the respective pre-exposure value. Data were generally available over the period from 5 minutes before start of exposure to 10 minutes after the start of exposure (7 minutes postexposure) and included data recorded during exposure. The average of respective preexposure values was used as the first time point in each analysis. Twenty subsequent values at 30-second intervals for heart rate, oxygen saturation, and body temperature, and 10 subsequent values at 1-minute intervals for respiration rate, were analyzed. The time span used for repeated-measures testing was dependent

on availability of values at each time point. For oxygen saturation, a total of 18 values were missing because of interference from the ECD; these values were replaced with interpolated values. (This was not necessary for heart rate, respiration rate, and body temperature.) The normality requirement for using ANOVA was checked by performing a Kolmogorov-Smirnov test for normality on preexposure values. Tukey-Kramer adjustments were made for multiple testing. P G 0.05 was considered to be statistically significant.

RESULTS Survival Four animals survived the exposures, whereas 6 exhibited apnea immediately after the exposures. The blood-gas analyzer became nonfunctional for 1 survival animal; therefore, that experiment was terminated 30 minutes after exposure. Blood data from that experiment are not included in any further analyses in this study. Comparisons of blood and serum factors from survivors with nonsurvivors, for pre-exposure and immediate postexposure data, are presented in Tables 1 and 2. For pre-exposure values, there were only 3 significant differences between animal groups: Animals that died exhibited slightly higher pre-exposure hematocrit and percentage of LDH3 and lower percentage of LDH5 than did survivors. Nonsurvivors also exhibited higher immediate postexposure percentages of LDH1 and LDH3.

Muscle Contraction Force The maximal force of limb extension generally occurred at the start of each 7-second exposure period, with a slight drop in the force during the remainder of each exposure. Because of some eventual slippage of retaining straps on the 4 limbs, only the muscle-contraction measurements during the first three 7-second exposure periods were considered to be accurate reflections of limb movement. The level of maximal force (mean T SEM), averaged over those exposure periods, was 269 T 6 N for the forelimbs and 232 T 5 N for the hindlimbs.

Whole-Blood Sample Changes In each figure of blood and serum changes in this article, sampling time is shown in minutes, with ‘‘Pre’’ referring to before ECD exposure and ‘‘Post’’ referring to immediately after the 18 exposure cycles. For ease of presentation, the data are shown graphically for all 9 animals (3 survivors and 6 nonsurvivors)

TABLE 1. Blood Factors Before and After ECD Exposures Survivors Factor pH Lactate, mmol/L K+, mmol/L Na+, mmol/L Ca++, mmol/L Glucose, mg/dL Hematocrit

Nonsurvivors

Pre-Exposure

Postexposure

Pre-Exposure

Postexposure

7.43 T 0.01 1.1 T 0.2 3.7 T 0.1 138 T 1 1.26 T 0.1 100 T 23 30 T 2

6.84 T 0.02* 23.8 T 1.0* 7.6 T 0.5* 154 T 2* 1.39 T 0.2* 125 T 11 42 T 2*

7.40 T 0.02 1.0 T 0.2 3.8 T 0.1 140 T 1 1.30 T 0.2 94 T 8 34 T 0.4†

6.88 T 0.07* 22.8 T 3.2* 7.6 T 0.7* 154 T 2* 1.36 T 0.3 134 T 17* 46 T 1*

Values are presented as mean T SEM. *Significantly different, pre-exposure vs postexposure. †Significantly different, survivors vs nonsurvivors.

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TABLE 2. Serum Factors Before and After ECD Exposures Survivors Factor Myoglobin, ng/mL Total CPK, IU/L CPK-MM, % CPK-MB, % CPK-BB, % Total LDH, IU/L LDH1, % LDH2, % LDH3, % LDH4, % LDH5, % LDH1/LDH2 ratio

Nonsurvivors

Pre-Exposure

Postexposure

Pre-Exposure

Postexposure

17.6 T 3.6 1337 T 733 59.3 T 17.2 2.9 T 1.3 37.8 T 16.1 537 T 116 28.1 T 4.1 0.6 T 0.03 1.0 T 0.1 6.6 T 4.5 63.7 T 10.4 43.6 T 6.5

75.5 T 9.0* 1911 T 1145 55.8 T 15.3 1.5 T 0.3 42.6 T 15.4 871 T 235 25.1 T 4.1 0.6 T 0.1 1.2 T 0.2 21.1 T 2.4* 52.0 T 8.1 44.3 T 6.2

27.1 T 6.0 1096 T 374 49.6 T 10.9 3.7 T 0.9 46.8 T 10.2 817 T 108 37.7 T 6.8 1.1 T 0.1 2.2 T 0.2† 17.7 T 2.8 41.3 T 3.8† 36.9 T 3.4

64.7 T 14.9* 1111 T 177 71.5 T 10.7 3.2 T 1.2 25.3 T 9.6 737 T 85 48.6 T 5.8† 1.3 T 0.2 2.4 T 0.3† 14.0 T 3.0 33.8 T 5.6 40.7 T 5.1

Values are presented as mean T SEM. *Significantly different, pre-exposure vs postexposure. †Significantly different, survivors vs nonsurvivors.

combined. (Nonsurvivor pre-exposure and postexposure data, however, are listed individually in Tables 1 and 2.) Blood pH is shown in Figure 1. Some exposures resulted in pH values less than the lower limit of measurement of the blood-gas/electrolyte analyzer (6.8). Measurements of less than 6.8 were assigned a value of 6.8 for purposes of data analysis. The pH was significantly decreased below baseline values (regardless of survival status) immediately after ECD exposure and through 60 minutes after, but then slowly returned (in survivors) to pre-exposure values. Lactate (Fig. 2) was significantly elevated at all postexposure time points, with the exception of 180 minutes. Blood potassium and sodium were each statistically significantly increased immediately after exposure in both survivors and nonsurvivors (Table 1), but returned to baseline levels at the subsequent time point (data not shown). Blood calcium was significantly increased immediately after exposure only in survivors; blood glucose was significantly increased immediately after exposure only in nonsurvivors (Table 1).

FIGURE 1. Jugular venous blood pH (mean T SEM) of swine before and after exposure to ‘‘7 s on/3 s off’’ cycles, for 3 minutes. *Significantly different from pre-exposure value. n = 9 for pre and post; n = 3 for minutes 30Y180.

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Hematocrit (Fig. 3) was significantly increased immediately, 30 minutes, and 60 minutes after exposure.

Serum Sample Changes Serum myoglobin was increased significantly immediately after exposure in both survivors and nonsurvivors (Table 2) and at time points 30, 90, 120, and 150 minutes after exposure (data not shown) in survivors. There were no significant changes in total CPK, CPK isoenzyme percentages (MM, MB, and BB), or total LDH. (LDH isoenzyme percentages and significant differences are shown in Table 2.) Levels of troponin T were undetectable at all points, with the exception of 4 animals that exhibited levels of 0.02 to 0.07 ng/mL at single points. Two animals showed a troponin I level of 0.02 or 0.09 at single points; 1 animal (that survived) had levels of 0.35, 0.15, 0.11, 0.36, 0.00,

FIGURE 2. Jugular venous lactate (mean T SEM) of swine before and after exposure to ‘‘7 s on/3 s off’’ cycles, for 3 minutes. *Significantly different from pre-exposure value. Some lactate values (any 915 mmol/L, at immediate, 30-minute, and 60-minute postexposure time points) from individual animals were obtained from serum rather than whole-blood samples. n = 9 for pre and post; n = 3 for minutes 30Y180. * 2011 Lippincott Williams & Wilkins

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FIGURE 3. Jugular venous hematocrit (mean T SEM) of swine before and after exposure to ‘‘7 s on/3 s off’’ cycles, for 3 minutes. *Significantly different from pre-exposure value. n = 9 for pre and post; n = 3 for minutes 30Y180.

0.50, 0.37, and 0.27 ng/mL at pre-exposure and each successive time point, respectively.

Heart Rate, Respiratory Rate, and Arterial Oxygen Saturation

S. Scrofa Exposed to Electronic Control Device

FIGURE 5. Respiration rate from 5 minutes before to 10 minutes after start of exposure (‘‘7 s on/3 s off’’ cycles, for 3 minutes). Respiration rate is in breaths per minute, recorded during 1-minute intervals. Vertical dashed lines mark start and end of exposure. *Significant difference from the pre-exposure value for survivors. §Significant difference from the pre-exposure value for nonsurvivors. ‡Significant difference between survivor and nonsurvivor values at the indicated time point.

For heart rate (Fig. 4), data through 6.25 minutes after start of exposure (14 time points) from 4 survivors and 5 nonsurvivors were available for analysis. There was a significant change over time for survivors and nonsurvivors and a significantly increased heart rate starting at 0.75 minutes for both groups. For survivors, the increase persisted (with 1 exception) through 6.25 minutes. For nonsurvivors, the increase was no longer significant at 3.25 minutes, immediately after termination of exposures, and later. Repeated-measures ANOVAs that included survival status showed no significant difference in heart rate between survivors and nonsurvivors at any time point.

Although no breaths occurred during each 7-second period of ECD exposure (other than a sustained single inspiration in some cases), breathing was observed during each 3-second rest period in animals that survived. Data through 5.5 minutes after start of exposure (6 time points) from 4 survivors and 5 nonsurvivors were available for analysis (Fig. 5). There were significant changes over time for survivors and nonsurvivors, and a significantly decreased respiration rate starting at 0.25 minutes (the first time point during exposures) that lasted through 4.5 minutes before it started to increase. With linear contrasts for nonsurvivors, there was a decreased respiration rate starting at 3.5 minutes, the first time point after exposures, and later. With repeated-measures ANOVA that included survival status,

FIGURE 4. Heart rate from 5 minutes before to 10 minutes after start of exposure (‘‘7 s on/3 s off’’ cycles, for 3 minutes). Heart rate is in beats per minute, represented as averages over 30-second intervals. Vertical dashed lines mark start and end of exposure. *Significant difference from the pre-exposure value for survivors. §Significant difference from the pre-exposure value for nonsurvivors.

FIGURE 6. Oxygen saturation from 5 minutes before to 10 minutes after start of exposure (‘‘7 s on/3 s off’’ cycles, for 3 minutes). Percent oxygen saturation was measured at 30-second intervals. Vertical dashed lines mark start and end of exposure. §Significant difference from the pre-exposure value for nonsurvivors.

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there were significant differences in heart rate between survivors and nonsurvivors. Post hoc pairwise comparisons revealed significant differences between the groups at 0.25 minutes and the 3 time points after exposure. Note that although survivor and nonsurvivor respiration rate seems different for the pre-exposure time point, pairwise comparison indicated no significant difference (P = 0.264). Repeated-measures ANOVA for 3 survivors and 4 nonsurvivors over all time points (10 time points after preexposure) revealed no additional significant differences for survivors but indicated that all but the last value for nonsurvivors were significantly different from the pre-exposure value. For oxygen saturation (Fig. 6), data through 6.25 minutes after start of exposure (13 time points) from 2 survivors and 6 nonsurvivors were available for analysis. Although survivor oxygen saturation decreased in a fashion similar to that of nonsurvivors over most of this period, survivor data were not analyzed separately or with its interaction with survival status because of the low number of survivors. There was a significantly decreased oxygen saturation starting at 1.75 minutes that persisted through 6.25 minutes for nonsurvivors.

DISCUSSION Muscle Contraction In terms of muscular contraction effectiveness (amount of force generated), peak values of force generated by the leg muscles were similar to those in previous studies of repeated X26 ECD exposures.1,2 Other investigators,5 using a comparable experimental preparation, found lower values of force generated6 during exposures to an earlier ECD model (‘‘M26’’ [trademark of TASER International, Inc]).

Lactate and pH Blood pH values may be useful for predicting survival in patients with conditions such as severe shock.7 In our current experiments, however, there were no significant differences in preY or postYECD exposure blood pH between survivors and nonsurvivors. The patterns of pH and lactate changes were similar to the previous ECD studies.1,2 Koliski et al8 used blood lactate concentration as a prognostic indicator of impending death in critically ill patients. In our current experiments, however, there were no significant differences in lactate levels before or after ECD exposures between survivors and nonsurvivors. Some of the factors referenced in the following sections are affected by lactate levels and pH, but are mentioned separately for discussion purposes.

Electrolytes and Hematocrit The increases in blood sodium, potassium, and calcium, after exposure, were consistent with previous studies of muscle stimulation or acute exercise (see Jauchem et al2 and Jauchem9 for discussion). A rise in blood potassium often occurs along with acidosis, whether metabolic or respiratory in origin.10 In our current experiments, hyperkalemia was more extreme than in the previous study of shorter periods of ECD exposure (cycles of 5-second on/5-second off).1 Within 30 minutes, however, potassium had returned to a normal level. Although extreme hyperkalemia may be associated with ventricular fibrillation or asystole,11 no such events occurred after ECD exposure (despite a reported greater susceptibility of swine to ventricular fibrillation than smaller mammals12). Distinctly lower values for hematocrit are common in pigs (compared to humans). The pre-exposure samples in the current experiments were within reference ranges as reported by Hannon

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et al13 in studies of conscious pigs. Nonsurvivors exhibited a significantly higher pre-exposure hematocrit than survivors. Although increased hematocrit can lead to thrombogenesis and increased mortality in certain disease states,14 the difference between groups in our current experiments was very small and unlikely to have played a role in survival. The increase in hematocrit after exposure was consistent with previous studies of muscle stimulation in anesthetized dogs.15

Myoglobin, CPK, and LDH In the current study, serum myoglobin was increased after exposure and remained elevated for the 3-hour follow-up period. The maximum value, however, was below referenced upper limits of ‘‘normal’’ values for humans (see Jauchem et al2 for discussion). Normal values for swine have not been defined. A comparison of myoglobin levels after X26 ECD exposures with those after toxic, ischemic, or traumatic rhabdomyolysis has been presented previously by Jauchem et al.2 In addition to myoglobin that may be released because of the contraction of muscles,16 a direct effect of electric pulses on myoglobin release from muscles has been demonstrated by Bhatt et al.17 The extent of myoglobin release was dependent on the number of pulses, pulse duration, and field strength. Increases in total serum CPK or percentage of CPK-MM have been reported in swine exposed to ECDs2 or after electrical stimulation (combined with rapid running for 5 minutes)18 and in horses exercising.19 In the present experiments, however, no such changes were observed. Some LDH-isoenzyme percentages exhibited significant differences between survivors and nonsurvivors or changes in the current experiments after ECD exposures. Because of the relatively large number of end points examined in this study, however, several statistically significant differences may have been expected by chance. Any clinical significance of these differences is unknown.

Heart Rate, Respiratory Rate, and Oxygen Saturation The increases in heart rate during the X26 exposure periods were greater than those seen in the previous study of 18 repeated ‘‘5-second on/5-second off’’ TASER ECD applications1 but less than those in studies of steady-state and exhaustive exercise.20 Pre-exposure respiratory rate was above the range reported by Hannon et al13 in conscious pigs. Cessation of effective breathing, which occurred during X26 exposure, was probably related, in part, to direct effects on muscles involved in respiration. Murray and Resnick21 noted that ECDs are capable of dramatically affecting the diaphragm and intercostal muscles. Davison and Lewer22 suggested that a specific electric-shock weapon could result in ‘‘forced inhalation.’’ Conscious humans are able to breathe during some ECD exposures, including those of relatively long duration.23 In some incidents of human deaths after ECD exposures, however, subjects have been reported to stop breathing immediately after the exposures (eg, see Peters24). Although 60-Hz electric current is not equivalent to output of a TASER ECD, several aspects regarding such current are worthy of consideration in relation to respiration. The current density required for tetanus of skeletal muscles caused by such exposure is about twice that required for paralysis of respiratory muscles (and respiratory arrest).25 The subsequent threshold for ventricular fibrillation is about twice that for respiratory muscle paralysis. During electroshock therapy, patients also exhibit apnea.26 Long ago, Jex-Blake27 suggested that some cases of immediate death due to electric shock could result from asphyxia * 2011 Lippincott Williams & Wilkins

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related to tetanic contraction of respiratory muscles. Lee and Zoledziowski28 found that respiratory arrest in anesthetized rabbits during electric shock was due to tetanic contraction of either some or all of the respiratory muscles (including all thoracic muscles), depending on the current. At lower current densities, some respiratory movements were present. In those cases, the authors suggested that tetanic muscle contraction of the whole chest was not complete. Koscove29 reviewed the possibility of respiratory arrest due to asphyxiation during electrical injury. Hodgkin et al30 reported that unanesthetized dogs exhibited longer cessations of respiration after limb-to-limb electric shock than did dogs that were administered ether, pentobarbital, or morphine. In fact, some unanesthetized animals did not recover adequate spontaneous breathing activity, in contrast to all of the medicated canines. Potential responses of unanesthetized swine in experiments similar to ours are unknown. The lack of adequate breathing (concurrent with continued organized QRS electrical activity of the heart) in nonsurvivors in the present experiments is consistent with previous observations of Hodgkin et al,30 who noted that victims of electric shock may exhibit inadequate or absent breathing, even though the heart continues to beat. The lack of respiration may have been similar to what Sawaguchi31 referred to as ‘‘asphyxia caused by external mechanical factors (such as external application of pressure to the naso-oral, cervical, or thoracic region).’’ In this situation, changes related to increased blood CO2 and acidemia result in noncompensatory (acute) respiratory acidosis. Reasons for sustained apnea in the nonsurvivors, however, are not clear. Lambertson32 noted that, during hypoxia, ‘‘if the respiratory neurons are so depressed that they no longer react to effects of hypercapnia, cessation of respiration will result.’’ Although blood PO2 and PCO2 were not measured in the current study, even a low number of ECD exposures can result in significantly decreased central venous PO2 and increased central venous PCO2 in anesthetized swine.2 In our current experiments, blood oxygen saturation was extremely low during and after ECD exposure. A complex combination of events with effects on respiratorycenter neurons can occur during hypoxemia, including accumulation of metabolic products, decreased ability of cells to react to chemical stimuli, and exaggeration of afferent inhibitory influences.32 Severe hypoxia alone may cause apnea, over wide ranges of pH and PCO2.33 In our experiments, blood oxygen saturation level tended to recover more quickly than blood pH. This finding was similar to results of previous ECD studies.1,2

S. Scrofa Exposed to Electronic Control Device

chanical ventilation), it is likely that acidosis would have still been present because of contraction of muscles. The acidosis and associated accumulation of lactate would appear to be one of the major concerns regarding long-duration (eg, several minutes) exposures. Effects of ECD exposure on a conscious animal model were not investigated in this study. Any proposed use of such a model, however, must include assessment of the degree and duration of discomfort relative to the potential benefit. The lack of effective breathing during ECD exposures in anesthetized swine was in contrast with the study of conscious human volunteers of Ho et al.23 Experiments of repeated ECD exposures of the durations used in the current study, however, would not be possible, ethically, in humans (whether anesthetized or conscious).

CONCLUSIONS After ECD exposure, transient increases in hematocrit and blood potassium, sodium, and calcium, even though statistically significant, were of relatively low magnitudes and returned close to pre-exposure levels within 30 minutes. Blood pH was significantly decreased after exposure, but subsequently returned toward a baseline level. Muscle contractions and changes in respiration each could have contributed to the acidosis. Lactate was highly elevated, with a slow return toward baseline. In conclusion, 3 minutes of cycling exposures (7 seconds on, followed by 3 seconds off, repeatedly) to the output of the TASER X26 ECD (modified for the longer exposure periods) resulted in significant changes in blood chemistry. Only 4 of 10 animals survived. In animals that survived, levels of most of the blood factors returned to baseline. On the basis of the overall survival rate, further development of useful ECDs (for long-term incapacitation during military operations) may require consideration of longer pauses between repeated exposures over a 3-minute period. ACKNOWLEDGMENTS The authors thank Curtis M. Klages, DVM, Major, Veterinary Corps, US Army, for surgically implanting the jugular venous catheters; Specialist Jonathan F. Montes and Sergeant Michael D. Hudson, US Army, for anesthesia maintenance; and John L. Ashmore, General Dynamics Advanced Information Systems, for programming and operating the ECD. The valuable advice of Dr Alan Ashworth, Biobehavioral Sciences Branch, Directed Energy Bioeffects Division, Human Effectiveness Directorate, US Air Force Research Laboratory, is greatly appreciated.

Overall Relevance of Results to Possible ECD Repeated-Exposure Scenarios Because of the relatively large number of end points, any clinical significance of the small (but statistically significant) differences between survivors and nonsurvivors in a few factors (hematocrit, LDH3, and LDH5) pre-exposure is unknown. On the basis of this study of 3 minutes of cycling exposures (7-second on/3-second off) to an ECD on blood factors, it is apparent that, although major changes in lactate and pH occur, some animals are still able to survive such scenarios. Nonsurvivors exhibited apnea, rather than cardiac effects such as ventricular fibrillation or asystole. When considering exposures to ECDs, a complex situation can result because of both muscle contractions and interruption of normal respiration. Respiration in the present experiments was significantly affected during exposure. Both respiratory and metabolic changes could have contributed to acidosis. Even if respiratory effects could have been alleviated (eg, by me* 2011 Lippincott Williams & Wilkins

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REFERENCES 1. Jauchem JR, Sherry CJ, Fines DA, et al. Acidosis, lactate, electrolytes, muscle enzymes, and other factors in the blood of Sus scrofa following repeated TASER\ exposures. Forensic Sci Int. 2006;161:20Y30. 2. Jauchem JR, Cook MC, Beason CW. Blood factors of Sus scrofa following a series of three TASER\ electronic control device exposures. Forensic Sci Int. 2008;175:166Y170. 3. Murphy D. TASER Anti-Personnel Munition (TAPM). National Defense Industrial Association Mines Demolition and Non-lethal Conference; June 5, 2002; Washington, DC. Available at: http:// www.dtic.mil/ndia/2002mines/murphy.pdf. Accessed August 27, 2007. 4. Bell NM. Inmate shocked for nearly 3 minutes. Charlotte Observer. October 6, 2005. 5. TASER International, Inc. Development of Long Range TASER\ Neuro-muscular Disruption Weapon. First Round Test Results, Phase I. Scottsdale, AZ: TASER International, Inc; 2002.

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6. Naval Studies Board. Chapter 3. Core thrusts. In: 2003 Assessment of the Office of Naval Research’s Marine Corps Science and Technology Program. Washington, DC: National Academies Press; 2004. Available at: http://fermat.nap.edu/books/0309089816/html/49.html. Accessed August 27, 2007. 7. Nishikawa Y, Fukumoto K, Watanabe F. Guanine deaminase in serum as an indicator of survival probability in severe shock patients. Clin Chim Acta. 1983;131:67Y73. 8. Koliski A, Cat I, Giraldi DJ, et al. Blood lactate concentration as prognostic marker in critically ill children [in Portuguese]. J Pediatr (Rio J). 2005;81:287Y292. 9. Jauchem JR. Re: acidosis, lactate, electrolytes, muscle enzymes, and other factors in the blood of Sus scrofa following repeated TASER\ exposures [letter]. Forensic Sci Int. 2007;168:e19. 10. Morgan HG. Acid-base balance in blood [review]. Br J Anaesth. 1969;41:196Y212.

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and left ventricular function in stallions. Equine Vet J. 1999;30(suppl):163Y165. 20. Hastings AB, White FC, Sanders TM, et al. Comparative physiological responses to exercise stress. J Appl Physiol. 1982;52:1077Y1083. 21. Murray J, Resnick B. A Guide to TASER Technology: Stunguns, Lies and Videotape. Whitewater, CO: Whitewater Press; 1997. 22 Davison N, Lewer N. Bradford Non-lethal Weapons Research Project. Research Report No. 4. Bradford, UK: Bradford University, Department of Peace Studies, Centre for Conflict Resolution; 2003. Available at: http://www.bradford.ac.uk/acad/nlw/research_ reports/docs/BNLWRPResearchReportNo4_Dec03.pdf. Accessed August 27, 2007. 23. Ho JD, Dawes DM, Bultman LL, et al. Respiratory effect of prolonged electrical weapon application on human volunteers. Acad Emerg Med. 2007;14:197Y201.

11. Tran HA. Extreme hyperkalemia. South Med J. 2005;98:729Y730.

24. Peters M. Can a TASER kill? Greeley (Colorado) Tribune. July 9, 2006.

12. Hearse DJ, Sutherland FJ. Experimental models for the study of cardiovascular function and disease. Pharmacol Res. 2000;41: 597Y603.

25. Koumbourlis AC. Electrical injuries. Crit Care Med. 2002;30:S245.

13. Hannon JP, Bossone CA, Wade CE. Normal physiological values for conscious pigs used in biomedical research. Lab Anim Sci. 1990;40:293Y298.

27. Jex-Blake AJ. Goulstonian lectures: death by electric currents and by lightning. Br Med J. 1913;1:425Y430, 492Y498, 548Y552, 601Y603.

14. Kwaan HC, Wang J. Hyperviscosity in polycythemia vera and other red cell abnormalities [review]. Semin Thromb Hemost. 2003;29: 451Y458.

28. Lee WR, Zoledziowski S. Effects of electric shock on respiration in the rabbit. Br J Ind Med. 1964;21:135Y144.

15. Bolter CP, Critz JB. The time course of plasma enzyme changes accompanying skeletal muscle stimulation. Experientia. 1976;32:883Y884. 16. Roxin LE, Venge P, Friman G. Variations in serum myoglobin after a 2-min isokinetic exercise test and the effects of training. Eur J Appl Physiol Occup Physiol. 1984;53:43Y47.

26. Fish R. Electric shock, part III: deliberately applied electric shocks and the treatment of electric injuries. J Emerg Med. 1993;11:599Y603.

29. Koscove EM. The TASER\ weapon: a new emergency medicine problem. Ann Emerg Med. 1985;14:1205Y1208. 30. Hodgkin BC, Langworthy O, Kouwenhoven WB. Effect on breathing of an electric shock applied to the extremities. IEEE Trans Power App Syst. 1973;92:1388Y1391.

17. Bhatt DL, Gaylor DC, Lee RC. Rhabdomyolysis due to pulsed electric fields. Plast Reconstr Surg. 1990;86:1Y11.

31. Sawaguchi A. Pathophysiological study of asphyxia and its applications to medico-legal diagnosis [in Japanese]. Nippon Hoigaku Zasshi. 1994;48:403Y419.

18. Hallberg JW, Topel DG, Christian LL. Creatine phosphokinase isoenzymes in stress-susceptible and stress-resistant pigs. J Anim Sci. 1979;49:1464Y1469.

32. Lambertson CJ. Abnormal types of respiration. In: Mountcastle VB, ed. Medical Physiology. 13th ed. St Louis, MO: CV Mosby Co; 1974:1522Y1537.

19. Rueca F, Conti MB, Porciello F, et al. Relationship between running speed, isoenzymes of serum creatine kinase and lactate dehydrogenase

33. Guntheroth WG, Kawabori I. Hypoxic apnea and gasping. J Clin Invest. 1975;56:1371Y1377.

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ORIGINAL ARTICLE

The Methadone Epidemic Methadone-Related Deaths on the Rise in Vermont Michelle E. Madden, MD* and Steven L. Shapiro, MDÞþ

Abstract: The prevalence of methadone-related overdose deaths is increasing worldwide and has been a topic of recent debate. Methadonerelated deaths, to this point, have not been systematically reviewed in the state of Vermont. All of the methadone-related fatalities from 2001 to 2006 (total, 76 cases), which were examined by the Vermont Office of the Chief Medical Examiner were retrospectively reviewed. The mean age of the decedents was 36 years (range, 16Y74 years), and 72% were male. The manners of death were classified as follows: 84% accident, 12% undetermined, and 4% suicide. The mean level of methadone was 457 ng/mL (range, 50Y3793 ng/mL). The substances causing death were determined to be methadone alone in 26 (34%), methadone with only other prescribed medications in 29 (38%), methadone with only illicit drugs (excluding tetrahydrocannabinol) in 13 (17%), methadone with both illicit and prescribed medications in 5 (7%), and methadone with ethanol in 3 (4%). The methadone was obtained by illegal diversion (sale, gift, or theft) in 67% of cases. In the remaining cases (33%), the methadone was obtained by physician_s prescription for chronic pain (60%), acute pain or injury (8%), methadone maintenance therapy for heroin dependence (8%), and unknown reasons (24%). The number of overdose deaths has increased 4-fold from 2001 (17 deaths) to 2006 (79 deaths). The proportion of methadone-related deaths has increased by 300% from 2001 (0.6% of reported deaths, 12% of overdose deaths) to 2006 (3% of reported deaths, 37% of overdose deaths). Methadone maintenance therapy for heroin dependence in our population comprises an insignificant number of the methadone-related deaths (3% of the decedents). In Vermont, the populations most at risk are those taking methadone for chronic pain and those obtaining diverted methadone for abuse. Education of clinicians regarding the increasing number of methadone-related deaths, the potential for abuse and diversion, and the pharmacokinetics of methadone may help halt this epidemic and reduce the number of fatalities from this drug. Key Words: methadone maintenance therapy, drug diversion, chronic pain, dependence, pharmacokinetics (Am J Forensic Med Pathol 2011;32: 131Y135)

T

he number and prevalence of methadone-related deaths in the United States and worldwide has increased over the last decade.1Y3 While this has been a topic of recent discussion, and forensic pathologists have noticed an increasing trend, methadone-related deaths to this point have not been systematically reviewed in the state of Vermont.

Manuscript received January 16, 2008; accepted June 30, 2008. From the *Department of Pathology and Laboratory Medicine, University of Vermont and Fletcher Allen Health Care, Vermont, NY; †Office of the Chief Medical Examiner, Vermont Department of Health; and ‡Department of Pathology, University of Vermont, Burlington, VT. Reprints: Steven L. Shapiro, MD, Office of the Chief Medical Examiner, Vermont Department of Health, 111 Colchester Ave, Burlington, VT 05401. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0131 DOI: 10.1097/PAF.0b013e3181e8af3d

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BACKGROUND Heroin abuse and dependence began increasing in the post-World War II era. By the 1950s and 1960s, it had reached epidemic proportions, particularly in New York City.4,5 The heroin-related death rate during this time increased from 7.2 per 10,000 deaths in 1950 to 35.8 per 10,000 deaths in 1961. And by 1961, death related to heroin injection had become the leading cause of death in young adults in New York City, with a mean age of 29.6,7 It was because of these alarming figures that several independent researchers began exploring a substitution approach to heroin treatment. Methadone, or dolophine, a longacting agonist with a half life of 24 to 36 hours, was first synthesized in pre-World War II Germany for analgesia. In 1949, Isbell and Vogel at the US Public Health Hospital showed that methadone was the most effective substitution medication for the treatment of heroin dependence.6,8 The protocol was to discontinue methadone after a short taper. Follow-up studies in the 1950s and 1960s, however, showed a high relapse rate of over 90% once methadone was discontinued.6 Methadone maintenance treatment (MMT) was studied intensively beginning in 1964 at The Rockefeller University by a research laboratory overseen by Nyswander and Dole.9 They determined that the amount of daily methadone should be sufficient to relieve narcotic craving, block the effects of administrated heroin or other short-acting opioids, suppress the opioid abstinence syndrome for 24 to 36 hours, develop tolerance to the analgesic effects of methadone and develop tolerance to the euphoria, sedation, and other narcotic effects of methadone.6,9Y11 Analysis of these signs and symptoms in a patient allowed establishment of a titrated daily maintenance dose. In the beginning, these studies were conducted in inpatients over weeks to months; however, studies evaluating inpatient versus outpatient methadone treatment in 1965Y1966 showed no significant difference in outcomes.12 Thus, the outpatient methadone clinic model was adopted in 1966 for the expansion of MMT throughout the United States.6 Since these fundamental studies, there have been several studies documenting the benefits of MMT. These benefits include the reduction of criminal activity,13 reducing the costs of crime,14 decreasing illicit drug use by opiate abusers,15 improving social integration,16 improving employment prospects,17 and reducing the morbidity and mortality of opiate users.18Y21 While this is a positive change, recent trends suggest that the increase in methadone use in some cases may be problematic. The Office of Analysis and Epidemiology, under the US Department of Health and Human Services and the Centers for Disease Control and Prevention has identified recent trends in overdose and specifically methadone-related deaths between 1999 and 2004.1 During this time period, methadone-related deaths have increased 390%. Methadone-related deaths have increased from 4% of all overdose/poisoning deaths to 13% of all overdose/poisoning deaths. The relative increase in methadonerelated overdose deaths from 1999 to 2004 was greater than for any other individual substance. The largest increase was noted in the 15 to 24 year age group, which was 11-fold higher in 2004 than in 1999.1

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TABLE 1. Total Overdose and Methadone-Related Deaths

Year

Total Deaths Number

Overdose Deaths Number (%)

2001 2002 2003 2004 2005 2006 Total

346 748 762 776 844 841 4317

17 (4.9) 47 (6.3) 71 (9.3) 55 (7.1) 67 (7.9) 79 (9.4) 336 (7.8)

Methadone-Related Deaths

Number

Percent Overdose Deaths

Percent Total Deaths

2 8 13 7 17 29 76

11.8 17 18.3 12.7 25.4 36.7 22.6

0.6 1.1 1.7 0.9 2 3.4 1.8

These national trends are mirrored in the state of Vermont. It became apparent that there were an increasing number of methadone-related deaths in Vermont. Until this point, these deaths have not been systematically reviewed. The objective of this retrospective study was to review all of the methadonerelated deaths in Vermont over a 6-year period to identify trends, sources of methadone, and to characterize the populations at risk. From these data, it will be feasible to identify potential problem areas within the current system.

MATERIALS AND METHODS There were 76 methadone-related deaths in the state of Vermont between the years 2001 and 2006. The cases were identified by searching the Vermont Office of the Chief Medical Examiner (OCME) database for cases in which methadone was identified in decedents_ blood and urine. Each case was identified by number and each corresponding file was read individually. Medical examiner and police investigation reports along with hospital medical records were included in the study. Furthermore, the toxicology report for each individual case was examined separately. About 76 cases were examined. Autopsies had already been performed on the decedents as all deaths in which there is a suspicion of drug involvement have full autopsies. Toxicological examination by gas chromatography with mass spectrometry was performed on all specimens by a commercial reference laboratory to identify individual substances. Cases chosen for the study included only drug overdose decedents who died in the state of Vermont between January 2001 and December 2006. Overdose deaths in which methadone was cited as a cause of death, alone or in combination with another illicit or prescribed drug were classified as methadonerelated deaths. The classification of the cause of death was determined by a forensic pathologist. This determination was dependent on the circumstances of death, medical and scene background investigation, and the presence of a lethal level of methadone and/or its major metabolite, 2-ethylidene-1,5-dimethyl-3,3-diphenylpyrrolidine either alone or in combination with other drugs, as determined by the pathologist. The presence of the drug on its own was not enough to classify the case as a methadone-related death. For all methadone-related deaths, we examined the gender, age, geographical location, medical history of individual and family, the indication of and dose for methadone prescription if available, other prescribed drugs, the blood levels of methadone, 2-ethylidene-1,5-dimethyl-3,3-diphenylpyrrolidine, and other prescribed and illicit drug levels.

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We identified the total cases as either belonging in a diversion group or in a prescription group. The methadone-related deaths attributed to diversion were determined by the absence of a physician_s prescription. If the individual had a prescription for any reason, including, but not limited to MMT, they were included in the prescription group.

Calculations and Trend Analysis We calculated the mean and median age, mean and median levels of methadone, percent male decedents, manner of death, the number and percentages of deaths due to methadone only, methadone with illicit drugs, methadone with other prescription drugs (not necessarily prescribed to them), and methadone with alcohol. Finally, we identified the total number of deaths and the total number of overdose deaths reported to the OCME in the state of Vermont between 2001 and 2006 for comparative analysis and to identify trends over time.

RESULTS Of 4317 deaths reported to the OCME in the state of Vermont between 2001 and 2006, 336 were overdose deaths and 76 of those were attributed to methadone. Over this time period, there was a 4-fold increase in overdose deaths from 2001 (17 deaths) to 2006 (79 deaths). The number of methadonerelated deaths increased from 2 to 29 per year over the 6-year time period. The proportion of methadone-related deaths increased by 300% from 2001 (0.6% of reported deaths, 11.8% of overdose deaths) to 2006 (3.4% of reported deaths, 36.7% of overdose deaths) (Table 1). Because we found the total number of reported deaths and overdose-related deaths to change significantly from 2001 to 2002, a separate analysis was performed looking at the same data from 2002 to 2006. Between 2002 and 2006, the total number of overdose deaths in Vermont rose from 47 (6.3% of reported deaths) to 79 (9.4% of reported deaths). The number of methadone-related deaths during this time increased from 8 (1.7% of reported deaths, 17.0% of overdose deaths) to 29 (3.4% of reported deaths, 36.7% of overdose deaths), representing a greater than 2-fold increase in methadone-related deaths in 5 years. The mean age of the decedents was 36 years, the median was 35 years (range, 16Y74 years) and 55 (72%) were male. The mean level of methadone was 457 ng/mL (range, 50Y3793 ng/mL). The manners of death were classified as follows: 64 (84%) accident, 9 (12%) undetermined, and 3 (4%) suicide (Table 2). The substances causing death were determined to be methadone

TABLE 2. Decedent Characteristics and Manner of Death Number (%) Mean age (yr) Median age (yr) Sex Male Female Mean methadone level (ng/ml) Manner of death Accident Undetermined Suicide

36 35 55 (72) 21 (28) 457

Range 16Y74 16Y74

50Y3793

64 (84) 9 (12) 3 (4)

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DISCUSSION

TABLE 3. Decedent Groups Number (%) Methadone only with only illicit† drugs with only prescription drugs with both illicit† and prescribed drugs with only alcohol How methadone obtained Illegal drug diversion Physician prescription Indication Chronic pain Acute pain/injury Opioid dependence (MMT)‡ Unknown

The Methadone Epidemic

Percent With Rx*

26 (34) 13 (17) 29 (38) 5 (7) 3 (4) 51 (67) 25 (33) 15 (20) 2 (3) 2 (3) 6 (8)

60 8 8 24

*Rx indicates physician methadone prescription. †Excludes cannabinoids. ‡Neither decedent in outpatient MMT in Vermont. MMT indicates methadone maintenance treatment.

alone in 26 (34%), methadone with only other prescribed medications in 29 (38%), methadone with only illicit drugs (excluding tetrahydrocannabinol) in 13 (17%), methadone with both illicit and prescribed medications in 5 (7%), and methadone with ethanol in 3 (4%) (Table 3). The most frequent prescription drugs used in combination with methadone were benzodiazepines, antidepressants, and other opioids. The methadone was obtained by illegal diversion (sale, gift, or theft) in 51 (67%) cases. In the remaining 25 (33%) cases, the methadone was obtained by physician_s prescription for chronic pain in 15 (60%), acute pain or injury in 2 (8%), methadone maintenance therapy for heroin dependence in 2 (8%), and unknown reasons in 6 (24%) (Fig. 1, Table 3).

The prevalence of methadone-related overdose deaths is increasing in the state of Vermont. This echoes a similar increase throughout the entire United States.1 The number of overdose deaths in our state has increased by over 4-fold during the time between 2001 and 2006, and over 2-fold in the years from 2002 to 2006. The number of methadone-related deaths has increased over 14-fold, from 2 to 29 per year in 2001 and 2006, respectively (Fig. 1). The proportion of overdose deaths that are methadone-related has similarly increased from 12% to 37% of overdose deaths between 2001 and 2006, an increase of over 300% in 6 years. In 2006, methadone-related deaths comprised 3% of the total deaths reported to the OCME for the entire state. Interestingly, none of these deaths was associated with the state_s outpatient MMT programs. It is clear that there is a public health problem and it is essential to attempt to understand why methadone-related deaths are steadily climbing. The most common substances causing death in our population were methadone alone or in combination with other prescription drugs (34% and 38%, respectively). The most frequent prescription drugs were benzodiazepines, other opioids, and antidepressants. This is not surprising as there are many articles that indicate a synergistic respiratory depressant effect of methadone and other central nervous system depressants. Corkery et al discuss the fact that most methadone deaths occur as a result of respiratory depression. They argue that this is more likely to occur when used in combination with other opiates, alcohol, or benzodiazepines.22 Others have advertised the particular danger of alcohol and benzodiazepines with methadone.3,23Y25 As a result of such reports of overdose and death associated with concurrent benzodiazepine use, in 2006 the Federal Drug Administration issued a public health advisory against using other drugs with methadone.26 In addition, Roxane Laboratories, Inc. added precautionary statements against using benzodiazepines with methadone.27 MMT programs in Vermont were shown to be safe and effective in our study; patients in these programs comprise a negligible number of the methadone-related deaths in the state. Over the 6-year time period, only 2 of the 76 decedents (3%) were enrolled in a methadone maintenance program at the time

FIGURE 1. Methadone-related deaths in Vermont. * 2011 Lippincott Williams & Wilkins

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of death. One of the decedents was in an inpatient facility receiving treatment for heroin dependence and an eating disorder, and the other was enrolled in an outpatient methadone clinic in Massachusetts and died in Vermont, having received takeaway doses for a vacation. Thus, strictly speaking, there have been no methadone-related deaths involving patients enrolled in outpatient MMT in Vermont between 2001 and 2006. Rather, it appears the populations most at risk are those obtaining diverted methadone for abuse (67% of the total decedents) and those taking methadone for chronic pain (20% of the total decedents). There may be several as of now unidentified reasons for the increase in both methadone abuse and methadone-related deaths. However, there are 3 compelling reasons that will be discussed here. One is the relation of methadone-related deaths to methadone maintenance programs. Although this has been found to be negligible in Vermont, a significant proportion of methadone-related deaths in other states and abroad have been in those in maintenance programs.3,25,28,29 Second, is an increase in the use of methadone as a treatment for chronic and acute pain. Finally, the increase in prescription use has had the unintended consequence of significant illegal drug diversion. The latter 2 explanations account for at least 90% of methadonerelated deaths in the state of Vermont. Williamson et al has explored the safety of methadone prescribing in South Australia due to an increase in methadone prescribing for chronic pain. They found that their MMT program was generally safe, as shown by a decline in mortality despite higher doses and increased availability of takeaway doses. This was attributed to the fact that at higher doses, the opioid craving is decreased, and thus patients are less likely to seek other drugs. In addition, they found that the increase in prescribing methadone for chronic pain was the likely source of the large problem of illegal diversion they are experiencing.3 However, some studies suggest MMT programs contribute to a significant proportion of the methadone-related deaths. Gagajewski and Apple found that 34.7% of decedents in Minnesota between 1992 and 2002 were enrolled in MMT programs at the time of death while 39% were illicit users (diverted methadone) and 15% were chronic pain patients.28 Shah et al looked at methadone-related deaths in New Mexico between 1998 and 2002. They found that at least 21.7% of the total decedents were in MMT programs and 18.9% had physician prescriptions for chronic pain. Only 7.7% of the decedents in New Mexico had definitively obtained diverted methadone.29 From these data and from our own study, it is apparent that the amount of drug diversion, chronic pain-related and MMT-related deaths varies with geography. This likely is dependent on several factors intrinsic to the area. For example, the population and the prevalence of opioid dependence, the policies of the MMT clinics regarding dosing, takeaways and patient follow-up, the local climate for physician prescribing of methadone for chronic pain, and the amount of demand for drug diversion will inevitably change in different areas, thus making it important to study and understand one_s own population and risk stratification. Vermont is a small state with a relatively homogeneous population. There are 3 main methadone clinics with 1 mobile unit and plans for a fourth clinic to open soon. Our clinics have strict patient follow-up and limit the number of takeaways that are available to patients. The state program guidelines are significantly more restrictive than the federal guidelines on takeaways. Takeaways are a privilege of long-term, stable patients. It is unclear why Vermont has had no MMT-associated methadone deaths over the study period while other similar studies in other states have shown rates above 20% of all methadone-

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related deaths over comparable study periods. Possible explanations are the restrictions on takeaway doses, a smaller population and/or closer follow-up. There are 2 significant limitations of this study. One is the difficulty in obtaining information regarding the sources of methadone. We rely on the assistant medical examiner and police reports as well as medical records when they are available. This is often not sufficient to exactly categorize the data and may have resulted in an overestimate of the amount of drugs obtained via diversion. A second possible confounder in our data is a result of a change in leadership within the OCME during the study period. This change resulted in an increase of the number of autopsies performed by the staff. The numbers of overdose deaths from 2001 may be falsely low which may have resulted in an overestimate of the rate of increase of methadone-related deaths. For this reason, a second analysis was performed, looking at the increase in methadone-related deaths from 2002 to 2006. This increase, although smaller, still represented a greater than 2-fold increase in methadone-related deaths during this time period. This figure is likely a more representative change, although it is impossible to state this with certainty. Despite the limitations of the study, it is clear that methadonerelated deaths are increasing at a rapid rate in Vermont, as in other states in New England and in the United States as a whole. Our focus in Vermont should turn to further exploring our population at risk to determine what we can do to eliminate the growing problem. As stated above, in many cases the source of methadone is unknown, therefore it is difficult to determine to what extent diversion is a significant problem. Our data suggest it to be an important factor in Vermont. The increase in prescriptions for chronic pain is an additional area to investigate for possible adjustments. Education of clinicians regarding the increasing number of methadone-related deaths, the potential for abuse and diversion, and the pharmacokinetics of methadone may help halt this epidemic and reduce the number of fatalities from this drug. ACKNOWLEDGMENTS The authors thank Brittany Philbin for her time searching the medical examiner database, and Drs Wayne Kurz, Todd Mandell, and Teresa Madden for their helpful comments and thoughtful discussions. REFERENCES 1. Fingerhut LA. Increases in methadone-related deaths: 1999Y2004 [CDC National Center for Health Statistics]. 2006. Available at: http://www.cdc. gov/nchs/products/pubs/pubd/hestats/methadone1999Y04/methadone 1999Y04.htm. Accessed August 10, 2007. 2. Drummer OH. Recent trends in narcotic deaths. Ther Drug Monit. 2005;27:738Y740. 3. Williamson PA, Foreman KJ, White JM, et al. Methadone-related overdose deaths in South Australia, 1984Y1994. Med J Aust. 1997;166:302Y305. 4. Courtwright DT, Joseph H, Des Jarlais DC. Addicts Who Survived: An Oral History of Narcotic Use in America, 1923Y1965. Knoxville, TN: University of Tennessee Press; 1989. 5. Andima H, Krug D, Bergner L, et al. A prevalence estimation model of narcotics addiction in New York City. Am J Epidemiol. 1973;98:56Y62. 6. Joseph H, Stancliff S, Langrod J. Methadone maintenance treatment (MMT): a review of historical and clinical issues. Mt Sinai J Med. 2000;67:347Y364. 7. Halpern M, Rho YM. Deaths from narcotism in New York City: incidence, circumstances, and postmortem findings. NY State J Med. 1966;66:2391Y2408.

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8. Isbell H, Vogel VH. The addiction liability of methadone (amidone, dolphine, 10,820) and its use in the treatment of the morphine abstinence syndrome. Am J Psych. 1949;195:909Y914. 9. Dole VP, Nyswander ME. A medical treatment for diacetylmorphine (heroin) addiction: a clinical trial with methadone hydrochloride. JAMA. 1965;193:80Y84. 10. Dole VP, Nyswander ME, Kreek MJ. Narcotic blockade. Arch Intern Med. 1966;118:304Y309. 11. Joseph H, Appel P . Historical perspectives and public health issues. In: Center for Substance Abuse Treatment, US Department of Health and Human Services, eds. State Methadone Treatment Guidelines. Treatment Improvement Protocol (TIP) Series #1. Washington, DC: DIANE Publishing; 1993:11Y24. 12. Gearing FR, Schweitzer MD. An epidemiologic evaluation of long-term methadone maintenance treatment for heroin addiction. Am J Epidemiol. 1974;100:101Y112. 13. Joseph H, Woods J. A point in time: the impact of expanded methadone maintenance treatment on citywide crime and public health in New York City 1971Y1973. Belg Arch Public Health. 1995;53:215Y231. 14. Godfrey C, Stewart D, Gossop M. Economic analysis of costs and consequences of the treatment of drug misuse: 2-year outcome data from the National Treatment Outcome Research Study (NTORS). Addiction. 2004;99:697Y707. 15. Marsch LA. The efficacy of methadone maintenance interventions in reducing illicit opiate abuse, HIV risk behavior and criminality: a meta-analysis. Addiction. 1998;93:515Y532. 16. Metrebian N, Shanahan W, Stimson GV. Feasibility of prescribing injectable heroin and methadone to opiate-dependent drug users: associated health gains and harm reduction. Med J Aust. 1998;168:596Y600. 17. Coid J, Carvell A, Kittler Z, et al. Opiates, criminal behavior and methadone treatment [Home Office RDS]. 2000. Available at: http://www.homeoffice.gov.uk/rds/pdfs/crimebehav.pdf. Accessed August 10, 2007.

The Methadone Epidemic

18. Ward J, Hall W, Mattick RP. Role of maintenance treatment in opioid dependence. Lancet. 1999;353:221Y226. 19. Wilson P, Watson R, Ralston GE. Methadone maintenance in general practice: patients, workload, and outcomes. Br Med J. 1994;309: 641Y644. 20. Caplehorn JR, Dalton MS, Haldar F, et al. Methadone maintenance and addicts_ risk of fatal heroin overdose. Subst Use Misuse. 1996;31:177Y196. 21. Risser D, Ho¨nigschnabl S, Stichenwirth M, et al. Mortality of opiate users in Vienna, Austria. Drug Alcohol Depend. 2001;64:251Y256. 22. Corkery JM, Schifano F, Ghodse AH, et al. The effects of methadone and its role in fatalities. Hum Psychopharmacol Clin Exp. 2004;19:565Y576. 23. Levine B, Wu SC, Dixon A, et al. Site dependence of post mortem blood methadone concentration. Am J Forensic Med Pathol. 1995;16:97Y100. 24. Rogers WO, Hall MA, Brissie RM, et al. Detection of alprazolem in three cases of methadone/benzodiazepine overdose. J Forensic Sci. 1997;42:155Y156. 25. Seymour A, Black M, Jay J, et al. The role of methadone in drug-related deaths in the west of Scotland. Addiction. 2003;98:995Y1002. 26. FDA Public Health Advisory [FDA]. 2006. Available at: http://www.fda.gov/cder/drug/advisory/methadone.htm. Accessed September 2, 2007. 27. Roxane Laboratories, Inc. Methadone Hydrochloride Drug Information [FDA] [revised]. 2006. Available at: http://www.fda.gov/cder/foi/label/ 2006/006134s028lbl.pdf. Accessed September 2, 2007. 28. Gagajewski A, Apple FS. Methadone-related deaths in Hennepin County, Minnesota: 1992Y2002. J Forensic Sci. 2003;48:668Y671. 29. Shah N, Lathrop SL, Landen MG. Unintentional methadone-related overdose death in New Mexico (USA) and implications for surveillance, 1998Y2002. Addiction. 2004;100:176Y188.

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ORIGINAL ARTICLE

Prevalence of Alcohol in Blood Samples From Traffic Accident Cases in Turkey Serap Annette Akgu¨r, MD, PhD,* Hasan Ertas, PhD,Þ A. Ender AltN ntoprak, MD, PhD,þ Meral Ozkan, PhD,* and Gu¨l KitapcNoglu, MD, PhD§ Abstract: Alcohol is one of the main causes of traffic accidents worldwide. With a population of 70 million, 12 million vehicles, and 18 million drivers (16% women), Turkey is one of the European countries that has a high incidence of road traffic accidents. In accordance with Turkish laws, subjects were considered to be positive when alcohol blood concentration exceeded 50 mg/100 mL. The objective of the present study was to obtain reliable and comparable data about alcohol use in traffic cases in Turkey. All cases are admitted to the emergency department at Ege University Medical Faculty. The cases from police officers are described as traffic control cases. Alcohol was detected in the blood of about 54.4% of the traffic-related cases during October 2005 to March 2007. It has been observed that, in 17.4% of the traffic accident cases, the blood alcohol level was 50 mg/dL or less, which is the legal limit in Turkey for car drivers. Alcohol prevalence was 57.2% in male cases and 43.6% in female cases. In alcohol-positive cases; the ratios for males were 1.73 times more frequent in traffic-related cases. Prevalence data will help traffic safety professionals to adequately allocate resources and plan future efforts in reducing drinking-and-driving behavior and thereby reduce traffic accidents. Key Words: traffic accidents, alcohol, Turkey (Am J Forensic Med Pathol 2011;32: 136Y139)

A

lcohol is one of the main causes of traffic accidents worldwide. From several studies, it has been documented that drugs affecting the central nervous system may impair driving performance and lead to the possibilities of their involvement in traffic accidents. The contribution of alcohol to traffic accidents has been evaluated in a large number of epidemiological and pharmacological studies. All these studies highlighted the increased risk of road crashes for drivers under the influence of alcohol.1Y4 According to the World Health Organization reports, traffic accidents are among the main reasons for public health damage: in the fifth place in undeveloped countries, and in the 10th place in developed countries.5 With a population of 70 million, 12 million vehicles, and 18 million drivers (16% women), Turkey is one of the European countries that has a high incidence of road traffic accidents. According to the statistics released by Turkish Security Headquarters, in the first 3 months in 2007, 162,369 and, in March, 56,139 traffic accidents occurred.6 With these data, Turkey is in the first place in Europe and seventh worldwide in traffic accidents. It is known that Izmir, which is the third largest city in Turkey, is in the third place regarding the number of traffic accidents on the basis of data compiled in 2007.

Manuscript received February 5, 2008; accepted May 7, 2008. From the *Poison Research and Application Center and Departments of †Chemistry and ‡Psychiatry, and §Biostatistics, Faculty of Medicine, Ege University, Bornova, Izmir, Turkey. Reprints: Serap Annette Akgu¨r, MD, PhD, Ege University Poison ¨ .TNp Fak. ARGEFAR Research and Application Center, ZAUM (E.U YanN), 35100 Bornova, Izmir, Turkey. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0136 DOI: 10.1097/PAF.0b013e3182186f07

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Because human performance is affected by using alcohol, an epidemiological study of the involvement of alcohol is a fundamental interest for road safety. This study aimed at obtaining reliable and comparable data about alcohol use for traffic cases in Turkey.

MATERIALS AND METHODS The cases were assessed where the individuals were involved in traffic violations and traffic accidents who were admitted to the emergency medicine department for an injury caused by a traffic crash between October 2005 and March 2007. The cases from police officers are described as traffic control cases (TCCs). All TCCs were admitted to the hospital for blood alcohol testing after they were tested and determined as positive for alcohol use by an on-site breath analyzer by police officers because of their slurring speech, smell of alcohol, tremor, and so on, in the controls. The toxicological analysis was performed at Ege University Poison Research and Application Center in Izmir. Six hundred sixtytwo blood specimens were screened for alcohol using CEDIA (cloned enzyme donor immunoassay), and positive cases were confirmed by the HS-GC/MS (head spaceYgas chromatograph/ mass spectrometer) method. A sample was considered positive for alcohol when the blood alcohol concentration (BAC) was greater than 5 mg/dL. The reported cases were classified according to the type of traffic cases; vehicle accidents (VAs; the traffic accidents involved only car), road accidents (RAs; passengerbased traffic accidents), motorbike accidents (MAs), and TCCs. Statistical analysis was performed by using SPSS 15.0 (SPSS Inc, Chicago, Ill).

RESULTS Of the traffic-related 662 cases, male accounted for 83.4% (n = 552), and females 16.6% (n = 110) (Fig. 1). Three hundred sixty-four cases were found to be alcohol positive. The alcohol results of traffic-related cases are shown in Table 1. When the frequency of alcohol prevalence is compared on the basis of gender,

FIGURE 1. Number of cases based on gender. Am J Forensic Med Pathol

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TABLE 1. Distribution of Alcohol-Positive and Alcohol-Negative Cases According to Gender Alcohol

Gender Total

Male Female

Alcohol Positive

Alcohol Negative

n

%

n

%

n

%

316 48 364

57.2 43.6 55.0

236 62 298

42.8 56.4 45.0

552 110 662

100.0 100.0 100.0

Total

the prevalence of alcohol positiveness in women was significantly lower than that of males. In male cases, 57.2% were positive; in female cases, 43.6% were positive for alcohol. The ratios for males were 1.73 times more frequent in traffic-related cases (Fisher exact test, P = 0,012; odds ratio, 1.73 [95% confidence interval, 1.145Y2.613]). As it is shown, the alcohol positiveness is significantly different between all traffic groups (Table 2). The percentage of alcohol levels in traffic accidents and TCCs are given in Figure 2. Table 3 summarizes the statistical evaluation of BAC of each group according to gender. Mean BACs between the alcoholpositive traffic accident cases (APTACs) (146.63 [SD, 99.96] mg/dL) and the alcohol-positive TCCs (APTCCs) (78.56 [SD, 45.41] mg/dL) were significantly different (t = 4.551; P = 0.000001). In 364 alcohol-positive cases (APCs), 2.6% had an alcohol concentration at level I (blood alcohol between 0.01 and 0.19 g/L), 12.4% were at level II (blood alcohol between 0.20 and 0.50 g/L), 23.3% were at level III (blood alcohol between 0.50 g/l and 1 g/L), and 16.3% were at level IV (blood alcohol 91 g/L) (Fig. 3). In the APTACs, 17.3% (n = 8) were under the legal limit, and the mean level was 33.63 (SD, 14.74). In the APTCCs, 28.9% (n = 91) were under the legal limit, and the mean level was 32.40 (SD, 11.95). The mean alcohol levels over the legal limit were 155.1 (SD, 91.01) (n = 30) in the APTACs and 96.90 (SD, 40.93) (n = 224) in the APTCCs. The distribution of age in cases is as follows: 3% were younger than 18 years, 72.3% were between 18 and 39 years of age, 15.6% were between 40 and 49 years of age, and 9.1% were older than 50 years. The frequency of the traffic cases is given in Table 4 and is depicted in Figures 4 and 5.

DISCUSSION AND CONCLUSION For many years, attention has primarily focused on alcohol, and most countries have established legal limits for BAC during driving. In accordance with Turkish laws, subjects were considered

FIGURE 2. Percent of alcohol levels in traffic accidents and TCCs.

to be positive when alcohol blood concentration exceeded 50 mg/ 100 mL. The Law Prohibiting Teenagers From Drinking regulates minimum drinking age in Turkey, and people younger than 18 years are prohibited from purchasing and consuming alcohol.

Drinking-and-Driving Legislation in Turkey The law that controls driving under the influence (DUI) of alcohol in Turkey is the Turkish Road Traffic Law. The Road Traffic Law and Related Legislation-Prohibition for DUI of alcoholic beverages, narcotics, and euphoric substances, section 97 states ‘‘Impaired individuals by using narcotics and euphoric substances and alcoholic beverages are prohibited for driving under the influence of these substances on roads. Observing supporting evidence of impairment in an individual due to the use of psychotropic substance that have features like narcotics, sedatives, and euphoric substances needs to be examined and sent to Forensic Medicine Council if present or to the health services associated with Ministry of Health and Social Services for blood and urine analysis. If these analyses are not available in these places, the samples are sent to the nearest official Health Service or Criminal Police Laboratories.’’ According to Road Traffic Law article number 48, the driver’s licenses of drivers who have consumed alcohol above the limit are temporarily suspended for 6 months in case offirst act and for 2 years in case of second act. At the end of the duration of the second act, licenses of suspended drivers are subjected to behavior development course for drivers. If he/she succeeds on the course, he/she is considered to be eligible to obtain a driver’s license again. In the case of a third or further action committed by the drivers, they are put into jail for up to 6 months, and their driving license is taken for 5 years.7

TABLE 2. Gender and Alcohol Positiveness According to the Traffic Cases VAs Gender Male

Female

Alcohol positive Alcohol negative Total Alcohol positive Alcohol negative Total

RAs

MAs

TCCs

Total

n

%

n

%

n

%

n

%

n

%

W2

df

P

26 115 141 6 40 46

18.4 81.6 100.0 13.0 87.0 100.0

8 43 51 0 19 19

15.7 84.3 100.0 0.0 100.0 100.0

6 40 46 0 2 2

13.0 87.0 100.0 0.0 100.0 100.0

276 38 314 42 1 43

87.9 12.1 100.0 97.7 2.3 100.0

316 236 552 48 62 110

57.2 42.8 100.0 43.6 56.4 100.0

280.01

3

0.000001

84.82

3

0.000001

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TABLE 3. Blood Alcohol Concentrations (Number of Cases, Mean and SD, and Minimum and Maximum Levels [in mg/dL]) of Groups, According to Gender n Male VAs RAs MAs TCCs Total Female VAs TCCs Total Total VAs RAs MAs TCCs Total

Mean

SD

Minimum

103.1 84.8 79.0 43.9 60.7

12 157 43 10 10

417.0 375.0 247.0 237.0 417.0

6 41 47

67.7 83.2 81.2

36.5 54.8 52.7

11 12 11

101.0 235.0 235.0

32 8 6 315 361

132.0 227.9 116.2 78.6 87.2

98.9 84.8 79.0 45.4 59.7

11 157 43 10 10

417.0 375.0 247.0 237.0 417.0

In our study, alcohol was detected in the blood at about 55.0% in all the traffic-related cases. If the classified groups are closely examined, prevalence of alcohol for traffic accidents is distributed as 13.8% for VAs, 11.4% for RAs, and 12.5% for MAs. For TCCs, the rate of those who were admitted to the hospital for blood alcohol testing after they were tested and determined as positive by an on-site test was very high (77.3%) as expected. Alcohol-impaired driving is a serious threat to health. It is reported that, in the United States, 40% of traffic deaths and 9% of traffic injuries are alcohol related. Drinking and driving perhaps represents a biggest obstacle in American roadways.3,8 Similarly, in the European Union, 30% to 50% of traffic accidents are also related to alcohol intake.9 The alcohol prevalence in traffic cases is as follows: 29% in Greece,10 46% in Hungary,11 26% in France,12 and 49.0% in Italy.13 In this study, in APCs, the ratios for males were 1.73 times more frequent in traffic-related cases. In Turkey, consumption of alcohol is widespread, particularly in men, and among the drivers, 84% are men according to recently released data (March 2007).6 A reduction in the legal blood alcohol limit has been widely thought as the most important step for reducing alcoholrelated traffic accidents. Many drivers consider these legal limits as a guide to safe drink-driver’s levels.14 In our study, the prevalence below the legal limits of alcohol positiveness in traffic accident cases was 17.3%, and in the TCCs, it was 29.9%.

FIGURE 3. General overlook of the distribution of blood alcohol levels in APCs.

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VAs n

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%

G18 yr 5 3.5 19Y39 yr 91 64.5 40Y49 yr 24 17.0 950 yr 21 14.9 Total 141 100.0 Female G18 yr 0 0.0 19Y39 yr 36 78.3 40Y49 yr 4 8.7 950 yr 6 13.0 Total 46 100.0

Male

146.9 227.9 116.2 77.9 88.1

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TABLE 4. The Number of Cases According to Age and Gender

Maximum

26 8 6 274 314

&

RAs n

%

MAs n

%

TCCs n

%

Total n

6 11.8 8 17.4 0 0.0 19 23 45.1 30 65.2 254 81.2 398 10 19.6 3 6.5 49 15.7 86 12 23.5 5 10.9 10 3.2 48 51 100.0 46 100.0 313 100.0 551 1 5.3 0 0.0 0 0.0 1 10 52.6 1 50.0 33 76.7 80 3 15.8 1 50.0 9 20.9 17 5 26.3 0 0.0 1 2.3 12 19 100.0 2 100.0 43 100.0 110

% 3.4 72.2 15.6 8.7 100.0 0.9 72.7 15.5 10.9 100.0

Among drivers who were suspected to be influenced by alcohol, the BACs below the legal limits were found to be 32%, 18%, and 2% of the Norwegian, Icelandic, and Finnish cases, respectively (legal limit for BAC, 0.05%). Also, they were found to be in 10% of the Danish cases (BAC, 0.08%) and 20% of the Swedish cases (BAC, 0.02%).15,16 A prospective study that enrolled 2354 patients admitted to an Italian emergency department for an injury caused by a traffic accident showed that the BAC was under the legal limit (50 mg/dL) in 10.7% of them.17 A number of studies showed evidence that imposing lowered legal blood alcohol limits has a beneficial effect on traffic safety.18 In the recent years, several European countries have changed their limits.14 In a study reviewed by Moskowitz and Fiorentino19 in 2000, it is reported that drivers with BAC of 50 mg/dL have a significantly impaired driving ability. And even a BAC of 20 mg/dL has led to a reduction in driving ability. In another study, it has been shown that those with BAC of 40 mg/dL were significantly different than those with BAC 0.0 mg/dL in driving impairment.20 The lower legal limit was reduced from 50 to 20 mg % on July 1, 1990, in Sweden. Norstro¨m and Laurell21 and Borschos22 have pointed out an important decrease in the number of traffic accidents after the legal alcohol limit was reduced to 20-mg/dL level. Detection of alcohol and other psychoactive substances in the blood of drivers involved in traffic accidents in Turkey is enforced by law. However, police authorities have preferred to check mostly the level of alcohol in the exhaled air using a breath analyzer, not any other test for drugs. However, some very

FIGURE 4. Frequency of cases in males according to age. * 2011 Lippincott Williams & Wilkins

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6. Traffic Accidents Statistics in Turkey, 2007. Available at: http://www.egm.gov.tr/teadb/istatistikler/orta.htm. Accessed September 3, 2007. 7. Turkish Highway Traffic Regulations. Turkish Highway Traffic Statute, number: 2918. Available at: http://www.trafik.gov.tr/mevzuat/ mevzuat_kanun_ve_yonetmelikler.asp. Accessed September 16, 2007. 8. Williams AF. Alcohol-impaired driving and its consequences in the United States: the past 25 years. J Safety Res. 2006;37:123Y138. 9. European Commission. Road death: a terrible, human, social and economic cost. EU Bulletin. 2000;6:1.4.49. 10. Papadodima SA, Athanaselis SA, Stefanidou ME, et al. Driving under the influence in Greece: a 7-year survey (1998Y2004). Forensic Sci Int. 2007;174:157Y160.

FIGURE 5. Frequency of cases in females according to age.

recent studies on DUI psychoactive substances would allow a more considerable attention for the problem in road traffic safety in Turkey.23 As we closely examined the data from traffic statistics, among the reasons for withdrawal of driver’s license at 95% was DUI of alcohol in our country. Despite the enormous public health burden of traffic accidents, there exist few studies about drinking-driving on Turkish roadways. The National Forensic Medicine Council releases annual reports including samples sent by forensic doctors or as instructed by a court for legal purposes, especially for fatal accidents. There are no long-term data on the percentage of alcohol prevalence in nonfatal traffic accidents and TCCs in Turkey. Commonly, self-reported data have been widely adopted as complements to roadside surveys. A number of studies showed that the contributions of alcohol to traffic accidents are decreased because of attention to the problem.8 Studies on the prevalence of drinking and driving in the general population also have significant implications for public health policy. Prevalence data will help traffic safety professionals to adequately allocate resources and plan future efforts in reducing drinking-and-driving behavior and thereby reduce traffic accidents in Turkey. REFERENCES 1. Smink BE, Ruiter B, Lusthof KJ, et al. Driving under the influence of alcohol and /or drugs in the Netherlands 1995Y1998 in view of German and Belgian legislation. Forensic Sci Int. 2001;120: 195Y203. 2. Mura P, Kintz P, Ludes B, et al. Comparison of the prevalence of alcohol cannabis and other drugs between 900 injured drivers and 900 control subjects: results of a French collaborative study. Forensic Sc Int. 2003;133:79Y85. 3. Chou SP, Dawson DA, Stinson FS, et al. The prevalence of drinking and driving in the United States, 2001-2002: results from the national epidemiological survey on alcohol and related conditions. Drug Alcohol Depend. 2006;83:137Y146. 4. Kruger HP, Vollrath M. The alcohol-related accident risk in Germany: procedure, methods and results. Accid Anal Prev. 2004;36:125Y133. 5. Public Health Statistics throughout the World in 2000. World Health Organization Reports. Available at: www.who.ch. Accessed September 3, 2007.

11. Fell JC, Voas RB. The effectiveness of reducing illegal blood alcohol concentration (BAC) limits for driving. J Safety Res. 2006;37: 233Y243. 12. Mercier-Guyon C. Lowering the BAC limit to 0.05: results of the French experience. Presented at Transportation Research Board 77th Annual Meeting; Washington, DC; 1998. 13. Caputo F, Trevisani F, Bernardi M. Alcohol misuse and traffic accident. Lancet. 2007;369:463Y464. 14. Carmen del Rı´o M, Gomez J, Sancho M, et al. Alcohol, illicit drugs and medicinal drugs in fatally injured drivers in Spain between 1991 and 2000. Forensic Sci Int. 2002;127:63Y70. 15. Christophersen AS, Ceder G, Kristinsson J, et al. Drugged driving in the Nordic countriesVa comparative study between five countries. Forensic Sci Int. 1999;106:173Y190. 16. Augsburger M, Donze´ N, Me´ne´trey A, et al. Concentration of drugs in blood of suspected impaired drivers. Forensic Sc Int. 2005;153:11Y15. 17. Fabbri A, Marchesini G, Morselli-Labate AM. Positive blood alcohol concentration and road accidents: a prospective study in an Italian emergency department. Emerg Med J. 2002;19:210Y214. 18. Mann RE, Macdonald S, Stoduto S, et al. The effects of introducing or lowering legal per se blood alcohol limits for driving: an international review. Accid Anal Prev. 2001;33:569Y583. 19. Moskowitz H, Fiorentino D. A Review of the Literature on the Effects of Low Doses of Alcohol on Driving-Related Skills (DOTHS 809 028). National Highway Traffic Safety Administration. Washington, DC: Department of Transportation; 2000. 20. Compton RP, Blomberg RD, Moskowitz H, et al. Crash risk of alcohol impaired driving. In: Mayhew DR, Dussault C, eds. Proceedings of Alcohol, Drugs and Traffic SafetyVT 2002: 16th International Conference on Alcohol, Drugs and Traffic Safety: August 4Y9, 2002. Montreal, Canada: International Council on Alcohol, Drugs and Traffic Safety (ICADTS); 2002:39Y44. 21. Norstro¨m T, Laurell H. Effects of lowering the legal KAD-limit in Sweden. In: Mercier-Guyon C, ed. Proceedings of the 14th International Conference on Alcohol, Drugs and Traffic SafetyVT’97: September 21Y26, 1997. Annecy, France: Centre d’Etudes et de Recherches en Medecine du Traffic; 1997:87Y94. 22. Borschos B. An evaluation of the Swedish drunken driving legislation implemented on February 1, 1994. In: Laurell H, and Schlyter F, eds. International Conference on Alcohol, Drugs and Traffic SafetyVT’2000: May 22Y26, 2000. Stockholm, Sweden: International Council on Alcohol, Drugs and Traffic Safety (ICADTS); 2000. 23. Akgu¨r SA, Do¨nmez T, Yemizcigil A. Oral fluid analysis for driving under the influence of drugs. Adli TNp Bu¨lteni. 2006;11:19Y22.

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ORIGINAL ARTICLE

Sudden Death as a Complication of Bacterial Endocarditis Angela Byramji, MBBS,* John D. Gilbert, FRCPA,Þ and Roger W. Byard, MBBS, MD*Þ

Abstract: Three cases are reported to demonstrate the range of possible lesions and wide variation in lethal mechanisms that may be found in cases of unexpected death subsequently shown to be due to bacterial endocarditis. Case 1: A 36-year-old man was found dead on his bedroom floor surrounded by drug paraphernalia. At autopsy, acute myocardial ischemia was present caused by coronary artery ostial occlusion complicating acute bacterial endocarditis of the aortic valve. Case 2: A 54-year-old man with chronic renal failure was found dead in bed at home. At autopsy, a left middle cerebral artery territory cerebral infarct was present due to septic embolization from bacterial endocarditis involving the aortic valve. Case 3: A 23-year-old man was found collapsed in a pool of blood. At autopsy, upper airway hemorrhage from an arteriobronchial fistula was present caused by septic pulmonary infarction from previous endocarditis of a congenital ventricular septal defect. This report demonstrates that bacterial endocarditis may still be a cause of sudden and unexpected death presenting to forensic mortuaries and that the underlying mechanisms may involve complex sequences of pathological changes that compromise vascular function. Key Words: bacterial endocarditis, embolization, septic infarct, arteriobronchial fistula (Am J Forensic Med Pathol 2011;32: 140Y142)

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nfective endocarditis may be associated with significant mortality due mainly to the interactions of comorbidities and endorgan dysfunction.1 Mycotic aneurysms may uncommonly complicate infective endocarditis leading to vascular rupture or local sepsis.2 Abscesses are another rare complication that may lead to the formation of fistulous tracts. Three cases of sudden death are reported where lethal sequelae of bacterial endocarditis were unexpectedly revealed at autopsy demonstrating the wide range of fatal mechanisms that may be encountered in this condition.

CASE REPORTS Case 1 A 36-year-old man was found dead on his bedroom floor surrounded by drug paraphernalia. External examination of the body revealed no evidence of trauma and no injection sites. At autopsy, the heart was enlarged (638 g) with multifocal areas of fibrous scarring and mottling suggestive of recent ischemic damage. A large amount of vegetation/thrombus material was adherent to the aortic valve with infiltration of the underlying myocardium extending to involve the anterior leaflet of the mitral valve. Both coronary artery ostia were obstructed by Manuscript received May 7, 2008; accepted July 19, 2008. From the *Discipline of Pathology, The University of Adelaide; and †Forensic Science SA, Adelaide, South Australia, Australia. Reprints: Roger W. Byard, MBBS, MD, Discipline of Pathology, Level 3 Medical School North Building, The University of Adelaide, Frome Rd, Adelaide 5005, Australia. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0140 DOI: 10.1097/PAF.0b013e31821984fb

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vegetations. Histological examination of the lesion on the aortic valve revealed organizing thrombus with focal areas of acute inflammation and microabscess formation. Gram staining showed numerous colonies of gram-positive coccobacilli. Areas of chronic, organizing, and acute ischemic change were identified within the heart. Toxicological examination of blood revealed nontoxic levels of methamphetamine, diazepam, and tetrahydrocannabinol. Death was due to myocardial ischemia caused by coronary artery ostial occlusion complicating acute bacterial endocarditis.

Case 2 A 54-year-old man was found dead in bed at home. He had a medical history that included hypertension, type 2 diabetes mellitus, peripheral vascular disease, and chronic renal failure. At autopsy, hemorrhagic infarction of the left middle cerebral artery territory was found with cerebral edema, marked uncal notching, and midline shift. Histological examination of the brain showed focal cortical microabscesses with small vessels containing karyorrhectic debris with neutrophils and occasional gram-positive cocci. The heart was enlarged (527 g) with fibrinous vegetations that on microscopy were also found to contain gram-positive cocci. Death was due to a left middle cerebral artery territory cerebral infarct due to septic embolization from bacterial endocarditis involving the aortic valve.

Case 3 A 23-year-old schizophrenic man was found collapsed outside a house surrounded by a pool of blood. The case was treated as suspicious by attending police officers; however, external examination of the body did not reveal any significant injuries. At autopsy, there was blood within the upper aerodigestive tract with widespread hemoaspiration into both lungs, predominantly involving the right lower lobe. This was associated with a consolidated area around the right lower lobe bronchus and adjacent lower lobe branch of the right pulmonary artery with a 2- to 3-mm diameter fistula running between the artery and bronchus. There was also blood within the mouth and a large amount of blood within the stomach, duodenum, and small intestine. Histological examination of the fistula showed inflammatory granulation tissue, which was capped focally with fibrinous exudate containing an acute inflammatory infiltrate and occasional small colonies of gram-positive cocci between the lumina of the pulmonary artery and the bronchus. Laminated blood clot with a postmortem overgrowth of gram-positive cocci protruded into the lumen of the bronchus. Other findings at autopsy included a small patent septal defect in the lower anterior aspect of the interventricular septum with no evidence of active endocarditis. There were no valvular vegetations. There were no sources of hemorrhage within the mouth, pharynx, esophagus, stomach, or small intestine. There was no evidence of trauma, nor were there other underlying organic illnesses that could have caused or contributed to death. Death was attributed to exsanguination from an arteriobronchial fistula complicating a pulmonary abscess. Am J Forensic Med Pathol

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Subsequent review of the medical history revealed a 6-week admission to hospital 4 months before death with bacterial endocarditis due to Staphylococcus aureus complicating a congenital ventricular septal defect. Echocardiography had shown a large vegetation protruding into the right ventricle, which had shed emboli into both lungs causing septic infarcts with abscess formation. Antibiotic therapy had been successfully undertaken, although follow-up computed tomography scans and chest x-rays showed persistence of a soft-tissue opacity in the hilum of the right lung. A computed tomographyYguided biopsy of the mass was being planned. Anesthetic complications associated with attempted resuscitation in this case involving systemic air embolism through the patent ventricular septal defect have been previously reported.3

DISCUSSION Infective endocarditis may be subclassified into acute and subacute forms. Acute endocarditis is characterized by highgrade fever associated with rapid cardiac damage and metastatic infection of extracardiac sites via the circulatory system. Death occurs within weeks without treatment. Subacute endocarditis is more slowly progressive unless complications such as a mycotic aneurysm arise.1 One of the difficulties of treatment lies in completely eradicating septic loci, as responsible organisms may lie deep within vegetations and antibiotic resistance is increasing.4 The clinical characteristics of infective endocarditis have changed significantly since the description by Osler5 with an increase in the age at onset and some studies now reporting that the most common etiological agent is S. aureus,6,7 although others have found that viridans streptococci are still a major pathogen.4,8 The increasing numbers of patients seen with S. aureus endocarditis may be related to increasing use of intravascular lines/devices, recreational drugs, and prosthetic heart valves.1,7 Degenerative aortic and mitral valve disease now predominates over rheumatic heart disease as the underlying abnormality,9 and a study by Hoen et al7 reported that 47% of patients with infective endocarditis presented without knowledge of a preexisting cardiac disorder. Although it has been reported that the incidence of endocarditis has remained stable,7,8 others have asserted that the incidence is in fact increasing.4 The incidence does vary geographically among different patient cohorts because of associated risk factors, with, for example, intravenous drug users having an estimated 7-fold greater risk than patients with rheumatic heart disease or prosthetic valves.4 In the reported cases, endocarditis was associated with drug abuse, chronic renal failure, and a congenital cardiac defect. Organisms promote the formation of vegetations by inducing platelet aggregation and activating the clotting cascade resulting in layers of fibrin being deposited along with bacteria. Although organisms deep within vegetations may be metabolically inactive, organisms on the surface proliferate and are continuously shed into the circulation.1,4 Mortality rates vary depending on the type of organisms and the underlying pathology with lethal mechanisms involving both cardiac and extracardiac pathology. Cardiac complications include acute congestive cardiac failure from perforated native or bioprosthetic valve leaflets, rupture of infected chordae tendineae, valvular obstruction from bulky vegetations, or sudden intracardiac shunts from fistulous tracts or prosthetic dehiscence. Acute congestive cardiac failure occurs more commonly in native aortic valve endocarditis. Congestive cardiac failure resulting from deterioration of valvular and ventricular function is the most important predictor

Sudden Death and Bacterial Endocarditis

of adverse outcome requiring surgical therapy.10 Periannular infections are associated with increased mortality and cardiac failure, with a need for surgery, and are found in 10% to 40% of native valve and 45% to 100% of prosthetic valve infections. Common sequelae include perivalvular cavities and abscesses that can cause conduction disturbances especially heart block, which is frequently seen in native aortic valve infection.10 Rarely, abscesses can progress to form fistulous intracardiac tracts.11 As in cases of acute rheumatic fever, coronary artery embolization of fragments of vegetations may occur with resultant myocardial ischemia.12 In case 1, direct occlusion of coronary artery ostia had resulted in lethal ischemia. Extracardiac complications include systemic embolization in 22% to 50% of cases found primarily with aortic and mitral valve infections due to S. aureus, Candida, the HACEK group of gram-negative bacilli (Haemophilus, Actinobacillus, Cardiobacterium, Eikenella, and Kingella spp), and Abiotrophia organisms.10 Embolization most commonly occurs within the first 2 to 4 weeks of antibiotic treatment, with the rate of events during the first 2 weeks dropping from 13 to less than 1.2 embolic events per 1000 patient-days. However, embolic events may occur before diagnosis or even after completion of therapy. The central nervous system is the most common site for embolic complications, with more than 90% of emboli lodging in the middle cerebral artery distribution, as in case 2. After embolization, mycotic aneurysms may occur in 2% to 25% of patients with intracranial aneurysms having a high overall mortality rate of 60%, which increases to 80% with rupture.10 In case 3, pulmonary abscesses had most likely resulted from direct seeding by infected emboli. Bland emboli may result in aseptic infarction and are a well recognized complication in the spleen, with infarction occurring in 40% of left-sided cases of infective endocarditis. However, of those, only approximately 5% will develop splenic abscess.10 The presence of a ventricular septal defect in the reported case had resulted in formation of a fibrin-platelet vegetation on the right side of the defect with embolization via the pulmonary artery. Persistence of the infection despite apparently adequate antibiotic cover resulted in necrosis of the walls of a major airway and artery and intervening connective and pulmonary tissues. Fistula formation

TABLE 1. Causes of Unexpected Death in Cases of Infective Endocarditis Cardiac Acute congestive cardiac failure Heart block Fistulae, eg, aorta root to cardiac chamber Myocardial infarction Extracardiac Embolic events Organ infarction Mycotic aneurysm rupture Arteriobronchial fistula Neurological Aseptic or purulent meningitis Intracranial hemorrhage Embolic stroke Seizures Encephalopathy Sepsis

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had then resulted in massive hemorrhage into the airways with sudden collapse. Infective endocarditis is a complex clinical entity, and despite advances in diagnosis, prompt antibiotic therapy, and surgical intervention, the mortality has changed little over several decades.11 The reported cases are instructive in demonstrating rare and complex sequences of pathological changes that may lead to unexpected death in individuals with this condition involving vascular compromise. Valvular vegetations had caused direct obstruction of blood flow to the myocardium in 1 case, had compromised cerebral blood flow due to fragmentation and embolization in the second, and had caused ongoing pulmonary sepsis, with erosion of a major pulmonary vessel and airway, in the third. Bacterial endocarditis remains an uncommon condition that may still result in sudden death, the precise mechanisms of which may be understood only after careful delineation at autopsy. Causes of unexpected death in infective endocarditis are listed in Table 1. ACKNOWLEDGMENTS The authors thank the South Australian State Coroner, Mr M. Johns, for permission to publish selected details of these cases. REFERENCES 1. Karchmer AW. Infective endocarditis. Chapter 109. In: Harrison’s Principles of Internal Medicine. 16th ed. Kaspar D, Braunwald E, Hauser S, et al, eds. New York: McGraw-Hill; 2005:731Y740. 2. McCready RA, Bryant MA, Fehrenbacher JW, et al. Infected splenic artery aneurysm with associated splenic abscess formation secondary

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to bacterial endocarditis: case report and review of the literature. J Vasc Surg. 2007;45:1066Y1068. 3. Simes D, Gilbert J. Massive air embolism with pulmonary arterio-bronchial fistula and ventricular septal defect. Anaesth Intensive Care. 1997;25:420Y422. 4. Tak T, Reed KD, Haselby RC, et al. An update on the epidemiology, pathogenesis and management of infective endocarditis with emphasis on Staphylococcus aureus. WMJ. 2002;101:24Y33. 5. Osler W. The Principles and Practice of Medicine. London: Butterworth & Company; 1918:797Y804. 6. Fowler VG, Miro JM, Hoen B, et al. Staphylococcus aureus endocarditis: a consequence of medical progress. JAMA. 2005;293:3012Y3021. 7. Hoen B, Alla F, Selton-Suty C, et al. Changing profile of infective endocarditis: results of a 1-year survey in France. JAMA. 2002;288:75Y81. 8. Tleyjeh IM, Steckelberg JM, Murad HS, et al. Temporal trends in infective endocarditis: a population-based study in Olmsted County, Minnesota. JAMA. 2005;293:3022Y3028. 9. Beynon RP, Bahl VK, Prendergast BD. Infective endocarditis. Brit Med J. 2006;333:34Y39. 10. Bayer AS, Bolger AF, Taubert KA, et al. Diagnosis and management of infective endocarditis and its complications. Circulation. 1998;98:2936Y2948. 11. Paterick TE, Paterick TJ, Nishimura RA, et al. Complexity and subtlety of infective endocarditis. Mayo Clin Proc. 2007;82:615Y621. 12. Stahl J, Santos LD, Byard RW. Coronary artery thromboembolism and unexpected death in childhood and adolescence. J Forensic Sci. 1995;40:599Y601.

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ORIGINAL ARTICLE

Impact of Identity Theft on Methods of Identification Jerri McLemore, MD,* Walker Hodges, BA,Þ and Amy Wyman, F-ABMDIþ

Abstract: Responsibility for confirming a decedent’s identity commonly falls on the shoulders of the coroner or medical examiner. Misidentification of bodies results in emotional turmoil for the next-of-kin and can negatively impact the coroner’s or medical examiner’s career. To avoid such mishaps, the use of scientific methods to establish a positive identification is advocated. The use of scientific methods of identification may not be reliable in cases where the decedent had assumed the identity of another person. Case studies of erroneously identified bodies due to identity theft from the state medical examiner offices in Iowa and New Mexico are presented. This article discusses the scope and major concepts of identity theft and how identity theft prevents the guarantee of a positive identification. Key Words: scientific methods of identification, identity theft, fingerprints, postmortem radiology (Am J Forensic Med Pathol 2011;32: 143Y145)

ner’s office utilize visual identification by an immediate family member if conditions permitted or that scientific methods of identification such as fingerprint or dental x-ray comparison or DNA analysis be used to establish a decedent’s correct identity.4 The legislative action insisting on the use of scientific methods to establish identity to avoid misidentification assumes that these methods absolutely confirm the decedent’s true identity. This assumption becomes invalid if the decedent during his/ her lifetime had fraudulently obtained someone else’s identity. A review of records from the Office of the Medical Investigator in Albuquerque, New Mexico, between the years 1996 and 2007 and from the Iowa Office of the State Medical Examiner in Ankeny, Iowa, between the years 2000 and 2007 uncovered at least 5 known cases where a person’s acquisition of a false identity before death led to erroneous identification of the decedent even when scientific methods of identification were used.

CASE DETAILS ne of the many functions of most medical examiner or coroners’ offices is the appropriate identification of the deceased. In most cases, the decedent’s identification is based on visual confirmation with comparison of the decedent to a photograph on a driver’s license or by recognition by a family member or friend. When the decedent’s physical characteristics are obscured by postmortem changes or trauma, other methods of identification are utilized. Usually, these methods, also known as scientific methods of identification, include comparing unique characteristics of the decedent with known reference material obtained before death such as comparing antemortem and postmortem fingerprints, comparing antemortem and postmortem dental x-rays, and comparing medical and surgical records to correlate surgical and medical devices such as orthopedic hardware and pacemakers that may have unique serial numbers. X-ray comparisons are an established tool for identification of bodies, and the use of other unique markers other than dentition such as the frontal sinus has been utilized.1,2 Identity can also be confirmed by comparing the decedent’s DNA profile with known biological relatives. Misidentification of a person whose death falls under the jurisdiction of the medical examiner or coroner can have catastrophic repercussions for the next-of-kin and can jeopardize the credibility of the medical examiner or coroner. In 2006, misidentification of 2 young women involved in a motor vehicle crash made national headlines.3 In an effort to prevent such an error from ever occurring again, the state’s legislation passed a bill of which one component was a requirement that the coro-

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Manuscript received July 27, 2008; accepted January 4, 2009. From the *Department of Pathology-Autopsy Service, Wake Forest University School of Medicine, Winston-Salem, NC; †Iowa Office of the State Medical Examiner, Ankeny, IA; and ‡Central Office Investigators, Office of the Medical Investigator, Albuquerque, NM. Reprints: Jerri McLemore, MD, Department of Pathology-Autopsy Service, Wake Forest University School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0143 DOI: 10.1097/PAF.0b013e31820c29c3

Case 2

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A middle-aged man was found dead slumped over the steering wheel of his semitruck, which was parked at a truck stop. His commercial driver’s license, which indicated that he was from another state, was used to identify the decedent. Visual identification seemed straightforward because there was no trauma or postmortem changes obscuring the facial characteristics. The commercial driver’s license was sent back to the Department of Motor Vehicles in the originating state, which then listed Jonathan S. as deceased. A detective in that state, who was actively investigating a Jonathan S. for a string of robberies, noticed that Jonathan S. was listed as deceased. The detective knew that Jonathan S. was alive and well but incarcerated in a local prison. The incarcerated Jonathan S. had the same social security number and date of birth as the driver’s license found on the decedent. The widow of the decedent was located from the beneficiary information the trucking company kept on file. The widow, who had received and cashed benefit payments ascribed to Jonathan S., claimed that her husband, a Jonathan W., had been the trucker who had died at the truck stop. Further investigation revealed that Jonathan S. and Jonathan W. had both at one time been incarcerated in the same prison at the same time. Jonathan W. had been arrested multiple times for driving while intoxicated, making him ineligible to obtain a commercial driver’s license. Presumably, Jonathan W. had made arrangements to assume or simply steal Jonathan S.’s identity to obtain a commercial driver’s license.

The medical examiner’s office investigated the death of an inmate known as Phillip B., who had died in prison. When the family claimed the decedent’s body to take back to Mexico for burial, they informed the office that the decedent’s actual name was John B. and that Phillip B. was John’s brother. Because of the discrepancy in identification, fingerprints were obtained from the body and sent to the Federal Bureau of Investigation. Fingerprint comparison confirmed that the decedent’s name was Phillip B.

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The family continued to dispute the identification and provided a birth certificate for John B., claiming that it belonged to the decedent. To further complicate the situation, Phillip B. and John B. were only a few years apart in age and were similar in appearance, and both had been arrested and incarcerated multiple times in different states while using each other’s names. Both brothers had fingerprints in the legal system under each other’s names. Medical records and x-rays were then used in an attempt to resolve the identification dispute. Nearly all of the medical records from the prison and 2 different hospitals in the area were attributed to Phillip B.; however, a few documents in the medical records and several notes to the prison nurse requesting a dental appointment were signed with the name John B. Before his incarceration, the decedent had injured his hand, requiring surgery. Surgical staples were still in the hands. The family obtained the x-rays of the hand from the hospital in another state. Unfortunately, the decedent had used a different name altogether, Juan B., when he received his medical care. The decedent’s remains were released to the family under the name, Phillip B. Verification of the decedent’s true identity was complicated by a number of factors including illegal immigration status to the United States, the commission of crimes resulting in fingerprints while possibly under an assumed name, receiving medical care including x-rays while possibly under an assumed name, and the biological similarity of the decedent and the ‘‘victim,’’ which was his brother. Because of the limited manpower and resources and the complexity of the situation making an absolute positive identification difficult if not impossible, a decision was made to identify the decedent based on the preponderance of scientific evidence and the name officially recognized by the state upon his incarceration. The decedent’s remains were released to the family under the name, Phillip B.

Case 3 The medical examiner’s office investigated the death and conducted an autopsy on a middle-aged man, Ron C., who had died of an apparent self-inflicted shotgun wound of the head. The man had lived in his community for approximately 20 years before his death, and preliminary identification was established based on circumstantial evidence including the location of death within the decedent’s secured residence, the clothing the decedent was wearing, and the bodily characteristics of the decedent. The shotgun wound resulted in facial trauma that hindered visual identification of the decedent. To be thorough, the medical examiner decided to confirm the decedent’s identity using a scientific method. The decedent’s dental records and dental x-rays were retrieved from the local dentist’s office and matched with the postmortem dental x-rays providing a positive identification. Meanwhile, law enforcement officials were having difficulty locating a social security number for the decedent. While searching Ron C.’s residence, officers uncovered a separate room that had no access. After breaking through the drywall, the officers discovered a fullsized Jeep inside the room. The owner of the Jeep was eventually traced back to a man from another state, Richard J., who had reported the Jeep as stolen nearly 2 decades prior. Law enforcement officials in this other state were unable to locate Richard J.; however, they did locate his ex-wife and a sister who reported that Richard J. had swindled a business partner out of a substantial amount of money and had then fled the state around the same time that the Jeep had been reported as stolen. To resolve the confusion surrounding the decedent’s identification, a photograph of the decedent during his life was found

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in his residence. Although he was 20 years older, the ex-wife and the decedent’s sister were able to confirm his identity as Richard J. A sample of DNA was obtained from the decedent’s sister and compared with DNA from a blood sample taken from the decedent at autopsy confirming the visual identification.

Case 4 A middle-aged man was found in his residence with an apparent gunshot wound of the head. Because of the facial trauma and postmortem changes present, the decedent’s identification was confirmed as Steven G. by ante mortem and postmortem fingerprint comparison. A few months after finalization of the autopsy report, the decedent’s brother contacted the medical examiner’s office claiming that he was Steven G. and that the decedent had stolen his identity. During the time, he was impersonating Steven G. The decedent had been arrested and fingerprinted, thereby establishing a criminal record under his brother’s name.

Case 5 A Hispanic man died of a gunshot wound. His identification was confirmed by fingerprint comparison through the Federal Bureau of Investigations. His family in Mexico eventually heard of his death and notified officials of his real name. He had been arrested and fingerprinted while in the United States and had given his false name and identification to the arresting law enforcement officials.

DISCUSSION A person’s identity is based on a number of attributes, some of which are unique to the individual. These attributes can be divided into the following 3 classifications: biometric, biographical, and attributed.5 Biometric identity consists of those unique attributes often used to make a positive identification such as fingerprints, DNA, and even physical appearance. Attributed identity consists of those components of identification given at birth such as a person’s name, birthday, and social security number. Biographical identity consists of those components that are built up over a lifetime such as medical or surgical history, dental history, credit ratings, and employment and military history. Scientific methods of identification rely on both biometric and biographical identification attributes of an individual such as DNA, fingerprint comparison, dental records and x-ray comparison, and surgical and medical records comparison especially if orthopedic hardware tagged with a unique serial number is present. The inherent problem with confirming a decedent’s identity based on these various types of identification markers lies in the need to obtain reference material for comparison. Antemortem medical records, dental records, and fingerprints need to be available to compare with autopsy findings. Even the use of DNA requires that biological material obtained from the decedent before death or from the decedent’s biological relatives is available. Difficulties with identification arise when the decedent has assumed a false identity or stolen another person’s identity and accrued biographical and biometric attributes under the assumed name. According to the Federal Trade Commission, identity theft is one of the fastest-growing crimes in the United States, and approximately 9 million Americans have their identities stolen each year.6 It is also a significant worldwide problem. A number of factors have contributed to the identity theft explosion including the reliance on easy-to-obtain credit; the easy dissemination of personal identifiers such as social security numbers, credit card information, and other personal information; and the popularity of transactions using Internet-based companies, credit cards, and debit cards. Illegal immigration has also contributed to this * 2011 Lippincott Williams & Wilkins

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explosion by creating an environment encouraging acquisition of stolen social security numbers and false documents used to establish identity. Unfortunately, identities can be stolen easily. Just a few ways that identities can be stolen are by dumpster diving, skimming, phishing, the change-of-address ploy, stealing wallets and purses for the personal information that they contain, and pretexting.7 Dumpster diving entails going through an identity theft victim’s trash looking for unshredded personal information such as the victim’s name, address, and credit card or bank statements. Skimming refers to the use of a small electronic device that can read the magnetic strips on credit or debit cards, downloading and storing the personal information on the card. Someone placing a change-of-address request at a local post office can divert mail from the rightful owner’s residence to the perpetrator’s address, thereby obtaining personal information. Pretexting involves the perpetrator calling organizations such as credit card companies or banks and, with limited information such as the victim’s name or address, extracting additional personal information needed to open a line of credit or divert money from the victim’s bank account. Phishing and a related term, pharming, are similar tactics in that each method impersonates a legitimate Web site to trick a user of that site to disclose personal information, which is then used to steal a person’s identity.8 When a coroner or medical examiner is charged with identifying a decedent, assurances of positive identification break down when the decedent was living under an assumed name. Unfortunately, these erroneous identifications will usually become recognized only after the autopsy and usually after a significant amount of time has passed. Efforts to rectify the misidentification depend on use of photographs of the decedent, his/her fingerprints or x-rays, or DNA analysis. Depending on the circumstances of the death and the resources of the office investigating the death, material such as DNA, fingerprints, dental charting, x-rays, and photography of the decedent may not have been collected. Collection of this material is even less likely to be performed if the body had undergone an external examination at the place of death or at a local funeral home in lieu of a full autopsy. Although common forensic autopsy practice recommends obtaining an identification photograph of the decedent, a blood sample if available for possible DNA analysis and at least a thumbprint if possible for every body that undergoes a complete autopsy, full body x-rays, dental x-rays or dental charting, and examination of orthopedic hardware for serial numbers are rarely performed in cases where identification is not an apparent issue. Even when x-rays, medical records, DNA samples, fingerprints, and photographs of a decedent are available, establishing a true identity may be problematic for a variety of reasons. Identity theft between biologically related family members will complicate the use of DNA analysis. Acquisition of biographical data such as medical records and dental x-rays while under an assumed identity will complicate antemortem and postmortem comparisons of these materials. Investigation to resolve discrepancies in identification will often cross jurisdictional borders, both nationally and internationally, creating difficulties in tracking down vital documents and acquaintances to corroborate the identity. Investigations to confirm a decedent’s identity in these cases are time-consuming and overburden agencies with limited manpower and resources. Subsequently, areas that have higher numbers of deaths requiring investigation by the coroner’s or medical examiner’s office, areas that have a relatively larger population of illegal immigrants, and areas that have a rela-

Identity Theft on Methods of Identification

tively high crime rate overall add to the difficulties faced by law enforcement agencies and medicolegal death investigators in establishing a true identity. Misidentification of a decedent in these jurisdictions will more likely be discovered by the decedent’s family or acquaintances. Because identity theft and assumptions of false identities have exposed a weakness in reliance on scientific methods of identification, the coroner’s or medical examiner’s office may need to temper its guarantee of establishing a decedent’s correct identification by recognizing that misidentifications will probably occur in these situations. Consideration should be given to collecting an identification photograph, fingerprints, and a DNA sample on all bodies investigated by a coroner’s or medical examiner’s office including bodies viewed for cremation permits and where bodies are externally examined ‘‘out in the field’’ instead of being transported to the morgue for full autopsy. In cases of homicide, confirmation of the decedent’s stated identity needs to be established as much as possible using scientific methods. Also, additional specimens such as dental and skeletal x-rays, documentation of serial numbers of any medical or orthopedic devices, retrieval of biographical data such as medical records, and cross-checking with various attributed data such as the social security number and birth certificate may become necessary in case discrepancies in identity surface at a later date. In the past few years, there has been a push on the national level for an electronic death registration system and intelligence reform that would enable authentication of vital events such as allowing a decedent’s birth and death records to be cross-matched in real time across state borders.9 Once this system is implemented, the number of misidentifications of decedents recognized at the time of the death investigation will probably increase.

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REFERENCES 1. Angyal M, Derczy K. Personal identification on the basis of antemortem and postmortem radiographs. J Forensic Sci. 1998;43(5):1089Y1093. 2. Kirk NJ, Wood RE, Goldstein M. Skeletal identification using the frontal sinus region: a retrospective study of 39 cases. J Forensic Sci. 2002;47(2):318Y323. 3. CBS Broadcasting Inc./Associated Press. Fallout from tragic hospital mix-up: misidentification of two young women puts coroners in spotlight. Indianapolis, June 2, 2006. Available at: http:// www.cbsnews.com/stories/2006/05/31/national/main1673090.shtml. Accessed June 13, 2008. 4. Gard B. News release [state Sen Beverly Gard Web site]. February 22, 2007. Available at: http://www.in.gov/S28/Insight/2-22-07.htm. Accessed June 13, 2008. 5. Hamadi R. Identity Theft: What It Is, How to Prevent it, and What If It Happens to You. London, Great Britain: Vision Paperbacks; 2004. 6. Identity theft. Federal Trade Commission Web site. Available at: http://www.ftc.gov/bcp/edu/microsites/idtheft/consumers/ about-identity-theft.html. Accessed February 20, 2007. 7. Hammond R. Identity Theft: How to Protect Your Most Valuable Asset. Franklin Lakes, NJ: Career Press; 2003. 8. Schmidt S, McCoy M. Who Is You?: The Coming Epidemic of Identity Theft. Urbandale, IA: The Consortium, LLC; 2005. 9. NAPHSIS Web site. Available at: http://www.naphsis.org/ index.asp?bid-1019. Accessed October 8, 2008.

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ORIGINAL ARTICLE

Errors on Death Certificates Requiring Amendments The Broward County Experience Danit Fischtein, MD, BScN, RN, NE* and Stephen J. Cina, MDÞ

Abstract: The medical examiner’s office in Broward County is responsible for determining the cause and manner of death in cases falling under its jurisdiction and issuing death certificates on these decedents. Amendments are occasionally required to correct misinformation on death certificates or within the autopsy reports. The purpose of this study was to investigate the major causes for the amendments and to develop strategies to avoid future errors. We found 128 cases from 2006 to 2007 that required amendments; 103 contained sufficient data in the file for further analysis. Over this time period, 3790 death certificates were issued over that same period, resulting in a 3.37% amendment rate. In this study, the cohort included both males and females with a ratio of 2:1. Their ages ranged from newborn to 103 years, with a mean age of 49 years. Of the 103 amended cases, amendments were made to the cause (n = 30) and often the manner (n = 21) of death listed on the death certificate; the remaining changes were limited to the autopsy report. The most common reasons for amendments included reception of delayed laboratory findings (35%), acquisition of additional medical history (22.5%), and typographic errors (15.5%). Typographic errors mainly occurred because of inaccuracies in the names originally provided to our office, the use of aliases by decedents, incorrect personal/demographic history, or various misspellings by funeral homes or medical examiner staff. The most significant reclassifications involved changing certified natural deaths to accidental overdoses and vice versa, based on toxicological analysis. Because of delays in specimen turnaround, these amendments often were made months after the original death certificate was issued. STAT urine drug screening has been helpful in reducing the number of amendments made, but certain drugs of significance are missed by rapid screens. Given that our office performed complete toxicological analysis on all cases over this period, it seems likely that we detected several overdoses that would have been missed if natural deaths were not routinely screened for potential toxins. Key Words: amendment, forensic, death certificate, medical examiner, autopsy, Broward County (Am J Forensic Med Pathol 2011;32: 146Y148)

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he Broward Medical Examiner’s Office (MEO) performs between 1500 and 1800 autopsies per year on cases falling under our jurisdiction according to Florida law. To remain compliant with state practice guidelines and standards promulgated by the National Association of Medical Examiners, a finalized autopsy report is generated within several days to a few weeks after completion of the gross autopsy in the majority of Manuscript received August 10, 2008; accepted May 27, 2009. From the *Division of Emergency Medicine, University of Toronto; and Ryerson University, Toronto, Canada; and †Department of Pathology, Nova Southeastern University College of Osteopathic Medicine, Broward County, FL. Dr Cina is deputy chief medical examiner, Broward County, Florida. Reprints: Danit Fischtein, MD, Medical Examiners Office, 5301 Southwest 31st Avenue, Fort Lauderdale, FL 33312. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0146 DOI: 10.1097/PAF.0b013e31820c2ee6

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cases. In most cases, the cause and manner of death determination remain unchanged after receipt of adjunctive studies. In a few cases, however, further investigation and/or the results of toxicological analysis necessitate amendments to the death certificate and/or autopsy report. This may entail significant implications for both the family and other parties. Our literature review showed that few studies have been conducted to explore the reasons for amendments. This retrospective study examined reasons, methods, and frequency of amendments made by the MEO over the past 2 years. By analyzing these amendments, trends were noted, and methods for improvement have been implemented.

MATERIALS AND METHODS A total of 3790 autopsies were performed at the MEO in 2006 and 2007. Among those, 128 amended cases were found. Twenty-one of these could not be analyzed in detail in this study because of lack of information related to the initial cause and manner of death determination. Four additional cases were omitted because the autopsy was completed in 2005, although amendments were made in 2006. The case files including autopsy reports, summaries, cause and manner of death, and toxicology results (initial and final) for the remaining 103 amended cases were reviewed in detail. Information gathered included the date of autopsy, initial cause of death, contributory conditions, initial manner of death, date of amendment, final cause of death, final contributory conditions, final manner of death, reason for amendment, toxicology results, and general demographics of the decedent.

RESULTS Three thousand seven hundred ninety death certificates were issued on autopsies completed in 2006 and 2007, and 128 amendments were issued, resulting in a 3.37% total (death certificates and/or autopsy reports, predominantly the latter) amendment rate (Fig. 1). As noted above, only 103 were eligible for complete data analysis. Twenty-one amendments were made to the initial manner of death and 30 to the initial cause of death, listed on the death certificate. Reasons for amendments to the autopsy reports and, in some cases, the death certificate included additional laboratory findings (35%); added medical history or investigatory findings (22.5%); typographic changes (15.5%); inadvertent omissions of findings such as scars, nonlethal arteriosclerosis, abrasions, and so on (12%); additional minor injuries (4%); additional final diagnoses (3.5%); added contributory findings (2.1%); histological findings (2.1%); photography review (0.7%); fingerprint analysis (0.7%); and discrepancies detected on internal quality assurance/quality control (0.7%) (Fig. 2). Of the 35% of amendments related to additional toxicology findings, 30 cases involved a change in the cause of death, with 21 requiring concurrent amendment of the manner of death. In the remaining 65%, drugs were detected by toxicological analysis, and their concentrations were subsequently incorporated Am J Forensic Med Pathol

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FIGURE 1. The amendment rate for death certificates generated from all autopsies performed in 2006 and 2007 was 3.37%.

into an amended autopsy report, but editing the death certificate was not required. In the cases where the cause of death was amended, toxicology results showed that either (1) drug use resulted in death, (2) drug use contributed to death, or (3) nonlethal drug concentrations were detected in cases initially determined to be a drug-related death based on the scene and circumstances. The initial cause of death of 14 cases were attributed to a natural disease process; however, toxicology showed lethal levels of drugs and/or ethanol. Two cases showed that drugs and/or alcohol were detected by a STAT manual toxicology screen, and thus, the cause of death was attributed to drugs or alcohol. In addition, in 6 cases that were not initially screened for drugs, the circumstances supported an accidental overdose, but ‘‘negative’’ toxicology resulted in amending the manner of death to natural. In 1 case deemed to be an overdose, microscopy/histology detected a natural cause of death, and drug use was relegated to a contributory factor. Three cases initially thought to be natural deaths caused by illness or disease had to be amended when toxicology results detected substances that contributed to death and thus changed the manner of death to accident from natural. The results of toxicological analysis often changed the manner of death as well as the cause of death. In 14 instances, the initial manner of death was changed from natural to accident when initially undetected drugs were determined to be the cause

FIGURE 2. Delayed toxicological results and additional history/investigation initiated 35% and 23% of the amendments, respectively.

Errors on Death Certificates

FIGURE 3. In 86% of amended cases where the manner of death changed, the proximate cause of death also changed. In the remainder, changes to part II of the death certificate were required.

of death rather than a disease process detected at the time of autopsy. Two additional cases were amended from natural to undetermined after laboratory results were received, and 2 changed from suicide to undetermined. The manner of death in 2 cases was altered from accident to natural where further tests determined that the high level of drugs was not the cause of death and was changed from natural to suicide. No amendments involved homicides. Additional medical records and investigation changed the cause of death in several cases but did not alter the manner of death. In 85% of cases where the manner of death was amended, the proximate cause of death (part I on the death certificate) was also changed. In 15% of cases, drug use was deemed to be a contributory factor to death rather than the proximate cause of death (Fig. 3).

DISCUSSION The death certificate is an important legal document that has many implications for various parties. It provides valuable information related to end-of-life legal matters, such as life insurance and inheritance. Family members also use the information related to the death for closure and comfort as well as identification of familial risk factors for certain diseases. It is also used for data collection and epidemiological purposes by local, state, and federal agencies.1 The MEO has been keeping close records over the past few years relating to trends in amendments to autopsy reports and death certificates and identifying means of limiting their necessity. Primary goals of the autopsy include determination of the cause and manner of death and identification of contributory factors. In many cases, this can be determined via gross examination; in others, adjunctive studies such as histology and toxicology are required. If the cause of death is not readily apparent at the time of autopsy, these cases are commonly issued a

FIGURE 4. Almost half of the amendments resulted in a change to the cause and/or manner of death.

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FIGURE 5. Inaccuracies in the decedent’s name (38%) and autopsy typographical errors (20%) accounted for most amendments of a clerical nature.

‘‘pending’’ death certificate. If drugs are not suspected in a case involving a person with significant natural disease processes or drug overdose is indicated by the clinical history and/or manual urine drug screen results, ‘‘final’’ death certificates are usually issued on the day of the autopsy. As this study shows, in a small fraction of cases, this may result in amendments months later. Of our 103 cases, the cause of death was amended in 29% of cases primarily related to additional laboratory findings, particularly toxicology reports. Laboratory findings also changed the manner of death in 20% of our amended cases (Fig. 4). A study conducted in New Mexico showed that 1% of death certificates had either cause or manner of death amendments. This figure is similar to our experience (0.79% change to cause of death, 0.55% to manner of death). The most common amendments in the New Mexico study involved the interaction of arteriosclerotic cardiovascular disease and intoxicants.2 This is similar to our experience in that 0.95% of all of our cases from 2006 to 2007 were amended to some degree (either autopsy report or death certificate) because of delayed toxicological results. As in New Mexico, many of our cases displayed significant cardiovascular disease at autopsy, leading to an erroneous determination of a natural death. Efforts have been made to ameliorate the possibility of finding significant toxicological results long after the case has been signed out. This has been addressed in large part by switching from urine ‘‘dipsticks’’ to more comprehensive STAT urine analysis using a Cloned Enzyme Donor ImmunoAssay (CEDIA) run on the Abbott Aeroset Chemistry Analyzer (Abbott Aeroset, Abbott Park, Ill). This drug screen is now available while the autopsy is in progress, and it can be performed even if less than 1 mL of urine is obtained. Furthermore, open communication between the toxicology staff and the pathologists has been strongly encouraged. This dialogue facilitates rapid review of blood enzyme-linked immunosorbent assay results by the medical examiner as it becomes available rather than after confirmatory testing by gas chromatography/mass spectrometry. This allows the pathologist to detect ‘‘surprise results’’ early and appropriately triage cases for quantification. Enzyme-linked immunosorbent assay blood screening can be rushed, and the results called in to the pathologist within days of the autopsy in the event that urine cannot be obtained for CEDIA. The second most common reason for amendments with death certificates was a lack of medical history. One study by Pritt et al1 showed that frequent causes of errors in death certification related to unfamiliarity with the medical history of the deceased. Often when the deceased is found, adequate medical history is not available. In our county, initial information is often obtained by a removal service working in conjunction with police officers on the scene except in homicides, child fatalities, and other complex cases. Although it would be optimal to have investigators in the field, budgetary constraints have made this difficult. Newton et al3 claimed that, ‘‘additional deterrents to

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autopsy in today’s competitive health care marketplace may include funding.’’ Even in an ideal system, however, it is often difficult to obtain adequate and complete medical information before commencing the autopsy. In our population, often the deceased is from out of town or does not have a regular family doctor. In other instances, it may be difficult to interview family members or obtain medical records in a timely manner. We have therefore focused our efforts on educating removal service personnel and primary responders from other agencies in hopes that they can obtain useful, preliminary medical information. The third most common cause of amendments involved typographic changes. This was most commonly due to lack of accurate demographic or personal information. In many of these cases, the body was discovered with no identification, or tentative identification was proved inaccurate. Resultantly, 37.5% of typographical errors were due to name changes and/or spelling errors of names. Inaccurate transcription, dictation, or proofreading of autopsy reports led to 18.8% of amendments to reports (eg, using ‘‘right’’ instead of ‘‘left’’); 12.5% involved spelling errors in medical terminology; 12.5% were due to errors of dates; 6.3% were related to race; 6.3% involved a change in birth date and/or age; and 6.3% were simple typographic errors involving grammar or spelling (Fig. 5). These errors have been discussed with the staff, and more attention has been given to typography during all stages of report generation and case finalization. In addition, 15% to 20% of all reports are peerreviewed as part of the office’s QA/QC program, resulting in increased factual accuracy and diminished clerical errors. To minimize distress to families and to not impede on police investigations, autopsies must often be performed before the receipt of all available information potentially relevant to the case. It is often not practical to wait until all medical history and personal information have been gathered. In most cases, the cause and manner of death can be determined at autopsy without a great deal of supporting material. Nonetheless, amendments may be required in some cases when more information becomes available.

CONCLUSIONS The most common cause of amendments to death certificates in Broward County have been related to delays in receiving toxicological information. Although no amendments in our study involved homicide cases, reclassifications of natural, accident, and suicide manners of death have occurred, resulting in significant legal and personal implications for family members and other interested parties. Introduction of CEDIA urine screening during the autopsy should reduce the major cause for amendments. Increases in staffing, both in investigations and toxicology, and acquisition of additional toxicology equipment would likely further reduce our amendment rates. Future studies in this area are needed to quantify the efficacy of our measures designed to reduce the number of amendments in Broward County. REFERENCES 1. Pritt BS, Hardin NJ, Richmond JA, et al. Death certification errors at an academic institution. Arch Pathol Lab Med. 2005;129(11): 1476Y1479. 2. Croft PR, Lathrop SL, Zumwalt RE. Amended cause and manner of death certification: a six-year review of the New Mexico experience. J Forensic Sci. 2006;51(3):651Y656. 3. Newton D, Coffin CM, Clark EB, et al. How the pediatric autopsy yields valuable information in a vertically integrated health care system. Arch Pathol Lab Med. 2004;128(11):1239Y1246.

* 2011 Lippincott Williams & Wilkins

ORIGINAL ARTICLE

The Flap by Flap Dissection in Terminal Ballistic Applied to Less Lethal Weapons Humbert de Freminville, MD, MSc, Fre´deric Rongieras, MD, MSc, Nicolas Prat, MD, MSc, and Eric J. Voiglio, MD, PhD, FACS, FRCS

Abstract: Medical examiners often have to solve questions such as firing distance and bullet trajectory for lethal weapons. Knowledge in the field of terminal ballistics has increased during the last 30 years and layer by layer dissection reveals superficial wounds that can be linked with the permanent cavity. At the end of the 1990s, terminal ballistics also focused on less lethal weapons and their wounds. Here, 2 different less lethal weapons with single bullets were tested on nonembalmed and undressed cadavers (N = 26) at different ranges and speeds. We have developed a technique for dissection which we call flap by flap dissection that reveals the advantage of the bullet-skin-bone entity, the absence of wounds linking its components and range of less lethal weapons. Key Words: flap by flap dissection, terminal ballistic, bullet-skin-bone entity, less lethal weapons (Am J Forensic Med Pathol 2011;32: 149Y152)

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he field of terminal ballistics has evolved over the last 30 years with the works of M. Fackler, MD (USA) and General J. Breteau VMD (FRANCE) who demonstrated the evidence of permanent cavity (crushing), and temporary cavity (stretching) (Fig. 1). Fackler1 worked on lethal weapons and developed the concept of wound profile while J. Breteau2 worked on bio instrumented pig tissue and perfect layer dissection techniques studying a large variety of wounds. The first teaching program related to wound ballistics began in Marseille (south of France) at the beginning of the 1990s and lasted for 4 years. It started again in Lyon (France) in September 2000 and now includes fundamental knowledge such as dissection. Studies of wounded tissues in lethal gunshot cases are usually performed by coroners who describe the entrance wound, try to identify bullet trajectory by probes, and describe the exit wound.3,4 The biomedical engineering approach to blunt ballistic traumas in less lethal weapons (LLW) is described by simulation or by dissecting post mortem human subjects (PMHS), on the basis of a large number of injury criteria such as the blunt criterion, the viscous criterion,5 and energy density required for penetration.6 Contrary to blunt lethal weapons, the literature does not appear to deal with approaches to dissection by pathologists. Manuscript received April 21, 2009; accepted September 18, 2009. From the UMRESTTE UMR T 9405, Universite´ de Lyon, Universite´ Claude Bernard Lyon 1, F-69373 Lyon Cedex, France. Reprints: Humbert de Freminville, MD, MSc, UMRESTTE UMR T 9405, Universite´ de Lyon, Universite´ Claude Bernard Lyon 1, Faculte´ de Me´decine Lyon-Est Claude Bernard, 8, Rockefeller Ave, F-69373 LYON Cedex 08, France. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0149 DOI: 10.1097/PAF.0b013e3181d03eba

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Therefore, we propose a specific method called flap by flap dissection, which can be easily applied during research and autopsies to obtain representative data. Furthermore, we could hope this will allow teams to compare their results and link research and forensic knowledge. This work describes the step-by-step approach taken by the coroner who analyses the different layers of tissue, from superficial to deeper layers of wounded tissues LLW cases with 2 different types of ammunition: a homogeneous rubber bullet, and a hybrid projectile.

MATERIALS AND METHODS Post Mortem Human Subject Twenty-six cadavers nonembalmed were obtained from an anatomic donation program in Lyon (France). All the experiments were conducted at the Anatomy Laboratory of the Faculty of Medicine of Lyon (France) in strict accordance with the French laws and regulations. The cadavers came from donors who had willingly donated them to science in their wills during their lifetime for teaching and research purposes. Ethical practices were adhered to throughout the testing, with all specimens being treated with respect.7 Twelve males and 15 females, aged from 74 to 97 years were placed on a specially designed seat and shot once in the frontal, temporal, sternal, and the tibial areas and a total of 104 injuries were produced. Different firing ranges were simulated and Table 1 gives the different velocities. The PMHS were not clothed to ensure direct contact between the ammunition and the anatomic target.

Gun and Ammunition A H&K 69 rifle-bore Handgun Launcher (Heckler & Koch, Oberndorf, Germany) was used on 23 PMHS with experimental less lethal hybrid ammunition and a flash ball.

FIGURE 1. Wound profile of lethal weapon (1) permanente cavity (2) temporary cavity.

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TABLE 1. Post Mortem Human Subject Data and Target Area Impact Velocity (m/s) PMHS

Hybrid ammunition

Homogeneous Ammunition

MB1 MB2 MB3 MB4 MB5 MB6 MB7 MB8 MB9 MB10 MB11 MB12 MB13 MB14 MB15 MB16 MB17 MB18 MB19 MB20 MB21 MB22 MB23 MB24 MB25 MB26 MB27

Gender Age

M F F M M M F M M M F F M M F F F F F F F M M F M F F

82 95 96 63 85 84 74 77 83 87 89 82 76 93 93 96 79 89 97 94 81 81 90 87 93 87

Forehead

64.0 64.5 64.4 55.5 62.7 56.4 49.3 43.1 53.2 50.8 Canceled 66.2 80.9 75.1 62.6 60.1 61.8 69.0 37.9 74.4 73.9 83.1 82.2 77.4 75.6 133.7 93.2

Temporal Sternal

67.4 60.6 71.2 51.9 61.9 58.8 55.3 53.1 57.7 53.7 77.3 78.6 80.6 68.1 55.9 53.4 76.2 50.0 75.4 76.1 82.4 87.5 77.0 73.3 121.2 91.1

64.3 65.0 65.2 60.0 55.7 56.2 47.9 48.0 49.2 92.2

Tibial

64.1 72.5 64.6 54.2 57.3 50.8 53.0 48.2 52.0 53.5

81.0 73.1 80.6 74.6 75.7 75.5 61.7 78.8 52.7 59.0 58.4 58.1 71.6 76.9 47.3 41.5 75.1 79,2 69.9 83.9 80.7 79,4 82.8 91,4 80.2 77.3 60.7 59.4 70.5 64.7 86.4 101.0

Velocity of hybrid and homogeneous ammunitions and situation of the lesions produced (underlined when fracture occurred).

Super Pro handgun launcher (Verney-Carron, Saint Etienne, France) was used on 3 PMHS. Both guns were placed 3 m away from the PMHS, and the firing range was simulated, from 4 to 50 m, by different cartridge loadings. The cadaver was fastened to a specially designed seat. The experimental less lethal hybrid ammunition (classified) (Fig. 2) was a 40 mm cartridge loaded with black powder. The projectile (weight 33 g, length 65 mm) was composed of a foam front part (weight 3 g, length 3.7 mm) and a plastic rear part (weight 30 g, length 28 mm). The homogeneous ammunition (Fig. 3) was a soft rubber ball (weight = 28 g cal 44/83) independent of the attached plastic rear part.

FIGURE 2. Hybrid ammunition 40  46 mm 33 g single bullet.

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FIGURE 3. Homogeneous ammunition (rubber bullet flash ball pro).

Terminal Ballistic and Flap by Flap Basis The purpose of the study was to describe skin and bone wounds in the case of LLW and whether links existed between both injuries. Flap by flap dissection consisted in analyzing different layers and manipulating them like the pages of a book to analyze wounds having the same orientation. We formulated the hypothesis that LLW wounds do not lead to very deep injuries during our preliminary tests, so the flap by flap process mainly included 2 flaps. Flap 1 was usually the first place of bullet contact with the specimen and included cutaneous and sub cutaneous tissues. Flap 2 involved aponevrotic tissue, muscle and bone. The conventional orientation8 described a frontal view, from head 0- to feet 180- (from right j90 to left +90-), and a sagital view (from front +90- to back j90-) (Fig. 4). During preliminary testing, it appeared that computerized tomography

FIGURE 4. Anatomic ‘‘Flap by Flap’’ orientation. * 2011 Lippincott Williams & Wilkins

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Flap by Flap Dissection in Terminal Ballistic

TABLE 3. Bruising and Fracture With Homogeneous Ammunition

Frontal Temporal Sternal Tibial (right)

Woundless

Abr

Lin

Arc

Str

0/3 1/0 0/3 1/3

1/0 1/0 3/0 1/0

0/0 0/0 0/0 0/0

0/0 0/3 0/0 0/0

2/0 1/0 0/0 1/0

Flap 1/flap 2 wounds: Abr Lin, Arc, Str. Abr indicates abrasion; Lin, linear; Arc, Arc-like; Str, star-like.

FIGURE 5. Flap by flap dissection on forehead area.

(or magnetic resonance imaging) scanning could be an additional method for describing bruising, but this was not the main purpose of this study. Neither polar nor trigonometric coordinates were used as they are unfamiliar to most practitioners. Images were taken of all the flap using conventional 2 D measurement (Fig. 5) to describe macroscopic bruising on flap 1 and sometimes fractures on flap 2.

Bullet-Skin-Bone Entity (BSB) Considering that both types of ammunition (hybrid and homogeneous) assumed to be used at the legal range (currently 10 m and more, but not less), the bullet-skin-bone (BSB) entity allowed us to identify whether or not links existed between injury severities and firing ranges.

RESULTS Different injury characteristics appeared during FbF dissection. The frequency and type of wounds depended on the body areas. Experimental hybrid ammunition (Table 2) caused abrasion injuries in more than 50% of cases with flat thin bone, with arclike bruising predominating on the frontal bone (which is spherical). There was no link between the 2 flaps in the presence of a wound if any. However, when abrasion occurred on skin only, no fracture was found below it. Rubber flash ball bullets (Table 3) did not cause fractures except to the thin temporal bone and there was no specific related skin wound in this particular case. All other skin injuries could be accompanied by bone fractures. This 2-step dissection procedure is significant. Wound occurrence depended on the interaction in the BSB entity.

The wound in flaps 1 and 2, were not linked to a specific velocity, and in 2 cases, fracture occurred at very low velocity (hybrid ammunition versus MB 7 and MB 19). Homogeneous ammunition was often harmful in flap 1, but may cause fractures in 33% of temporal bones without any associated skin injury. Figures 6 and 7 show examples of soft tissue injury produced by each type of ammunition.

DISCUSSION We tested a H&K 69 rifle-bore handgun launcher and Flash Ball Super Pro handgun with a single bullet commonly used in France, which is different from the United States where beanbag projectiles are also used.9 Since the beginning of the 1970s different types of less lethal ammunition have been used such as rubber bullets for riot control in Northern Ireland10 followed by the use of plastic bullet in 1973 in the same place and in the Israeli-Arab conflict in 2002. Several studies have pointed out the risk of severe injuries to the abdomen and thorax.11 It was noted, for example, that rubber bullets are unstable in the air explaining different and unexpected forms of blunting. Our review of the literature did not identify any study of the effects of hybrid and homogeneous bullet in view to determining the responsibility of the user relating to firing range. We wondered whether anatomic standards exist that are capable of linking a specific LLW wound to current use for example a policeman confronted by a mugger.

TABLE 2. Bruising and Fracture With Hybrid Ammunition

Frontal Temporal Sternal Tibial (right)

Woundless

Abr

Lin

Arc

Str

0/17 0/15 4/13 0/17

1/0 10/0 19/0 0/0

4/0 2/0 0/9 19/2

15/6 7/8 0/1 0/0

3/0 4/0 0/0 4/4

Flap 1/flap 2 wound: Abr Lin, Arc, Str. Abr indicates abrasion; Lin, linear; Arc, Arc-like; Str, star-like.

FIGURE 6. Linear bruising produced by hybrid ammunition on forehead area (MB 20, V = 74.4 m/s).

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In the case of LLW, it is not possible to ascertain the kind of fracture caused until studying flap 2, even when a skin wound has been clearly identified. Considering that both types of ammunitions are supposed to be used at a legal firing range (10 m and more, but not less), our description of the BSB entity allows coroners to find a link, if any, between wound severity and firing range. We recommended taking a flap larger than the visible wound or hole (quadrilateral and 15 cm from the middle was enough). The trajectory of each flap was from the left, so that we could analyze every flap from a similar position. As noted above, the PMHS were undressed, so it can be assumed that both sternal and tibial wounds would be different with clothed PMHS, which would have been shielded in this case. The main purpose of using unclothed PMHS was to analyze skin and bone wounds. The existence of deep injuries was not followed by a complete autopsy which is unusual during a complete forensic report. REFERENCES 1. Fackler ML. What_s Wrong With the Wound Ballistics Literature and Why. San Francisco, CA: Letterman Army Institute of research, Presidio of San Francisco CA 94129; 1987:27. Institute Report No. 239.

FIGURE 7. Abrasion produced by homogeneous ammunition on temporal area (MB 27, V = 91,1 m/s).

It is necessary to take into account different parameters that can significantly influence the results. The average age was 80.66 for the male, and 90.35 for the female. Also, skin texture and bone structure depended on both parameters. The cadavers were undressed during the test which may explain some skin lesions. Body wall temperature was around 4-C from the beginning and rose to 15-C to 17-C during dissection, still well below that of a living human being. Flap by flap dissection is a practical macroscopic practical method which only analyses permanent wounds, so there was no evaluation of associated temporary wounds (the Bstretch[ cavity described with lethal weapons). Usually 2 flaps were intended in the case of LLW similar to the procedure used for LW for which the concept of interaction between propellant and living tissues developed during the 1980s is accepted. We used the concept of interaction between bullet and living anatomic tissue developed by BRETEAU in 1984, for lethal weapons, which uses the term BSB in the case of LLW. During our dissection, this entity revealed that there were no links between wounds and firing distances. Consequently, coroner cannot answer the question of range of firing, contrary to the case of LW.12

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2. Breteau J. Centre de Recherche et d_Etude de la Logistique de la Police, Ministe`re de l_Inte´rieur, 168 Rue de Versaille, F78150 Le Chesnay, France. 3. Durigon M. Pratique Me´dico-Le´gale. Verneuil l’Etang, France: Elsevier Masson; 2007:83. 4. Dodd MJ. Terminal BallisticsVA Text and Atlas of Gunshot Wounds. Boca Raton, FL: CRC Press, Taylor and Francis; 2006:76. 5. Bronzino JD. The Biomedical Engineering HandbookVBiomedical Engineering Fundamentals. 3rd ed. Boca Raton, FL: CRC Press, Taylor and Francis; 2006:52.1Y53.1. 6. Bir CA, Stewart SJ, Wilhelm M. Skin penetration assessment of less lethal kinetic energy munitions. J Forensic Sci. 2005;50: 1426Y1429. 7. King AI, Viano DC, Mizeres N, et al. Humanitarian benefits of cadaver research on injury prevention. J Trauma. 1995;38:564Y569. 8. Kamina P. Pre´cis D_Anatomie Clinique: Anatomie Ge´ne´rale. Tome 1. Paris, France: Maloine; 2005:11. 9. Suyama J, Panagos PD, Sztajnkrycer MD, et al. Injury patterns related to use of less-lethal weapons during a period of civil unrest. J Emerg Med. 2003;25:219Y227. 10. Steele JA, McBride SJ, Kelly J, et al. Plastic bullet injuries in Northern Ireland: experiences during a week of civil disturbance. J Trauma. 1999;46:711Y714. 11. Siegel-Itzkovich J. Israeli doctors warn against rubber bullets. BMJ. 2002;324:1296. 12. Di Maio Vincent JM. Gunshot Wounds. Boca Raton, FL: CRC Press; 1985:54Y78.

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ORIGINAL ARTICLE

Guidelines for the Recognition of Cemetery Remains in Greece Constantine Eliopoulos, PhD,* Konstantinos Moraitis, PhD,Þ Federico Reyes, PhD,þ Chara Spiliopoulou, MD, PhD,Þ and Sotiris Manolis, PhD*

Abstract: Forensic pathologists frequently consult anthropologists for the identification of skeletonized human remains. These remains may be the result of criminal activity or remains that were unearthed because of erosion, or during construction projects. In some cases, human remains that had been previously buried in a cemetery may be the subject of a forensic investigation. Early recognition of cemetery remains prevents unnecessary efforts and conserves precious resources. One of the key characteristics of cemetery remains is the presence of embalmed tissue. However, there are countries where embalming is not a common practice, and other clues must be sought for identifying previously buried remains. Current funerary customs in Greece and, in particular, the tradition of exhumations result in a large number of misplaced human remains. The present study presents examples of cemetery remains from Greece and offers guidelines for recognizing changes on skeletal remains that may be indicative of a cemetery origin. Location of discovery, condition of the remains, and the types of associated artifacts are all factors that aid forensic anthropologists in identifying cemetery remains.

cemetery remains in Greece is the absence of embalmed tissue, because embalming is not a routine procedure in this country. Embalming is not commonly performed in other parts of the world, and the guidelines offered here may be of interest to forensic practitioners in such countries where embalming is not frequently practiced or is forbidden.3 Some of the key characteristics of cemetery remains in Greece include the location of discovery, the condition of the remains, the presence or absence of specific skeletal elements, and the nature of any associated artifacts. The guidelines presented in this work are derived from observations made on cemetery remains during the creation of the modern human skeletal collection at the University of Athens, which consists of 225 documented skeletons.4 Other sources include forensic cases submitted to the Department of Forensic Medicine and Toxicology at the University of Athens and cases encountered during exhumations conducted for medicolegal purposes.

Key Words: anthropology, skeletal remains, autopsy artifacts, cemetery (Am J Forensic Med Pathol 2011;32: 153Y156)

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orensic anthropology is an emerging discipline in Greece, with less than a handful of scientists being actively involved in it. Currently, forensic anthropologists in the country are engaged in medicolegal casework, which is conducted at the Department of Forensic Medicine and Toxicology of the University of Athens. Other areas of practice for forensic anthropologists include research in human identification and participation in international projects involving the excavation of mass graves. Some of the cases submitted for examination include cemetery remains. These are defined as human skeletal remains belonging to individuals who had been legally buried in a cemetery. Renovations or closures of cemeteries or even the distinctive nature of the Greek funerary customs may result in the misplacement of human remains. To save on resources spent investigating such cases, some guidelines are offered that aid in the early recognition of cemetery remains. Previous studies in North America emphasize the presence of embalmed tissue and embalming artifacts as the main indications of remains from a cemetery context.1,2 The main difference of

Manuscript received January 7, 2009; accepted September 18, 2009. From the *Department of Animal and Human Physiology, Faculty of Biology, and †Department of Forensic Medicine and Toxicology, School of Medicine, National and Kapodistrian University of Athens, Athens, Greece; and ‡Stratford Road, London, UK. This article was presented at the 16th European Meeting of the Paleopathology Association, August 28 to September 1, 2006, Santorini, Greece. Reprints: Constantine Eliopoulos, PhD, Department of Animal and Human Physiology, Faculty of Biology, National and Kapodistrian University of Athens, Panepistimiopolis 157 84, Athens, Greece. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0153 DOI: 10.1097/PAF.0b013e3182156405

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FUNERARY CUSTOMS OF GREECE To be able to recognize cemetery remains, a forensic anthropologist needs to have a sound knowledge of the funerary customs of the local society. Today, in Greece, the vast majority of the population belongs to the Christian Orthodox faith (approximately 97%)5; therefore, it is appropriate to consider the funerary customs as these are dictated and practiced by the Greek Orthodox Church. In addition, current Greek laws concerning the disposition of human remains should be taken into account. In regard to embalming, it is not performed regularly, with the exception of the cases where the dead are to be transported to or from another country. Another instance where embalming is practiced is for prominent figures of society, where the remains are placed in a church for public viewing for 2 or 3 days. The customary treatment of the body, once death has been ascertained, includes cleaning, clothing, and placement in a coffin. The hands and sometimes the lower jaw are tied together so that they are not affected by the development of rigor mortis.6 In the past, all these activities would be carried out by the family of the deceased, but in recent years, funeral homes make all the necessary preparations. After a funeral service that takes place in the church, the coffin is taken to the cemetery where it is lowered into the grave. The orientation of the body in the grave is the feet being on the east side and the head to the west, according to Christian tradition. Within a few days of the funeral, a marble structure is built over the grave. Families usually visit the graves where they place flowers and light candles and incense.7 However, what sets Greek funerary customs apart is the practice of exhumations. Typically, 3 or 5 years after the inhumation of an individual, the remains are exhumed and placed in a metal box. This practice originated in monasteries, where space was usually limited. The remains of monks were exhumed after a number of years so that there was place for additional inhumations. Slowly and for practical purposes, this tradition

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was adopted by villages and cities throughout the country and has been incorporated into religious practice.8 For the storage of the boxes containing exhumed remains, special buildings within the cemeteries exist, known as ossuaries. After a number of years in the ossuary, the remains may be disposed of in a communal underground pit, also located within the cemetery. In contrast to other European countries where cremation is widely practiced, it was only recently legislated in Greece.9 In the past, those who wished to have the remains of their relatives cremated sent the remains through a funeral home to neighboring countries where this procedure was performed. As a result of the funerary tradition of exhumations, large numbers of skeletons are present above ground at any given time in Greece. Therefore, it is not uncommon to have human remains that are misplaced for a variety of reasons. For example, cemetery workers may discard skeletons when the ossuaries are filled, especially in rural areas where there are no underground pits. In addition, unclaimed skeletons may be given by cemetery authorities to medical students who use them for studying human anatomy. This takes place only after an official application has been submitted to the cemetery director. At the end of their studies, the students will either pass the skeletons on to other students or dispose of them in refuse containers or secluded, nonresidential areas. Another manner in which human remains may be misplaced, which, however, is rare, is the unauthorized removal of remains from some ossuaries by individuals who wish to perform practical jokes.

LOCATION OF THE DISCOVERED REMAINS Greek cemeteries are operated by the municipalities in which they are located. With the exception of some family graves that are permanent, the majority of graves are reused at intervals of 3 years. The same is true for smaller communities such as villages. Here, however, the trend of shrinking populations does not present a problem of space in cemeteries; therefore, exhumations may take place after 5 years. The practice of exhumation and reuse of the graves ensures that cemeteries continue to be operational, because there is always space for new burials. A typical cemetery of relatively large size in the area of Athens has 20,000 graves and 15,000 boxes of exhumed remains stored in the ossuary. In some instances, cemeteries have to close so that the municipalities use the land for other purposes. In cases like these, the closure is not complete, but it involves only nonpermanent graves. Therefore, only part of the cemetery land may change its use. Permanent graves, which are usually located near the cemetery entrance and take up a small portion of the property, are rarely relocated. Two partial closures have taken place in the greater Athens area in recent years. The cemeteries of Neapoli and Anastasi have closed their areas of nonpermanent graves. This has been achieved gradually by not conducting any new inhumations in the past few years. When remains are found at or near old cemeteries, there is a high probability that these are not of forensic interest. However, location alone is not conclusive evidence for the presence of cemetery remains, and a proper assessment must take into consideration some additional factors, the most important of which is the condition of the skeletal elements.

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microenvironment of the grave are elements related to the physical traits of the remains that will be observed at the time of examination.10 Embalming has been noted as a key factor in the identification of cemetery remains. Researchers from North America, where embalming is very common, have described a number of attributes encountered in embalmed tissue.1,2 In Greece, however, embalming is not common, and the few embalmed bodies are usually buried in permanent graves. Observations on a large number of cemetery remains in Greece have resulted in the identification of a number of traits that are indicative of their origin. Most notable is coffin wear, a finding that has been described in other studies.1,11 Coffin wear refers to the erosion of pressure points of the supine skeleton, often observed on the occipital, scapular spines, humeral heads, spinous processes of the vertebrae, sacrum, innominates, and femora (Fig. 1). This erosion may be slight and affect only the superficial layers of the cortical bone, or in some cases, it may extend to the point that the underlying trabecular bone is exposed. In Greece, all coffins have a layer of sawdust in the bottom to absorb any decomposition fluids. Therefore, it is not uncommon to find sawdust adhering to the posterior surfaces of bones. Another trait found by the authors is the presence of both head and facial hair in many cases, a finding previously reported as being the result of the embalming process.1 Similarly, dehydrated brain tissue was found in cemetery remains in Greece, although the bodies had not been embalmed. These 2 unexpected finds may be the result of the hot and dry climate of Athens. Such climatic conditions could lead to the dehydration of tissues and prevent decomposition. The effect of the environmental conditions is further supported by the fact that mummified tissue was found in some remains, especially in the hands and feet. One of the standard procedures in cases of unexpected or violent deaths is the forensic autopsy. This process leaves its marks on the human body, and as expected, some cemetery remains possess the autopsy artifacts. First, the cranium is sectioned with an oscillating saw, to enable the examination of the brain.12,13 There are different types of autopsy cuts of the cranial vault, and some may be mistaken for perimortem trauma, especially in cases of fragmentary remains (Figs. 2AYD). Therefore, it is useful to be familiar with the characteristics and variation in autopsy cuts of the cranium. Another procedure that is typically performed during autopsy in Greece is the placement of absorbent fabric material within the cranial cavity

CONDITION OF THE REMAINS A number of factors may affect the degree of decomposition and overall condition of cemetery remains. Time since death, the condition of the body at the time of burial, and the

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FIGURE 1. Erosion of posterior femur and humerus (coffin wear). * 2011 Lippincott Williams & Wilkins

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Recognition of Cemetery Remains

FIGURE 2. AYD, Different types of cranial autopsy cuts.

after examination of the brain. The reason for this procedure is to prevent slippage of the skullcap from the base of the cranium during suturing of the head and to reduce the possibility of fluid leakage. During autopsy the ribs, sternum and clavicles are sectioned by saws or rib shears for the removal of the breastplate to enable the inspection of the thoracic viscera (Fig. 3). In addition, incisions to reflect the skin and subcutaneous tissue and expose the internal organs along the thoracic wall may result in cut marks on the ventral surface of the ribs.14 Anthropologists should be aware of the location and nature of these cuts so they are not confused with those produced in cases of intentional dismemberment or other types of sharp force trauma. Remains that have been used by medical students usually have a uniform bleaching covering all surfaces of each bone. Most students clean the skeletons by use of household bleach, which makes them white but may also cause chemical erosion. In

some cases, the bones have been drilled and articulated with wire (Fig. 4).15 Sometimes, bones used by students exhibit evidence of excessive handling, in the form of postmortem fractures. Furthermore, remains that have been taken from ossuaries and used for practical jokes may have residue of candle wax, paint, or even writing on them. Another sign that is suggestive of cemetery origin is the presence of excavation damage to the bones. This type of postmortem damage is most often caused by shovels, picks, and other tools used by cemetery workers. To make a correct

FIGURE 3. Autopsy cuts of the lateral parts of the manubrium.

FIGURE 4. Proximal radius and ulna showing evidence of drilling.

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assessment of the condition of the remains, it is necessary to have contextual information. Therefore, the examination of the scene by the anthropologist is essential so that all the taphonomic parameters can be considered.16

ASSOCIATED ARTIFACTS In addition to the physical appearance of cemetery remains, artifacts that are found in association with them may provide clues to their origin. Some of the most obvious artifacts are remnants of the coffin. These can include nails, handles, trimmings, or pieces of wood. Since the mid-1980s, the material used for coffins is MDF (medium-density fiberboard). Before that time, all coffins were made of oak, chestnut, or walnut. Aside from the material being used as an aid to establish chronology, some funeral directors can approximate the year of manufacture of a coffin, based on its stylistic design. Artifacts that may be found in association with cemetery remains also include crosses and icons that are placed in the coffin with the body. Pieces of marble, plastic flowers, oil lamps, incense holders, and framed photographs can also be found with the remains, as these are commonly part of the grave. Embalming artifacts are rarely found, because this practice is not widespread in Greece.

SUMMARY The current work was prompted by similar publications based on observations in North America, where burial customs are very different. Colleagues from countries where embalming is not widely practiced may benefit from the indicators presented in this article, so that cemetery remains are recognized early in the investigation. To identify skeletal remains that are not of forensic interest, a combination of the attributes presented here must be evaluated, because relying on a single indicator may be misleading. It is important to stress that forensic anthropologists should be familiar with local funerary traditions, so that they can recognize cemetery remains. The purpose of this is not to stop an investigation, but rather to help place investigation efforts into the right direction, thereby saving valuable time and other resources. ACKNOWLEDGMENTS The authors thank Mr K. Vervitas, vice president of the Athens Association of Funeral Directors, for information regarding practical aspects of funerals in Greece. They also thank Dr W. D. Haglund for his very useful comments during the preparation of the article.

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REFERENCES 1. Berryman HE, Bass WM, Symes SA, et al. Recognition of cemetery remains in the forensic setting. In: Haglund WD, Sorg MH, eds. Forensic Taphonomy: The Postmortem Fate of Human Remains. Boca Raton, FL: CRC Press; 1997:165Y170. 2. Rogers TL. Recognition of cemetery remains in a forensic context. J Forensic Sci. 2005;50:1Y7. 3. Adams VI, Ludwig J. Autopsy law. In: Ludwig J, ed. Handbook of Autopsy Practice. 3rd ed. Totowa, NJ: Humana Press; 2002:159Y165. 4. Eliopoulos C, Lagia A, Manolis S. A modern, documented human skeletal collection from Greece. HOMO. 2007;58:221Y228. 5. Bureau of Democracy, Human Rights, and Labor. International Religious Freedom Report 2008: Greece. US Department of State Web site. September 19, 2008. Available at: http://www.state.gov/g/drl/ rls/irf/2008/108449.htm. Accessed December 21, 2008. 6. Green J, Green M. Dealing with Death: A Handbook of Practices, Procedures and Law. 2nd ed. London: Jessica Kingsley Publishers; 2006. 7. Danforth LM. The Death Rituals of Rural Greece. Princeton, NJ: Princeton University Press; 1982. 8. Christodoulou TS. Regarding the Funeral [in Greek]. Athens, Greece: Omologia; 2004. 9. Greek Law 3448/06, Article 35. 10. Gill-King H. Chemical and ultrastructural aspects of decomposition. In: Haglund WD, Sorg MH, eds. Forensic Taphonomy: The Postmortem Fate of Human Remains. Boca Raton, FL: CRC Press; 1997:93Y108. 11. Ubelaker DH. Human Skeletal Remains: Excavation, Analysis, Interpretation. Washington, DC: Taraxacum; 1989. 12. Valentin F, d’Errico F. Brief communication: skeletal evidence of operations on cadavers from Sens (Yonne, France) at the end of the XVth Century. Am J Phys Anthropol. 1995;98:375Y390. 13. Knight B. Forensic Pathology. 2nd ed. London: Arnold; 1996. 14. Sheaff MT, Hopster DJ. Post Mortem Technique Handbook. 2nd ed. London: Springer; 2005. 15. Sledzik PS, Micozzi MS. Autopsied, embalmed, and preserved human remains: distinguishing features in forensic and historic contexts. In: Haglund WD, Sorg MH, eds. Forensic Taphonomy: The Postmortem Fate of Human Remains. Boca Raton, FL: CRS Press; 1997:483Y495. 16. Haglund WD. The scene and context: contributions of the forensic anthropologist. In: Reichs KJ, ed. Forensic Osteology: Advances in the Identification of the Human Remains. 2nd ed. Springfield: Charles C. Thomas; 1998:41Y62.

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ORIGINAL ARTICLE

Class Characteristics of Serrated Knife Stabs to Cartilage Derrick J. Pounder, FRCPA, Lesley Cormack, BMSc, Elizabeth Broadbent, BMSc, and John Millar, MB

Abstract: A total of 136 stab wounds were made in cartilage with 8 serrated knives and 72 stabs with 4 nonserrated knives. The walls of the stab track were documented by photography, cast with dental impression material, and the casts photographed. Staining the translucent cartilage surface with blue or green food dye improved photography. Serrated blades produced striations on cartilage in all stabbings. Patterns of blade serration beyond the broad categories of coarse and fine were recognizable. The overall pattern of striations was Birregularly regular.[ The distance between the blade-spine wound end and the first serration striation is a class characteristic of the knife which produced the defect, as are distances to the subsequent serration striations, which become ever close together and eventually merge near the blade-edge wound end. Serrated knives may be ground (scalloped) on either the left side or the right side of the blade and this class characteristic is identifiable from the walls of the wound track, on which the scalloped blade surface produces broad ridges and narrow striation valleys, with a reverse image on the opposing wound wall. A drop point serrated blade consistently produced an additional oblique mark angled from the blade-spine wound end, accurately reflecting the shape of the blade tip, and representing a chatter mark. Key Words: stab wounds, serrated knives, class characteristics, striations, chatter mark (Am J Forensic Med Pathol 2011;32: 157Y160)

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tabbing is a common method of homicide in many jurisdictions, and often the knife is a weapon of opportunity in the home.1 In a domestic setting, serrated knives are increasingly common, as is their use in homicides. Standard forensic texts state that stab wounds caused by serrated blades are not generally distinguishable from those caused by nonserrated blades.2 An important exception, recorded in the literature but not widely appreciated, is that stab wounds from serrated knives involving costal cartilages leave striations on the cut surface of the cartilage from the serration points on the blade edge. The renowned German forensic expert Wolfgang Bonte (1939Y2000) first drew attention to these tool marks on cartilage in the English language literature,3 having already published on the phenomenon in the German literature.4 Rao and Hart5 later reported a case in which grossly visible striae were observed on cut costal cartilages in a homicidal stabbing in which a serrated knife had been used. The literature contains few follow-up studies over the past 25 years,6Y9 a fact adversely commented upon in an appeal against a murder conviction in Florida,10Y12 which itself initiated vigorous debate.13,14

Manuscript received August 3, 2009; accepted November 16, 2009. From the Centre for Forensic and Legal Medicine, University of Dundee, Scotland, United Kingdom. Reprints: Derrick J. Pounder, FRCPA, Centre for Forensic and Legal Medicine, University of Dundee, Dundee DD1 4HN, Scotland, United Kingdom. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0157 DOI: 10.1097/PAF.0b013e3181db7ee4

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In light of the increased availability of serrated knives, the high frequency of anterior thorax wounds in homicidal stabbings,15 and the potential value of the examination of severed costal cartilage for the purpose of including or excluding a putative weapon, we undertook a study of experimental stab wounds in porcine and bovine costal cartilage using a variety of serrated blades to assess the potential utility of the technique.

MATERIALS AND METHODS Serrated knives were purchased in department stores and their characteristics documented. Standard terminology with respect to knife blade anatomy has been used16: the edge of the blade refers to the working part or cutting surface; the spine of the blade refers to the top of the blade opposite the edge, and is unsharpened in the single-edged blades used in these experiments; the tip of the blade refers to the forward quarter of the blade and includes the point, which is the very end part of the blade; the right side of the blade is the side towards the right of a person holding the knife by the handle, tip uppermost, with the edge facing away from the holder_s body, and similarly the left side of the blade is on the left side of that person. (When displayed knives are traditionally positioned with the handle to the right side of the viewer, the blade to the left side of the viewer, with the edge below and the spine above, so that the left side of the blade faces the viewer). The term Bback of the blade[ has not been used since this may refer to either the spine or the right side of the blade so giving rise to confusion. Serrations17 are introduced during the final grinding process by removing scallops of metal from the blade edge on one side (either the right or the left) leaving the other side flat, so that serrated blades may be either right side ground (scalloped) or left side ground (scalloped). Porcine and bovine rib cages were sourced from a commercial butcher and lengths of rib cartilage were dissected away from the sternum and ribs. The cartilage was tethered at both ends with string tied to nails at the corners of a wooden chopping board with the cartilage sitting upon a 500 g block of modeling clay, to allow for penetration of the blade through the cartilage. The stabbing was achieved slowly with the knife at 90- to the cartilage and the knife then withdrawn. The section of cartilage with the stab wound was trimmed to a smaller size and the stab wound opened by inserting a scalpel blade back first into the wound and rotating the scalpel so as to extend the ends of the stab canal to the margins of the cartilage without damaging the stab track. Stabs were performed and stab wounds dissected in a systematic way so that the right wall of the stab wound corresponding to the right side of the knife blade and the left wall of the stab wound corresponding to the left side of the knife blade were always identified. The exposed stab wound surface was rinsed with water and blotted dry with paper towel. The cut surfaces were examined by naked eye and then photographed using markedly oblique lighting to accentuate any striations. A range of colors (red, blue, green, yellow, and black) of food dye were used to stain the cartilage in an attempt to reduce specimen translucency and reflectance which made photodocumentation difficult. After photo-documentation the cut surfaces were cast using Provil Novo Medium C.D.2 fast set vinyl

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FIGURE 1. Cast of the left wall of a stab in cartilage from a straight spine left-side ground serrated blade (mm scale). The distance between striations reduces with increasing distance from the wound end representing the spine of the blade.

polysiloxane dental impression material (Heraeus Kultzer, South Bend, IN). The casts were photographed.

RESULTS AND DISCUSSION Stab wounds made using a drop point coarsely serrated blade (32 stabs), 3 different straight spine coarsely serrated blades (60 stabs), a straight spine finely serrated blade (12 stabs), a straight spine mixed coarse and finely serrated blade (12 stabs), a drop point finely serrated blade (20 stabs), and a clip point blade with coarse serrations, produced prominent striations on the cartilage in all cases. Stabs with 3 different drop point nonserrated blades (60 stabs) and a straight spine nonserrated blade (12 stabs) produced no gross striations of the type produced by serrated blades, although much finer striations corresponding to blade edge imperfections could sometimes be seen. Photography of striation marks on the cut surface of the cartilage was difficult due to translucency and reflections.5 Prolonged exposure to the heat of photographic lighting dried the specimen. Staining the cartilage surface with a blue food dye improved the quality of photographs, as did the green dye but to a lesser extent. There was no substantial improvement using red, yellow, or black food dyes. Photography of the opaque dental casting material was straightforward and striation marks were more readily recorded in photographs of casts. In all of the stab wounds, using a variety of serrated knives it was possible to identify by naked eye examination striations on the cut surface of the cartilage corresponding with the serration points of the blade. Stabs produced by coarsely serrated blades were easily distinguished from those produced by finely serrated blades. The pattern of serrations on a standard coarsely serrated knife blade is characterized by a gap between the point of the blade and the first serration point, with subsequent serration points being evenly spaced along the length of the blade. With the knife blade passing vertically through the cartilage this serration pattern on the blade leaves a significant gap between the wound end corresponding to the blade spine and the first striation representing the first serration point. Subsequent striations on the cartilage, corresponding to serration points further along the blade, are separated by decreasing distances between each other, corresponding with the projected alignment of the serrations relative to the width of the blade (Fig. 1). Toward the other end of the wound, corresponding to the cutting edge of the blade, the striation marks are so close together or overlaid that they are not individually recognizable. The pattern could be characterized as Birregularly regular.[ It is this overall pattern which is characteristic of a serrated blade. With finely serrated blades the individual fine striations are visible and grouped, as are the serrations on the blade, with

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sparing between the groupings. The overall pattern produced is the same as with coarsely serrated blades except that the single coarse striations are replaced by groups of fine striations which become ever narrower with an ever reducing distance between the groupings ie, the same Birregularly regular[ pattern. The pattern of fine serrations on a blade is an identifiable class characteristic as a result of between-blade variability in the number of striations per group, the extent of sparing between striation groups and the presence or absence of interspersed coarse striations. Within the overall pattern of striations there is a variability which reflects class characteristics of the blade. The distance between the end of the wound representing the spine of the blade and the first serration striation mark is a class characteristic, as are the distances of all of the subsequent serration striations (or groups of striations from finely serrated blades) from the blade-spine wound end. The 2 factors determining these latter distances would appear to be the distance between the serration points on the blade and the shape of the blade. Since both of these factors are unknown if the blade is not available, it would seem impossible to reliably deduce either from the pattern of serrations. It may be possible, at least in theory, for two quite different blades, having different blade shapes and different separations of serration points, to produce the same or a closely similar pattern of striation marks. Therefore, some caution should be exercised in weighing the significance of a serration pattern which appears identical to a putative weapon until further experience and data is acquired. With coarsely serrated blades, the striations observed correspond with the prominent tips of the serrations on the blade so that the space between them corresponds with the scalloped edge of the serration. If the scalloping is on the left side of the blade then the scallops create broad ridges on the left wall of the wound with narrow striation valleys between representing the serration points. By contrast the right wall of the same wound track shows mirror-image broad valleys with narrow striation ridges between. In this way an examination of the 2 walls of the wound allows a determination of whether the serrated blade which produced it was left side scalloped (ground) or right side scalloped (ground). When making this assessment from casts rather than the original wound it is important to remember that the cast is a reverse image of the original, so that the cast of the right wall of the wound has the same appearance as the original left wall of the wound. In both the original specimen and casts it is easier to observe the striations when they are present as ridges

FIGURE 2. Cast of the left wall of a stab in cartilage from a drop point right-side ground serrated blade (mm scale). The striations appear as broad ridges with narrow valleys between. Contrast with Figure 3. * 2011 Lippincott Williams & Wilkins

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FIGURE 3. Cast of the right wall of a stab in cartilage from a drop point right-side ground serrated blade (mm scale). The striations comprise broad valleys with narrow ridges between. Contrast with Figure 2.

rather than valleys, because they stand out more sharply in oblique lighting (Figs. 2 and 3). In one set of experiments, in all of 20 of stab wounds using a drop point coarsely serrated blade, an oblique mark was observed passing from the wound edge corresponding to the spine of the blade upwards towards the surface of the wound in the cartilage. The mark was present but faint in 20%; present, fully formed but not readily obvious to an untrained eye in 50%; and clearly visible even to an untrained eye in 30% (Fig. 4). By contrast for a straight spine coarsely serrated blade the mark was seen in only 1 of 20 stabs, and then it was fully formed but not obvious to an untrained eye (Fig. 5). A similar mark was not observed in 20 stab wounds made with a drop point nonserrated blade. Comparison of this mark with the knives indicated that it represents the blade edge at the tip. The V-shape between the blade-spine wound end and this mark reflects accurately the shape of the tip of the blade (Fig. 6). The location of this unusual mark suggests that it was produced when tissue was initially trapped in the concavity of the first scallop, causing the blade to jar slightly. If this proposed mechanism of formation is correct then it would be appropriate to characterize the mark as a Bblade tip chatter mark.[ The greater prominence and frequency of this chatter mark in stabs from the drop point serrated blade may be the result of either the more prominent serrations of that blade and/or the drop point shape which increases the initial lateral

FIGURE 4. Cast of the right wall of a stab in cartilage from a drop point right-side ground serrated blade showing a prominent blade tip chatter mark (mm scale).

Characteristics of Serrated Knife Stabs to Cartilage

FIGURE 5. Cast of the left wall of a stab in cartilage from a straight spine left-side ground serrated blade (mm scale). The striations appear as broad valleys and narrow ridges. There is a barely discernable blade tip chatter mark.

movement of the blade during the stabbing. It remains to be seen whether this is merely a feature of the experimental model or is observable in case material. In summary the class characteristics of a serrated blade which might be determined from striation marks in cartilage include (a) the overall pattern of coarse and/or fine serrations, (b) the distance between the spine of the blade and the first serration point, (c) the distances between the spine of the blade and the subsequent serration points, (d) whether the blade was right side or left side ground (scalloped), and (e) the shape of the tip of the blade if a chatter mark is present. We have not addressed in this study the issue of finer striations produced by imperfections in blades, both serrated and nonserrated, which may be individualizing characteristics and so provide further valuable tool mark information.

FIGURE 6. The blade tip chatter mark as shown in Figure 5 together with the straight spine serrated blade which produced it (mm scale).

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REFERENCES 1. Ormstad K, Karlsson T, Enkler L, et al. Patterns in sharp force fatalities- a comprehensive forensic medical study. J Forensic Sci. 1986;31:529Y542. 2. Spitz W. Sharp force injury. In: Spitz W, ed. Spitz and Fisher_s Medicolegal Investigation of Death: Guidelines for the Application of Pathology to Crime Investigation. 4th ed. Springfield, IL: Charles C. Thomas; 2006:566. 3. Bonte W. Tool marks in bones and cartilage. J Forensic Sci. 1975;20: 315Y325. 4. Bonte W. Considerations on the identification of notch traces from stabbing injuries [in German]. Archiv Fu¨r Kriminologie. 1972;149: 77Y96. 5. Rao V, Hart R. Tool mark determination in cartilage of stabbing victim. J Forensic Sci. 1983;28:794Y749. 6. Ernest RN. Toolmarks in cartilage revisited. AFTE J. 1991;23:958Y959. 7. Mikko D, Hornsby BJ. On the cutting edge IIYYan identification involving a knife. AFTE J. 1995;27:293. 8. Thompson E, Wyant R. Knife Identification Project (KIP). AFTE J. 2003;35:366Y370. 9. Wong DT. Preservation and examination of tool marks on cartilage and bone. AFTE J. 2007;39:265Y280.

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10. Joseph J Ramirez v. State of Florida, Supreme Court of Florida, No. 66,992, March 16, 1989. Available at: www.law.fsu.edu/library/flsupct/ 66992/op-66992.pdf. Accessed July 29, 2009. 11. Joseph J Ramirez v. State of Florida, Supreme Court of Florida, No. 78,386, January 5, 1995 Available at: http://www.law.fsu.edu/library/ flsupct/78386/op-78386.pdf. Accessed July 29, 2009. 12. Joseph J. Ramirez v State of Florida, 2001 WL 1628609, 27 Fla. L. Weekly S18. Supreme Court of Florida; 2001. 13. Garcia CH. Are knife-prints reliable evidence: an analysis of tool mark evidence and Ramirez v. State. AFTE J. 1993;25: 226Y280. 14. Clow CM. Cartilage stabbing with consecutively manufactured knives: a response to Ramirez v. State of Florida. AFTE J. 2005;37: 86Y116. 15. Karlsson T. Homicidal and suicidal sharp force fatalities in Stockholm, Sweden. Orientation of entrance wounds in stabs gives information in the classification. Forensic Sci Int. 1998;93:21Y32. 16. Fisher J. Knife anatomy, parts, names, components and definitions. Available at: http://www.jayfisher.com/knife_anatomy,_parts,_names. htm#Knife_Definitions. Accessed September 24, 2009. 17. Wolf B. The New Cooks_ Catalogue. New York, NY: Knopf; 2000. Available at: http://www.cooking.com/products/howtobuy/experts. asp?ClassNo=0510. Accessed September 24, 2009.

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ORIGINAL ARTICLE

Homicides of Pregnant Women Peter Lin, MD and James R. Gill, MD

Abstract: Homicidal injury is a leading cause of death among pregnant and postpartum women in the United States. We studied all homicides in which the victim was pregnant at the time of the lethal injury. Records of the New York City Office of Chief Medical Examiner were reviewed. There were 27 homicides: the age ranged from 15 to 41 years (mean 27 years). The causes of death were: 13 gunshot wounds, 7 asphyxial deaths (eg, neck compression), 5 stabs, 1 blunt, and 1 blunt/stab. The gestational age ranged from 8 weeks to 40 weeks with an average of 24.5 weeks. Two live born infants (40 and 28 weeks gestation) were delivered following gunshot wounds of the mother and infant, however, both subsequently died. The victim and suspect were known to each other in 19 homicides. Of these, 16 involved an existing or prior intimate relationship including: 2 current husbands, 1 ex-husband, 9 current boyfriends, 3 ex-boyfriends, and 1 father. The issues that arise for the forensic pathologist include proper collection of a DNA sample from the fetus, estimation of the gestational age, and certification of death. Key Words: forensic pathology, homicide, pregnant, maternal, matricide, fetus (Am J Forensic Med Pathol 2011;32: 161Y163)

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omicidal injury is a leading cause of death among pregnant and postpartum women in the United States.1 Until the most recent international classification of diseases, injuries, and death (ICD-10), the definition of maternal death differed among various public health agencies. The Centers for Disease Control and Prevention used the terms pregnancy-related and pregnancy associated deaths because the ICD-9 did not include these deaths.2 The current ICD-10 includes deaths due to injuries (Table 1).3 In the United States, maternal mortality over the past century has dramatically decreased.4 Maternal mortality from injuries, however, has remained constant.5 Homicidal and other types of injuries are major contributors to maternal mortality.6 The homicide of a pregnant woman raises both medicolegal and legal issues with regard to death certification and the criminal justice system. In some jurisdictions, the death of the fetus may be considered in homicide charges.7 We review 11 years of homicides investigated by the New York City Medical Examiners Office in which the victim was pregnant at the time of death.

MATERIALS AND METHODS The New York City Office of Chief Medical Examiner (NYC OCME) investigates all unexpected, violent, and suspicious deaths in New York City. By statute, these deaths must be reported to the OCME. Between January 1, 1998 and January 1, 2009, there Manuscript received August 6, 2009; accepted September 18, 2009. From the New York City Office of Chief Medical Examiner and Department of Forensic Medicine, New York University School of Medicine, New York, NY. Reprints: James R. Gill, MD, Office of Chief Medical Examiner, 520 First Avenue, New York, NY 10016. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0161 DOI: 10.1097/PAF.0b013e3181d3dc3b

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were 6578 homicides investigated and certified by the NYC OCME. We searched all medical examiner death certificates and electronic autopsy reports between January 1, 1998 and January 1, 2009 in which the decedent was pregnant at the time of death and the manner of death was homicide. We reviewed the medical examiner records which included the autopsy, toxicology, police, and medical examiner investigators_ reports. All deaths underwent autopsy and toxicology testing. The manner of death is determined by the circumstances and the cause of death. It includes: natural, accident, suicide, homicide, therapeutic complication, and undetermined.8 The medicolegal definition of homicide is death at the hand of another or death due to the hostile or illegal act of another.9 In New York State, fetal death is defined as Bdeath prior to the complete expulsion or extraction from its mother of a product of conception, indicated by the fact that after such separation, the fetus does not breathe or show any other evidence of life such as beating of the heart, pulsation of the umbilical cord, or definite movement of voluntary muscles[ (Public Health Law Section 4160(1)). In New York, the fetal death certificate requires the cause of death but not the manner of death. Postmortem blood was collected in each death, preserved with sodium fluoride, and stored at 4-C. All toxicologic testing was performed by the Forensic Toxicology Laboratory at the Office of Chief Medical Examiner. Ethanol concentrations were determined in blood using head space gas chromatography. Urine specimens were routinely tested for opiates, barbiturates, benzoylecgonine (BE), and methadone by enzyme immunoassay. If urine were not available, blood was tested for opiates, BE, and barbiturates using radioimmunoassay. Quantitations of morphine, codeine, and BE were done using gas chromatography/mass spectrometry (GC/MS). Urine or blood also was analyzed for basic drugs (including cocaine) by gas chromatography with a nitrogen phosphorous detector (GC/NPD). Homicides were classified by the following circumstances: family dispute/abuse, current or former intimate partner, dispute, robbery, drug-related, sex-crime, random, unknown.

RESULTS There were 27 homicides: the maternal age ranged from 15 to 41 years (mean = 27 years) and the racial/ethnic breakdown included 21 Black, 5 Hispanic, and 1 White. The causes of death included: 13 (48%) gunshot wounds, 7 (26%) asphyxial deaths (eg, neck compression), and 5 (18%) stabs, 1 (4%) blunt, and 1 (4%) blunt/stab. For homicides of all women between the ages of 12 to 44 years over a 3 year period, there were: 35% gunshot wounds, 30% sharp injuries, 19% asphyxia, 8% blunt, 4% thermal injury, and 4% combination. The gestational age ranged from 8 to 40 weeks with an average of 24.5 weeks. In 2 instances, only a gestational sac was identified, and in one instance, only an implantation site was identified. In 2 instances, a liveborn infant was delivered but subsequently died, both of which involved gunshot wounds of the mother and infant. These 2 infants were certified as homicides. In 22 of the 27 homicides, information concerning the relationship of the victim to the suspected perpetrator was available.

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TABLE 1. Definitions of Maternal Deaths Definition Maternal death

Late maternal death Direct obstetrical deaths Indirect obstetrical deaths

Pregnancy-related deaths Pregnancy-associated deaths

Pregnancy-related deaths

The death of a woman while pregnant or within 42 d of termination of pregnancy, irrespective of the duration and site of the pregnancy, from any cause related to or aggravated by the pregnancy or its management but not from accidental or incidental causes.2 The death of a woman from direct or indirect obstetric causes more than 42 d but less than one year after termination of pregnancy. Those that result from obstetrical complications of the pregnancy, labor, and puerperium. Those that result from previous existing disease or disease that developed during pregnancy and which was not due to direct obstetrical causes but was aggravated by the physiologic effects of pregnancy The death of a woman while pregnant or within 42 d of termination of the pregnancy, irrespective of the cause of death. All natural and unnatural deaths that occur during pregnancy or the post-partum period, defined as anytime up to 1 yr following termination of pregnancy. A pregnancy-associated death that is causally related to pregnancy.

Immediate/Proximate Causes

Organization

Eclampsia, sepsis due to chorioamnionitis, hemorrhagic complications, hypertensive cardiovascular disease

WHO/ICD-10

Peripartum cardiomyopathy

WHO/ICD-10

Eclampsia, sepsis due to chorioamnionitis, hemorrhagic complications Hypertensive cardiovascular disease, rheumatic heart disease

WHO/ICD-10

Gunshot wound, blunt injury, drug intoxication

WHO/ICD-10

Gunshot wound, blunt injury, drug intoxication

CDC/ACOG

Peripartum cardiomyopathy, rheumatic heart disease aggravated by the physiologic effects of pregnancy

CDC/ACOG

WHO/ICD-10

WHO/ICD-10 indicates World Health Organization/Manual of the International Statistical Classification of Diseases, Injuries, and Causes of Death, 10th edition (1993); CDC/ACOG, Center for Disease Control and Prevention/American College of Obstetricians and Gynecologists.

In 3 homicides, the victim was an innocent bystander. The victim and suspected perpetrator were known to each other in 19 homicides. Of these, 16 involved an existing or prior intimate relationship (the suspected perpetrators included 2 current husbands, 1 ex-husband, 9 current boyfriends, 3 ex-boyfriends, and 1 father), 1 involved gang-related activity, 1 robbery, and 1 retaliation by a neighbor for a prior robbery. Of the intimate partner deaths, 9 were due to gunshot wounds, 4 due to asphyxia, 2 sharp injury, and 1 blunt and sharp injury. No suspect was known in 5 deaths. Toxicological analysis on samples obtained from the autopsy was negative in 21 of the 27 homicides. Cocaine and ethanol were detected in 2 instances, cannabinoids in 2 instances, cocaine and methadone in 1 instance, and fluoxetine, benzodiazepines, and methamphetamine in 1.

DISCUSSION Homicidal injury is a leading cause of death among pregnant women in the United States.1,4Y6,10Y16 We review 11 years of homicides in New York City in which the victim was pregnant at the time of the fatal injury. Maternal mortality in the United States due to all causes has decreased dramatically over the past century, however, maternal mortality due to injuries has not decreased.4,5 Until 1993, maternal mortality was defined by the World Health Organization (WHO/ICD-9) as deaths due to natural complications of pregnancy and the postpartum period, such as hemorrhage or pulmonary embolism; deaths due to unnatural causes, including homicidal, suicidal, and accidental injuries, were excluded.7 To better capture all maternal deaths, the Centers for Disease Control and the American College of Obstetricians and Gynecologists, recommended in 1987 the term

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Bpregnancy-associated[ death to include all natural and unnatural deaths that occur during pregnancy or the postpartum period, defined as anytime up to 1 year following termination of pregnancy (Table 1). Using this broadened definition of pregnancy-associated death, recent studies have identified homicidal injury as a leading cause of death among pregnant women.5,12 Chang et al found homicidal injury to be the second most common cause of death among pregnant and postpartum women in the United States.1 Krulewitch et al found that pregnant adolescent women are 3 times more likely to be victims of homicide than their nonpregnant counterparts.10 Since a comprehensive national database of pregnancy-associated mortality was not readily available, the most reliable method for identifying pregnancy-associated deaths was through a combination of death record analysis (eg, linkage of death records with live birth and fetal death records, and review of medical examiner records). The majority of maternal homicides in this study were due to gunshot wounds. This is similar to a study by Dannenberg et al that analyzed maternal homicides between 1987 and 1991 in New York City. They reported that 39% of maternal deaths were due to injury of which 63% were homicides. Of these, 51% were due to gunshot wounds, 19% from sharp injury, 14% from strangulation, 7% from thermal injury/smoke inhalation, and 7% from blunt injuries. A high percentage of nongunshot-wound deaths might be expected in the intimate partner cohort if these are impulsive homicides and the perpetrators use what is available. Gunshot wound deaths, however, occurred more frequently than all other causes combined. This differed from the distribution of homicides among nonpregnant women of * 2011 Lippincott Williams & Wilkins

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child-bearing age which included 35% due to gunshot wounds (30% sharp injury, 19% strangulation, 8% blunt injury, and 4% thermal injury/smoke inhalation). The medical examiner_s role in these fetal/infant deaths is multifold. In instances where the fetus was delivered during or shortly after the maternal death, one must determine whether he/she was live born. The manner of death of the infant may have major legal repercussions.7 In New York State, a fetal death is defined as death Bprior to the complete expulsion or extraction from its mother of a product of conception, indicated by the fact that after such separation, the fetus does not breathe or show any other evidence of life such as beating of the heart, pulsation of the umbilical cord, or definite movement of voluntary muscles[ (Public Health Law Section 4160(1)). In these instances, a fetal death certificate is issued with only the cause of death and no manner of death listed. If there is any sign of life after expulsion, then this is a liveborn infant and he/she receives the standard death certificate with the cause and manner of death. Infant deaths due to homicidal maternal injury would be certified as homicides. If the fetus/embryo is Bdelivered[ at the autopsy, no death certificate is issued for the product of conception. Several procedures should be done during the autopsy of these homicides. The first is the collection of a DNA sample of the fetus or infant. This may include fetal/infant blood/tissue depending upon the size of the gestation. Placenta tissue is the least desirable because it has a mixture of DNA. The gestational age is determined by various body measurements (body and foot lengths). The extent of the examination of the embryo/fetus/ infant will depend upon the size of the conception and the presence or absence of direct fetal trauma. Investigation of clinical observations and pathologic examination of the placenta should be done for evidence of placental trauma (eg, abruption due to blunt injury). Acute abruptions may best be detected by sonography or at delivery since little blood may remain attached to the placenta by the time it is examined pathologically. Following the autopsy, the previously undelivered embryo/ fetus is returned to the mother_s body. The specific disposition of the fetal remains should be mentioned in the autopsy report. If the infant (or stillborn fetus) had been delivered prior to the autopsy, he/she should receive a unique laboratory number and is not returned to the mother_s body. A majority of suspected perpetrators were known to the victim and most were intimate partners. Intimate partner violence is a common scenario for female homicide regardless of whether the woman is pregnant. Anecdotal reports in some of the deaths in this study support the pregnancy as the motive for the homicide (boyfriend killed her because he did not want the responsibility) but without detailed information of all deaths of woman of child-bearing age, it is not statistically possible to confirm this risk factor.12,17 In the current ICD-10, changes were made to the classification and coding of maternal deaths. The changes pertain to indirect maternal causes and timing of deaths relative to pregnancy. BLate maternal death[ and Bpregnancy-related death[ were introduced in the ICD-10. The terminology has become complicated because various US agencies (eg, CDC_s Division of Reproductive Health) use different terms but with similar concepts. For example, the CDC_s Division of Reproductive Health_s (DRH) Bpregnancy-related death[ is similar to the ICD_s Bmaternal deaths[ and DRH_s pregnancy associated death is similar to ICD_s pregnancy related death (Table 1).18 The 2003 revision of the US Standard Certificate of Death introduced a

Homicides of Pregnant Women

standard format designed to use additional codes available in ICDY10 for deaths associated with pregnancy, childbirth, and the puerperium. Most States are expected to introduce or replace the pre-existing format with the standard items, so there will be greater standardization of pregnancy status across the country. As of 2009, approximately 30 states have done this (personal communication, Donna L. Hoyert, Division of Vital Statistics, NCHS, CDC). REFERENCES 1. Chang J, Berg CJ, Saltzman LE, et al. Homicide: a leading cause of injury deaths among pregnant and postpartum women in the United States, 1991Y1999. Am J Public Health. 2005;95:471Y477. 2. World Health Organization. Manual of the International Statistical Classification of Diseases, Injuries, and Causes of Death. Geneva, Switzerland: World Health Organization; 1977. 3. World Health Organization. Manual of the International Statistical Classification of Diseases, Injuries, and Causes of Death. 10th ed. Geneva, Switzerland: World Health Organization; 1993. 4. Lang CT, King JC. Maternal mortality in the United States. Best Pract Res Clin Obstet Gynaecol. 2008;22:517Y531. 5. Shadigian E, Bauer ST. Pregnancy-associated death: a qualitative systematic review of homicide and suicide. Obstet Gynecol Surv. 2005;60:183Y190. 6. Dannenberg AL, Carter DM, Lawson HW, et al. Homicide and other injuries as causes of maternal death in New York City, 1987 through 1991. Am J Obstet Gynecol. 1995;172:1557Y1564. 7. Lewin T. When the death of a fetus is murder. New York Times. May 20, 1994. 8. Hanzlick R. The Medical Cause of Death Manual. Northfield, IL: College of American Pathologists; 1994. 9. Adams VI, Flomenbaum MA, Hirsch CS. Trauma and disease. In: Spitz WU, ed. Spitz and Fisher_s Medicolegal Investigation of Death. 4th ed. Springfield, IL: Charles C Thomas; 2006:436Y459. 10. Krulewitch CJ, Pierre-Louis ML, de Leon-Gomez R, et al. Hidden from view: violent deaths among pregnant women in the District of Columbia, 1988Y1996. J Midwifery Womens Health. 2001;46:4Y10. 11. Rizzi RG, Cordoba RR, Maguna JJ. Maternal mortality due to violence. Int J Gynaecol Obstet. 1998;63(suppl 1):S19YS24. 12. Martin SL, Macy RJ, Sullivan K, et al. Pregnancy-associated violent deaths: the role of intimate partner violence. Trauma Violence Abuse. 2007;8:135Y148. 13. Krulewitch CJ, Roberts DW, Thompson LS. Adolescent pregnancy and homicide: findings from the Maryland office of the Chief Medical Examiner, 1994Y1998. Child Maltreat. 2003;8:122Y128. 14. McFarlane J, Campbell JC, Sharps P, et al. Abuse during pregnancy and femicide: urgent implications for women_s health. Obstet Gynecol. 2002;100:27Y36. 15. Dietz PM, Rochat RW, Thompson BL, et al. Differences in the risk of homicide and other fatal injuries between postpartum women and other women of childbearing age: implications for prevention. Am J Public Health. 1998;88:641Y643. 16. Horon IL, Cheng D. Enhanced surveillance for pregnancy-associated mortalityVMaryland, 1993Y1998. JAMA. 2001;285:1455Y1459. 17. Espinosa L, Osborne K. Domestic violence during pregnancy: implications for practice. J Midwifery Womens Health. 2002;47:305Y317. 18. Hoyert DL. Maternal mortality and related concepts. Vital Health Stat 3. 2007:1Y13.

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CASE REPORT

Three Different Mechanisms of Death An Unusual Form of a Child Murder by Asphyxia Ivan Dieb Miziara, MD, PhD and Flavio Bertaccini, MD

Abstract: We report a very unusual case of murder of a 4-year-old male white child who died of asphyxiation. Asphyxia occurred due to 3 factors: manual strangulation, hyperextension of the neck, and atlantoaxial subluxation. The offenses were carried out by a single assailant (the stepfather of the child) who strangled the child with his right hand, using his left hand to pull the hair of the child, forcing the head back and causing hyperextension of the neck, thereby dislocating the first and second cervical vertebrae. Key Words: manual strangulation, traumatic asphyxia, neck hyperextension, homicide (Am J Forensic Med Pathol 2011;32: 164Y165)

M

anual strangulation is a method of homicide that is primarily used when there is a great difference in physical size and strength between the assailant and the victim,1 such as between an adult man and a child. Death by asphyxiation is a common finding in forensic practice and requires elucidation concerning the manner in which the death occurred. In some cases, the victim dies as a result of a combination of different mechanisms of asphyxia.2 There have been few reports implicating multiple forms of asphyxia in the death of the same individual.3,4 Atlantoaxial subluxation rarely occurs as a consequence of manual strangulation. Here, we report a rare case: the murder of a child involving 3 forms of asphyxia, one of which was atlantoaxial subluxation.

DESCRIPTION OF THE CASE A 4-year-old male white child was found dead in the backyard of his house by his mother. A forensic autopsy was performed 6 hours later on the same day at the Franco da Rocha Medical Examiner’s Office, located in the city of Franco da Rocha, Brazil. At the time of death, the child measured 100 cm and weighed 10.5 kg. The external examination revealed cyanosis of the face, lips, and nails, together with conjunctival petechiae. There were no defense injuries and no signs of sexual violence. On the anterior neck, there were 2 crescent-shaped hematomas measuring 1.5  1 cm (Fig. 1). In addition, there was abnormal, exaggerated mobility of the cervical spine (Fig. 2). In the internal examination, we observed an area of blackish hemorrhagic infiltration, measuring 2.5  2 cm, in the paravertebral muscles (Fig. 3), with disruption of the anterior and posterior longitudinal ligaments, as

Manuscript received April 28, 2008; accepted November 13, 2008. From the Hospital das Clı´nicasYSa˜o Paulo University School of Medicine; and Legal Medicine Institute, Sa˜o Paulo, Brazil. Reprints: Ivan Dieb Miziara, MD, PhD, Hospital das Clı´nicasYSa˜o Paulo University School of Medicine, Teodoro Sampaio, 352-22, Sa˜o Paulo, Brazil 05406000l. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0164 DOI: 10.1097/PAF.0b013e318219c832

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well as of the interspinous ligaments, at C1YC2. In addition, the first and second cervical vertebrae were dislocated, without signs of fracture. There was meningeal and cerebral congestion, together with brain edema, principally in the region of the brainstem. During the dissection of the neck, we observed a blackish hematoma located in the right and left sternothyroideus muscles (Fig. 4). There was also hemorrhaging in the cervical musculature. There was hemorrhagic infiltration underlying the perichondrium of the right superior thyroid horn and 3 small (0.5 cm) submucosal hematomas within the larynx. In the lungs, we observed congestion and subpleural petechiae. Histological examination under microscopy revealed hemorrhagic infiltration of the brainstem and alveolar hyperinflation.

DISCUSSION This case is interesting because it describes a common form of child abuse by parents or caregivers: grabbing a child by the neck. It also describes a quite rare combination of 3 mechanisms of death. The assailant (the stepfather of the boy) squeezed the neck with his right hand, grabbed the hair with his left hand and pulled the head back. These sequential movements were so violent that the articulation between the first and second vertebrae was dislocated, thereby putting pressure on the brainstem. To our knowledge, there are no similar cases in the literature. Lupascu et al4 described a case of a 75-year-old woman killed by asphyxiation involving 3 mechanisms: suffocation, strangulation, and chest compression. In our case, manual strangulation was confirmed based on external evidence (bruises on the cervical skin) and internal evidence (laryngeal and perilaryngeal lesions) consistent with the method. However, we found no fractures of the larynx, which might be explained by the young age of the victim and the consequent elasticity of the laryngeal cartilages.

FIGURE 1. Crescent (fingernail)-shaped bruises on the anterior neck. Am J Forensic Med Pathol

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FIGURE 2. Exaggerated mobility of the cervical spine.

Dislocation of the C1YC2 joint was confirmed through direct examination, and hyperextension of the neck was evidenced by rupture of the ligaments surrounding the C1YC2 joint. In attempting to describe the mechanism involved, it must be borne in mind that the hyoid bone and laryngeal cartilage form an anatomic and functional whole, relatively strongly connected to each other and to the skull base, transmitting force from one structure to another.5 In all tissues, the hemorrhagic infiltrations were of medium intensity, suggesting that they occurred simultaneously. All forms of strangulation put pressure on the air passages, blood vessels, and nervous structures of the neck.5 However, the exact pathophysiological mechanism that leads to death in strangulation is not completely clear, although narrowing of the airway most probably plays a less important role than does obstruction of the blood vessels. Regarding the mechanism of death in the present case, we concluded that the victim died as a result of the combination of different mechanisms of asphyxia.2 The concentration of oxygen in the blood dropped sharply due to the mechanical compression of the neck, which reduced the supply of oxygen. Airflow was impaired by constriction of the laryngeal lumen (by

Three Different Mechanisms of Death

FIGURE 4. Hematoma of the right and left sternothyroideus muscles.

the hematomas and congestion of the mucous membranes). In addition, the extreme hyperextension of the neck might have caused narrowing of the upper airways. Conjunctival petechiae, as was seen in this case, should be considered a strong indicator of uninterrupted venous compression (for at least 10 seconds).5,6 In addition, the dislocation of the C1YC2 joint resulted in brainstem compression. As stated by Pu¨schel et al,7 injuries of the cervical spinal column and brainstem are quite rare in cases of strangulation. In a study of 821 hanging deaths, the authors found fractures of the cervical spinal column in only 6 cases, in which the fractures occurred between the segments C5 and C6. In the present case, the aggressor, the stepfather of the child, was arrested within 24 hours. He confessed to the murder but denied that the killing was intentional. He stated that he simply wanted to ‘‘teach the child a lesson.’’ REFERENCES 1. Knight B. Fatal pressure on the neck. In: Knight B, ed. Forensic Pathology. London, PA: Edward Arnold; 1991:334Y359. 2. Azmak D. Asphyxial deaths. a retrospective study and review of the literature. Am J Forensic Med Pathol. 2006;27:134Y144. 3. Blanco Pampin J, Garcia Varela L. Suicidal choking by a bizarre combination of inhalation to the bronchi and external neck compression. J Leg Med. 2001;3:119Y122. 4. Lupascu C, Lupascu C, Beldiman D. Mechanical asphyxia by three different mechanisms. Leg Med. 2003;5:110Y111. 5. Nikolic S, Micic J, Atanasijevic T, et al. Analysis of neck injuries in hanging. Am J Forensic Med Pathol. 2003;24:179Y182. 6. Plattner T, Bolliger S, Zollinger U. Forensic assessment of survived strangulation. Forensic Sci Int. 2005;153:202Y207.

FIGURE 3. Blackish hemorrhagic infiltration of the paravertebral muscles.

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7. Pu¨schel K, Tu¨rk E, Lach H. Asphyxia-related deaths. Forensic Sci Int. 2004;144:211Y214.

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CASE REPORT

Large Multifocal Cardiac Myxoma Causing the Sudden Unexpected Death of a 2-Month-Old InfantVA Rapidly Growing, Acquired Lesion Versus a Congenital Process? A Case Report Kiyoe Kure, MD, PhD,* Daniel Lingamfelter, DO,* and Eugenio Taboada, MDÞ

Abstract: We report the occurrence of a clinically undiagnosed biatrial myxoma with left ventricular involvement in a 2-month-old male infant, resulting in sudden death. During a routine well-baby examination, a grade 5 holosystolic murmur was detected at the left sternal border with radiation to the axilla and back. On the following day, the patient collapsed and died suddenly. An autopsy revealed a large multifocal neoplasm diffusely involving the aortic valve while displaying mitral, tricuspid, and left ventricular extensions. The ensuing histopathologic and immunohistochemical studies were diagnostic for myxoma. We discuss the occurrence of cardiac myxoma within the pediatric population and review the literature as to theorize whether this lesion was a congenital process versus a rapidly growing tumor that developed after the child was born. Lastly, we address the potential for sudden death in patients with such tumors. Key Words: myxoma, cardiac, heart, tumor, pediatric, murmur, sudden death (Am J Forensic Med Pathol 2011;32: 166Y168)

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yxoma of the heart comprises about half of all primary cardiac neoplasms, usually presenting as a unifocal lesion within the left atrium. Within the pediatric population, this tumor is, by contrary, a rare entity that may go undiagnosed, possibly resulting in death of the child. In this case, we report the occurrence of a clinically undiagnosed biatrial myxoma extending into the left ventricle in a 2-month-old male infant, resulting in sudden death, and discovered for the first time at autopsy.

CASE REPORT The patient was a 2-month-old full-term baby boy born by vaginal delivery to a gravida 3 para 2 mother. His growth was in the 96th percentile for weight and 50th and 25th percentiles for length at 1 and 2 months of age, respectively. His medical history included a right testicle hydrocele and regurgitation after feeding (diagnosed at five days of age) and fine motor skills delay (diagnosed at 2 months of age). On the day before the patient’s death, he received a wellbaby routine visit to his primary care physician to receive the scheduled vaccinations. During the physical examination, a

Manuscript received April 29, 2008; accepted August 14, 2008. From the *University of MissouriYKansas City and Truman Medical Centers; and †Children’s Mercy Hospital, Kansas City, MO. Reprints: Daniel Lingamfelter, DO, Truman Medical Center, Pathology Department, 2301 Holmes St, Kansas City, MO 64108. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0166 DOI: 10.1097/PAF.0b013e318219c84c

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grade 5 holosystolic murmur was detected at the left sternal border with radiation to the axilla and back. He was then scheduled for an appointment with a cardiologist at another hospital. However, on the following day, the patient suddenly collapsed in his mother’s arms. The parents immediately performed cardiopulmonary resuscitation, and he was transported to the hospital. Resuscitative measures were continued without response, and he was pronounced dead. A complete autopsy was performed. The most remarkable findings were seen in the heart. Cardiomegaly was present, with a heart weight of 52 g (normal expected weight, 27 T 7 g), but the heart was normally shaped with dextrorotation. Both the right and left atria were dilated. The left ventricle was also dilated and hypertrophic with a wall thickness of 1.0 cm (normal expected thickness, 0.6 T 0.15 cm). Multiple white, firm neoplastic nodules ranging from 0.3 to 1 cm involving the mitral, tricuspid, and aortic valves were identified. A 1.5  1.4-cm endocardial tumor nodule adherent to the mitral valve protruded into the left atrium; it involved predominantly the anterior and commissural cusps of the mitral valve and fibrous trigones as well as a portion of the left membranous septum (Fig. 1). The circumference of the mitral valves was reduced in size, nearly occluded by the nodular growth. The aortic valve was almost entirely occluded by a nodular tumor focus measuring 2.3  2.0 cm, with a valvular orifice measuring 0.1 cm in diameter (Fig. 2). The septal wall of the left ventricle contained a separate 0.3-cm subendocardial nodule, which was 1.0 cm from the mitral lesion. The tricuspid valve was thickened by an adhering pale, firm papillary-to-nodular endocardial tumoral growth that involved the entire valve and protruded into the right atrium. The pulmonary valve was not involved by any lesions. The foramen ovale was probe patent. The interventricular septum was intact.

MATERIALS AND METHODS The tissue was fixed in formalin, pressed in a routine fashion, then sectioned and stained with hematoxylin and eosin. For immunohistochemistry, formalin-fixed, paraffin-embedded tissue sections were deparaffinized and treated with 3% hydrogen peroxide. Tissue sections were incubated with antibodies to S-100, Ki-67, actin, desmin, vimentin, myo-D1, and myogenin.

RESULTS Microscopically, the cardiac nodules showed proliferations of spindle cells admixed with abundant myxoid material (Fig. 3). Patchy areas of necrosis and hemorrhage were noted. Scattered apoptotic cells were seen, whereas zero mitotic figures were counted after inspection of 10 high-power fields. Systemic tumor emboli were not identified, including examination of the Am J Forensic Med Pathol

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FIGURE 1. Tumor nodules (immediately inferior to each asterisk) bulging into the left atrium and involving the mitral valve (MV) and a focus of the left ventricle (LV). LA indicates left atrium.

FIGURE 3. A cellular area from the neoplasm, composed predominantly of spindle cells admixed with abundant myxoid material. Scattered apoptotic cells are seen. Hematoxylin-eosin stain, original magnification 400.

brain, kidneys, and lungs. The tumor cells were strongly positive for vimentin and S-100 (Fig. 4). An Alcian blue stain highlighted abundant interstitial mucin deposition among the tumor cells. The tumor cells reacted weakly for the smooth muscle marker actin, desmin, and were negative for myo-D1 and myogenin. The proliferation marker Ki-67 showed a proliferative index of 4.1%, calculated from a 1000-cell manual count. An immunohistochemical stain for CD31 highlighted endothelial cells lining normal-appearing vascular spaces but did not highlight the neoplastic cells. A diagnosis of myxoma was thereby reported.

ture. Data from a number of autopsy series report an incidence of approximately 75 per 1 million autopsies.1 The etiology for such sporadic cases is currently not well understood. Typically, cardiac myxoma affects adult females (3:1 female-to-male ratio), with a mean age of 55 years in sporadic cases. Cardiac myxoma usually occurs within the left atrium of the heart (86%),2 whereas biatrial involvement occurs in approximately 2.5% of cases.3 Ventricular involvement is rare in sporadic cases but relatively more common in familial cases. Albeit rare, there have been reported cases with biventricular and atrioventricular involvement.4 Within the pediatric population, cardiac myxoma is exceedingly rare.5 Moreover, only 2 other cases of biatrial myxoma in children have thus far been reported in the literature,6,7 but neither younger than 5 years. To our knowledge, our case represents the first reported occurrence of pediatric biatrial myxoma with left ventricular involvement and the youngest example of biatrial myxoma reported to date. As far as we know, the prenatal care and the newborn visits to the patient’s primary care doctor did not reveal any symptoms or signs suggesting cardiac problems until the last visit,

DISCUSSION We hereby report a rare multifocal cardiac myxoma in a 2-month-old patient involving both atria as well as the left ventricle, a clinically undiagnosed tumor that suddenly and unexpectedly ended this child’s life. Myxoma, a benign entity, accounts for approximately half of all primary cardiac neoplasms and is mostly sporadic in na-

FIGURE 2. Tumor (spanning between the asterisks) involving the entire aortic valve (AV). Punctate areas of hemorrhage are noted within the right central region of the lesion. A indicates aorta; LV, left ventricle.

FIGURE 4. The neoplastic cells stain strongly and diffusely with vimentin. Vimentin stain, original magnification  400.

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the day before the child’s sudden collapse. These previous negative findings might possibly be explained by either a congenital myxoma that was small or a rapidly growing tumor acquired after birth. Some cases definitively show that myxomas can be congenital manifestations, as the youngest reported case of cardiac myxoma was that of a stillborn fetus8 and a 10-hour-old infant with a 2  2  1.8-cm right atrial myxoma.9 To explore the possibility that this lesion was acquired, growth rates of cardiac myxomas within the medical literature were investigated. Such information is given in several studies, but the data are variable. Pochis et al10 described a myxoma with a growth rate of 0.44 cm/mo in a 62-year-old woman, whereas Roudaut et al11 reported a 6  4-cm myxoma that developed in a patient within only 8 months (0.75 cm/mo). Several other studies also published their results. However, these growth rates were obtained mostly by echocardiography, and the studies were performed on adult patients. In our case, a 2-month-old infant with multiple foci of tumor including a 2  2-cm lesion involving the mitral valve shows the most rapid growth rate that has ever been reported (1 cm/mo) if this is, in fact, an acquired tumor. In further support of an acquired neoplasm are the necrosis and hemorrhagic changes found in the tumor, which are very rare findings in cardiac myxoma and may indicate the possibility of a hypoperfusion phenomenon due to rapid tumor growth. On the contrary, strong factors favoring a congenital process with slower growth are (1) the lesion revealed a rather low proliferative index determined by immunohistochemical staining with Ki-67, and (2) no mitoses could be identified out of 10 high-power microscopic fields. As in this case, these tumors have been shown to cause sudden death, as defined by Cina et al12 as nontraumatic death within a short period following the onset of symptoms (usually G6 hours). Sudden death induced by myxomas is due either to tumor embolization with subsequent infarction or mechanical disturbances leading to conductive and hemodynamic aberrations.12 We favor the latter mechanism in this case because of the relatively large size of the neoplastic nodules and because tumor emboli were not identified in any of the tissues, including sections taken from brain, kidney, and lung. As far as the authors are aware, there have been 16 cases in the published literature of cardiac myxomas causing sudden death.12Y15 However, the actual number of occurrences is surely much higher, most notably in the 0- to 34-year-old age group.12 Because of the young age and unusually large, multiple foci of tumor, familial myxoma must be considered. Carney complex is inherited in an autosomal dominant manner. Its diagnosis usually relies on clinical diagnostic criteria and is characterized by skin pigmentary abnormalities, myxomas, schwannomas, and endocrine tumors producing hormonal overactivity disorders. Pale brown-to-black lentigines are the most common presenting feature of Carney complex and typically increase in number at puberty. Cardiac myxomas occur at a young age and may occur in any or all cardiac chambers. Mutations in 2 genes, PRKAR1A and an unknown gene at chromosomal locus 2p16, are causative. In our patient, there was no family history suggesting the above stated syndrome, nor did the patient show any other findings suggesting this inherited disease.

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SUMMARY We encountered a 2-month-old infant with a relatively large multifocal cardiac myxoma that caused the patient’s sudden, unexpected death, most likely through a mechanical disturbance. Although no definitive answer can be given as to whether this lesion was a congenital versus an acquired process, we favor a congenital etiology, a decision based on the likelihood that a multifocal tumor such as this likely did not develop within only 2 months, especially considering the lesion’s low mitotic rate and proliferative index. Furthermore, despite its substantial atrioventricular involvement, this lesion managed to remain clinically silent up until just 1 day before it proved fatal. Cardiac myxoma is extremely rare in the pediatric patient, especially in the 0- to 5-year age group. However, because of the anatomic location of the tumor as well as the possibility for tumor embolization, the potential for sudden death must be cautioned. REFERENCES 1. Reynen K. Frequency of primary tumors of the heart. Am J Cardiol. 1996;77(1):107. 2. Carney JA. Differences between nonfamilial and familial cardiac myxoma. Am J Surg Pathol. 1985;9(1):53Y55. 3. O’Brien-Connors M. Biatrial myxoma: rare incidence in cardiac surgery. Can J Cardiovasc Nurs. 2004;14(3):21Y23. 4. Reynen K. Cardiac myxomas. N Engl J Med. 1995;333(24):1610Y1617. 5. Ergina PL, Kochamba GS, Tchervenkov CI, et al. Atrial myxomas in young children: an alternative surgical approach. Ann Thorac Surg. 1993;56(5):1180Y1183. 6. Cilliers AM, van Unen H, Lala S, et al. Massive biatrial myxomas in a child. Pediatr Cardiol. 1999;20(2):150Y151. 7. Mahilmaran A, Seshadri M, Nayar PG, et al. Familial cardiac myxoma: Carney’s complex. Tex Heart Inst J. 2003;30(1):80Y82. 8. Reddy DJ, Rao TS, Venkaiah KR, et al. Congenital myxoma of the heart. Indian J Pediatr. 1956;23:210Y212. 9. Dianzumba SB, Char G. Large calcified right atrial myxoma in a newborn. Rare cause of neonatal death. Br Heart J. 1982;48(2): 177Y179. 10. Pochis WT, Wingo MW, Cinquegrani MP, et al. Echocardiographic demonstration of rapid growth of a left atrial myxoma. Am Heart J. 1991;122(6):1781Y1784. 11. Roudaut R, Gosse P, Dallocchio M. Rapid growth of a left atrial myxoma shown by echocardiography. Br Heart J. 1987;58(4):413Y416. 12. Cina SJ, Smialek JE, Burke AP, et al. Primary cardiac tumors causing sudden death: a review of the literature. Am J Forensic Med Pathol. 1996;17(4):271Y281. 13. Akyildiz EU, Tolgay E, Oz B, et al. Cardiac myxoma: an unusual cause of sudden death in childhood. Turk J Pediatr. 2006;48(2):172Y174. 14. Vassiliadis N, Vassiliadis K, Karkavelas G. Sudden death due to cardiac myxoma. Med Sci Law. 1997;37(1):76Y78. 15. Parker KM, Embry JH. Sudden death due to tricuspid valve myxoma with massive pulmonary embolism in a 15-month old male. J Forensic Sci. 1997;42(3):524Y526.

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CASE REPORT

Fatal Splenic Rupture Following Heimlich Maneuver Case Report and Literature Review Giovanni Cecchetto, MD,* Guido Viel, MD,* Attilio Cecchetto, MD, PhD,Þ Stefano Kusstatscher, MD,þ and Massimo Montisci, MD, PhD*

Abstract: The most effective resuscitative procedure in choking by foreign bodies is the Heimlich maneuver, described for the first time by Henry Heimlich (1974) and recognized by the US Surgeon General (1985) as the ‘‘only method that should be used for the treatment of choking from foreign body airway obstruction.’’ If performed correctly, this lifesaving maneuver is associated with rare complications, of which the most frequent are rib fractures and gastric or esophagus perforations. Other rare traumatic injuries such as pneumomediastinum, aortic valve cusp rupture, diaphragmatic herniation, jejunum perforation, hepatic rupture, or mesenteric laceration have been described. However, we are unaware of previous reports of splenic rupture after Heimlich maneuver. We present an interesting case of fatal hemoperitoneum due to a hilar laceration of the spleen following a correctly performed Heimlich maneuver. Key Words: spleen, splenic rupture, Heimlich maneuver, choking by foreign body, fatal peritoneal hemorrhage (Am J Forensic Med Pathol 2011;32: 169Y171)

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hoking by foreign body is a well-defined health problem particularly in children and the elderly, representing a lifethreatening emergency condition.1,2 The most effective resuscitative procedure in such cases is the Heimlich maneuver, described for the first time by Henry Heimlich3 in 1974 and recognized by the US Surgeon General (1985) as the ‘‘only method that should be used for the treatment of choking from foreign body airway obstruction.’’4 Correct application of this technique involves the rescuer placing his/her fist between the rib cage and the umbilicus with the thumb or the radial side of the first phalanx in contact with the abdomen. The fist is then grasped with the other hand, and quick thrusts are directed in a 45-degree upward arc.5 As a result of these thrusts, intrathoracic pressure is increased, and the foreign body is expelled. The force should be confined to the rescuer’s hands and adjusted based on the body size of the victim, with more force in an obese person and less force in a small child.6 If performed correctly, this lifesaving maneuver is associated with rare complications, of which the most frequent are rib fractures and gastric or esophagus perforation.6Y9

Manuscript received May 20, 2008; accepted July 19, 2008. From the *Department of Environmental Medicine and Public Health, Legal Medicine, University of Padova, Via Falloppio; †Department of Diagnostic Science and Special Therapies, Pathology Unit, University of Padova, Via Giustiniani, Padova; and ‡Department of Emergency, Hospital of Rovigo, Viale Tre Martiri, Rovigo, Italy. Reprints: Giovanni Cecchetto, MD, Department of Environmental Medicine and Public Health, Legal Medicine, University of Padova, Via Falloppio, 50, 35121 Padova, Italy. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0169 DOI: 10.1097/PAF.0b013e318219c878

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Other rare traumatic injuries such as pneumomediastinum,10 aortic valve cusp rupture,11 diaphragmatic herniation,12 jejunum perforation,13 acute thrombosis of an abdominal aortic aneurysm,14 hepatic rupture,15 or mesenteric laceration16 have been reported. However, we are unaware of previous reports of splenic rupture after Heimlich maneuver; here we present an interesting case of fatal hemoperitoneum due to a hilar laceration of the spleen following a correctly performed Heimlich maneuver.

CASE REPORT A 83-year-old man (height, 181 cm; weight, 92 kg) during lunch, at 2:45 PM, started choking in a steak house 35 km far from Padova (Italy). A male nurse, who was by chance eating in the same restaurant, was immediately called. He realized that the man was responsive but not able to speak because of a complete airway obstruction. Therefore, he performed the Heimlich maneuver 5 times, unfortunately without success. In the meantime, bystanders were involved to call the emergency number ‘‘118’’ asking for medical assistance in place. After 1 minute of abdominal thrusts, the victim became unconscious and collapsed. The male nurse, using the fingersweep technique, dislodged a piece of meat located deeply into the throat, and the patient, although remaining unconscious, recovered a superficial breathing with high respiratory rate. At 3:20 PM, the emergency team arrived; the team leader checked the airways and did not find any obstructions. Pulse was regular (110 beats/min), and blood pressure was 110/70 mm Hg. The victim underwent orotracheal intubation and intravenous crystalloid infusion. During transportation to the Hospital of Padova, the patient became unstable with low blood pressure (60/40 mm Hg; heart rate, 40 beats/min) and consequently epinephrine 1 mg was intravenously injected. At 4:38 PM, he arrived at the emergency room unconscious with pulseless electrical activity. Immediately advanced cardiac life support was performed with continuous cardiopulmonary resuscitation (CPR) and epinephrine infusion (1 mg every 3Y5 min). After 30 minutes of CPR, at 4:58 PM, the patient was pronounced dead. Two days after the death, a forensic autopsy was performed. External examination revealed an orange excoriation (diameter, 5 cm) in the epigastrium without any other traumatic injuries. At autopsy, 2000 mL of fluid blood was recovered from the peritoneal cavity. The spleen (200 g) showed an acute laceration 4 cm in length at the medial surface extending from the hilum to the inferior-medial extremity (Fig. 1A). Hilar vessels were not involved. The brain was swollen; the lungs were overinflated, and the liver was enlarged (2200 g). The gastrointestinal canal presented massive distension. No tears were found in airways, esophagus, stomach, or bowel.

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FIGURE 1. A, Rupture of the spleen caused by Heimlich maneuver. B, Vital tear with hemorrhagic infiltration (hematoxylin-eosin, original magnification 12). C and D, Fibrosis of splenic cords and venous sinuses indicated by # (trichromic, original magnification 50; hematoxylin-eosin, original magnification 50).

Histological investigation of the spleen confirmed the capsular and parenchymal tear. The microarchitecture was characterized by marked red pulp congestion with rare hypotrophic lymphoid follicles and hyaline vasculopathy (Fig. 1, B and C). Trichromic, elastic tissue fibers, and VerhoeffYvan Gieson staining showed a fibrosis of splenic cords and venous sinuses (Fig. 1D). Other relevant histological findings were acute pulmonary emphysema and steatohepatitis. Death was attributed to exsanguination due to traumatic splenic rupture.

DISCUSSION Splenic rupture is generally related to severe blunt abdominal trauma.17 Spontaneous injury or acute laceration following minor trauma represent rare events.17Y19 Several favoring conditions are known such as infectious diseases (malaria, Epstein-Barr virus, HIV, hepatitis), hematologic (idiopathic thrombocytopenic purpura) or neoplastic conditions (leukemia, lymphoma, multiple myeloma), drug assumption (heparin, warfarin, streptokinase), or, more generally, spleen enlargement and fragility.20 In our case, the spleen had a normal volume, but histological investigation revealed an increase of the fibrous component of the sinusoids and a hyaline vasculopathy. These alterations have never been reported among the causes of pathological splenic rupture, but are quite well known favoring conditions for splenic rupture after minor trauma.18,19,21 In our case, police investigations and scene circumstances have excluded a fall, a stroke by another person, or other traumatic events apart from the Heimlich maneuver and the CPR.

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Splenic laceration after CPR has been well documented and described in medical and forensic literature.22,23 In a recent review by Fitchet et al,22 its frequency has been reported being around 0.3%24 and 0.4%.25 Nevertheless, of all the reported injuries, only a handful spleen lacerations resulted in clinically important haemorrhage.22 Because of the fact that the spleen is well protected by the ribcage, splenic injuries caused by chest compressions are generally associated to rib fractures.22,24,25 In our case, forensic autopsy did not reveal bone fractures (sternal or rib fractures), and the abdominal cavity was filled with 2 L of blood. A hilar laceration of the spleen (not involving arterial or venous vessels) without other parenchymal or vascular injuries was found. A peritoneal hemorrhage due to a splenic tear (in the absence of major vessel damage) requires at least 1 hour to reach a volume of 2 L.20,22,23 Because CPR has been performed 30 minutes before death, and because there were no rib fractures, we can exclude with a high degree of probability that the splenic rupture has been a consequence of the CPR. Considering the hilar localization of the tear and its morphology and extension, it seems quite probable that the mechanism of production has been a stretch of the gastrosplenic ligament during the Heimlich maneuver. This lifesaving procedure causes a gastric compression with an increase of the intra-abdominal pressure and an external shift of the infradiaphragmatic organs. If the spleen is macroscopically and histologically normal, the tension on the gastrosplenic ligament generated during the abdominal thrusts is generally not sufficient to produce a laceration of the hilum, and this could be one * 2011 Lippincott Williams & Wilkins

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of the reasons why no previous cases of splenic rupture after Heimlich maneuver have been described. Nevertheless, our brief report could be of interest in forensic practice because, in some particular conditions (eg, fibrocongestive spleen), even the safe and lifesaving Heimlich maneuver should be taken into consideration as a possible cause of splenic rupture with fatal hemorrhage.

13. Razaboni RM, Brathwaite CE, Dwyer WA Jr. Ruptured jejunum following Heimlich maneuver. J Emerg Med. 1986;4:95Y98.

REFERENCES

15. Otero Palleiro MM, Barbagelata LC, Fernandez Pretel MC, et al. Hepatic rupture after Heimlich maneuver. Ann Emerg Med. 2007;49:825Y826.

1. Dolkas L, Stanley C, Smith AM, et al. Deaths associated with choking in San Diego county. J Forensic Sci. 2007;52:176Y179. 2. Berzlanovich AM, Fazeny-Dorner B, Waldhoer T, et al. Foreign body asphyxia: a preventable cause of death in the elderly. Am J Prev Med. 2005;28:65Y69. 3. Heimlich HJ. A life-saving maneuver to prevent food-choking. JAMA. 1975;234:398Y401.

12. Fearing NM, Harrison PB. Complications of the Heimlich maneuver: case report and literature review. J Trauma. 2002;53:978Y979.

14. Kirshner RL, Green RM. Acute thrombosis of abdominal aortic aneurysm subsequent to Heimlich maneuver: a case report. J Vasc Surg. 1985;2:594Y596.

16. Valero V. Mesenteric laceration complicating a Heimlich maneuver. Ann Emerg Med. 1986;15:105Y106. 17. Brady RR, Bandari M, Kerssens JJ, et al. Splenic trauma in Scotland: demographics and outcomes. World J Surg. 2007;31:2111Y2116.

4. Koop CE. The Heimlich maneuver. Public Health Rep. 1985;100:557.

18. Sterlacci W, Heiss S, Augustin F, et al. Splenic rupture, beyond and behind: a histological, morphometric and follow-up study of 254 cases. Pathobiology. 2006;73:280Y287.

5. Heimlich HJ, Patrick EA. The Heimlich maneuver. Best technique for saving any choking victim’s life. Postgrad Med. 1990;87:38Y48.

19. Tataria M, Dicker RA, Melcher M, et al. Spontaneous splenic rupture: the masquerade of minor trauma. J Trauma. 2005;59:1228Y1230.

6. Feeney SN, Pegoli W, Gestring ML. Pancreatic transection as a complication of the Heimlich maneuver: case report and literature review. J Trauma. 2007;62:252Y254.

20. Rosai J. Spleen. In: Rosai J, ed. Ackerman’s Surgical Pathology. 8th ed. St Louis, MO: Mosby; 1996:1775Y1776.

7. Haynes DE, Haynes BE, Yong YV. Esophageal rupture complicating Heimlich maneuver. Am J Emerg Med. 1984;2:507Y509.

21. Peera MA, Lang ES. Delayed diagnosis of splenic rupture following minor trauma: beware of comorbid conditions. CJEM. 2004;6:217Y219.

8. Bintz M, Cogbill TH. Gastric rupture after the Heimlich maneuver. J Trauma. 1996;40:159Y160.

22. Fitchet A, Neal R, Bannister P. Lesson of the week: splenic trauma complicating cardiopulmonary resuscitation. BMJ. 2001;322:480Y481.

9. Wolf DA. Heimlich trauma: a violent maneuver. Am J Forensic Med Pathol. 2001;22:65Y67.

23. Pestaner JP, Smialek JE. Splenic rupture following cardiopulmonary resuscitation. Resuscitation. 2002;54:216.

10. Agia GA, Hurst DJ. Pneumomediastinum following the Heimlich maneuver. JACEP. 1979;8:473Y475.

24. Krischer JP, Fine EG, Davis JH, et al. Complications of cardiac resuscitation. Chest. 1987;92:287Y291.

11. Chapman JH, Menapace FJ, Howell RR. Ruptured aortic valve cusp: a complication of the Heimlich maneuver. Ann Emerg Med. 1983;12:446Y448.

25. Patterson RH, Burns WA, Jannotta FS. Complications of external cardiac resuscitation: a retrospective review and survey of the literature. Med Ann Dist Columbia. 1974;43:389Y394.

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Role of Preoperative 3-Dimensional Computed Tomography Reconstruction in Depressed Skull Fractures Treated With Craniectomy A Case Report of Forensic Interest Guido Viel, MD,* Giovanni Cecchetto, MD,* Renzo Manara, MD,Þ Attilio Cecchetto, MD, PhD,þ and Massimo Montisci, MD, PhD* Abstract: Patients affected by cranial trauma with depressed skull fractures and increased intracranial pressure generally undergo neurosurgical intervention. Because craniotomy and craniectomy remove skull fragments and generate new fracture lines, they complicate forensic examination and sometimes prevent a clear identification of skull fracture etiology. A 3-dimensional reconstruction based on preoperative computed tomography (CT) scans, giving a picture of the injuries before surgical intervention, can help the forensic examiner in identifying skull fracture origin and the means of production. We report the case of a 41-year-old-man presenting at the emergency department with a depressed skull fracture at the vertex and bilateral subdural hemorrhage. The patient underwent 2 neurosurgical interventions (craniotomy and craniectomy) but died after 40 days of hospitalization in an intensive care unit. At autopsy, the absence of various bone fragments did not allow us to establish if the skull had been stricken by a blunt object or had hit the ground with high kinetic energy. To analyze bone injuries before craniectomy, a 3-dimensional CT reconstruction based on preoperative scans was performed. A comparative analysis between autoptic and radiological data allowed us to differentiate surgical from traumatic injuries. Moreover, based on the shape and size of the depressed skull fracture (measured from the CT reformations), we inferred that the man had been stricken by a cylindric blunt object with a diameter of about 3 cm. Key Words: computed tomography, 3D-CT reconstruction, blunt trauma, skull fractures, craniectomy (Am J Forensic Med Pathol 2011;32: 172Y175)

P

atients affected by severe cranial trauma with intracerebral and subdural hemorrhages generally undergo neurosurgical intervention.1Y4 The aim of the intervention is to evacuate hemorrhages; to remove bone fragments, which may eventually penetrate the brain; or more generally to reduce intracranial pressure.5,6 Because craniotomy and craniectomy remove skull fragments and generate new fracture lines, they complicate forensic examination and sometimes prevent a clear identification of skull fracture etiology. A significant portion of patients on whom a craniectomy is performed die after a long period of hospitalization in an Manuscript received May 20, 2008; accepted November 13, 2008. From the *Department of Environmental Medicine and Public Health, Institute of Legal Medicine, University of Padova; †Neuroradiologic Unit, University Hospital of Padova; and ‡Department of Diagnostic Science and Special Therapies, Pathology Unit, University of Padua, Padova, Italy. Reprints: Guido Viel, MD, Department of Environmental Medicine and Public Health, Institute of Legal Medicine, University of Padova, Via Falloppio 50, 35121 Padova, Italy. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0172 DOI: 10.1097/PAF.0b013e318219c88c

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intensive care unit.7,8 During this time, external and internal injuries can partially or completely recover. Consequently, even if present at the moment of hospitalization, scalp abrasions, defensive-type injuries, or brain contusions can be absent at autopsy, so that at postmortem examination only little information is still available. To reconstruct the initial event, radiological data (x-rays, computed tomography [CT], or nuclear magnetic resonance) obtained at hospital admission can be an essential source of morphological evidence.9

MATERIALS AND METHODS We report the case of a 41-year-old-man assaulted by his pusher, who was selling him few grams of cocaine. At the emergency department, he presented a severe cranial trauma with a skull fracture at the vertex, bilateral subdural hematoma, and multiple cortical and intraparenchymal contusions. The rapid impairment of Glasgow Coma Scale score from 14 to 8 forced the surgeons to perform a craniotomy to evacuate the subdural hematoma and to lower intracranial pressure. Despite such intervention, neurological conditions continued to worsen (Glasgow Coma Scale score declined to 4), and after a few hours, an additional craniectomy had to be performed. To visualize the relationship between the bone fragments and the superior sagittal sinus, a spiral CT angiography (CTA) was completed (slice thickness, 3 mm; reconstruction interval, 1 mm; kV 130; mA 182). Craniectomy did not improve neurological and clinical conditions. After 20 days, the patient developed bilateral pneumonia, which subsequently evolved into sepsis, and died 40 days after the initial trauma from multiorgan failure. At forensic external examination (performed 41 days after the trauma), no contusions, lacerations, or abrasions were found apart from a small bruise in the left frontal region of the scalp. At the right temporal and parietal region, a curvilinear scar (24 cm long) related to the neurosurgical procedures was present. Forensic autopsy revealed the following: & a vast traumatic subcutaneous hemorrhage of the scalp involving the right frontal and the right temporoparietal regions; & an absence of the frontal and parietal bones due to the craniectomy; & bilateral linear fractures of the parietal and frontal bones; & 2 fracture lines of the left frontal bone; & a defect due to the craniotomy located in the left frontal bone; and & 2 fracture lines at the base of the skull (anterior and medial fossae) representing an extension into the temporal fossa of the fractures of the vault. After 4 weeks of formalin fixation, the brain was sectioned coronally. Two cortical contusions, one involving the crest of Am J Forensic Med Pathol

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Other histological findings were bilateral bronchopneumonia, lung septal calciosis typical of prolonged times of hospitalization, focal myocardiosclerosis, and chronic inactive viral hepatitis. To analyze the morphology of the fractures and their location, a widely available 3-dimensional (3D) reconstruction (surface shaded display) based on CTA scans was used. A comparative study between autoptic and radiological data was performed.

RESULTS Three-dimensional reconstructions based on preoperative CTA clearly identified the following: & a depressed skull fracture at the vertex (6.0 cm long and 3.2 cm wide) with bone fragmentation (Fig. 2); & 3 fracture lines radiating from the depressed fracture, 2 from the right side along the parietal bone and 1 fracture line from the left side across the frontal bone (Fig. 2, A and B); & 1 fracture line extending along the right temporal bone (Fig. 2A); & 1 fracture line extending along the left frontal bone (Fig. 2B); and & the craniotomy defect (Fig. 2, A and B). The most important radiological finding was the visualization of the depressed fracture at the vertex, no more detectable at autopsy because of the craniectomy. Lacking this evidence, it would have been impossible to identify the etiology of the skull fractures and to properly reconstruct the event. Moreover, the comparative study between necroscopic and radiological data allowed a differentiation between surgical and traumatic lesions.

FIGURE 1. A, Coronal section of the brain after formalin fixation. Two cortical contusions are visible, one involving the crest of the gyri of the left medial superior frontal lobe and one involving the crest of the gyri of the right lateral inferior temporal lobe. B, Histological examination of the frontal contusion. Organized area of hemorrhage and necrosis; severe edema (hematoxylin-eosin, original magnification 25). C, Macrophages containing hemosiderin (black arrows) and reactive gliosis (hematoxylin-eosin, original magnification 100).

the gyri of the left medial superior frontal lobe (4  2 cm) and one involving the crest of the gyri of the right lateral inferior temporal lobe, were found (Fig. 1A). At histology, the contusions consisted of organized areas of hemorrhage and necrosis in a general context of severe edema (Fig. 1B). The presence of erythrophages, macrophages containing hemosiderin, reactive gliosis, and fibrillary astrocytes allowed us to date the cortical contusions at about 30 to 50 days before autopsy (Fig. 1C).

FIGURE 2. Three-dimensional CT reconstructions of the skull based on preoperative CTA scans. A depressed skull fracture at the vertex with bone fragmentation is clearly visible. A, Lateral view. Depressed fracture with 3 fracture lines radiating from the center, 2 from the right side along the parietal bone and 1 fracture line from the left side across the frontal bone. B, Frontal view. Fracture lines and craniotomy defect. C, Size of the depressed area: length, 6.0 cm; width, 3.2 cm; total area of about 18 cm2. D, Back view of the skull.

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FIGURE 3. Comparison between autoptic and radiological data. A, Three-dimensional CT reconstruction of the skull based on preoperative CTA scans. B, Picture of the skull at autopsy. The absence of the 2 sutured fracture lines (black arrows) on the left parietal bone in the preoperative 3D reconstruction (A) let us to establish that they have been produced during the craniectomy.

The absence of the 2 sutured fracture lines on the left parietal bone in the preoperative 3D-reconstruction (Fig. 3) let us to conclude that they have been produced during the craniectomy. The preoperative CT did not identify the transverse fractures at the base of the skull that have certainly been produced by the trauma. This represents a well-known limit of CT that can fail to identify transverse fractures of the anterior fossa or of the temporal bone when performed with slices thicker than 1 mm.10

DISCUSSION The findings collected at autopsy did not permit us to establish whether the skull had been stricken by a blunt object or had hit violently the ground. The absence of bone fragments at the vertex, the presence of new fracture lines produced during craniectomy, and the length of time between the initial trauma and forensic examination, as well as the healing of all external wounds, prevented a clear identification of the etiology of the skull fractures. The availability of a preoperative CTA, performed to define the exact relationship between bone fragments and the sagittal sinus, allowed us to obtain a 3D reconstruction of a depressed fracture at the vertex, to measure its size (length, 6.0 cm; width, 3.2 cm; with a total area of about 18 cm2), and to differentiate the fractures related to the trauma from those produced during the craniectomy. A depressed skull fracture is an important and well-known sign of blunt force trauma by an object with a narrow surface of impact.11Y13 The possibility to visualize and measure this kind of fracture at the vertex enabled us to interpret the 2 brain injuries at the left frontal lobe and at the right temporal lobe as coup and contrecoup contusions. The integration between radiological and autoptic findings indicated that the man, most probably, had been stricken by a blunt object with a small surface of impact. We also attempted to identify the metrical characteristics of the weapon involved and to reconstruct the sequence of events. A lot of factors such as the amount of hair; the thickness of the scalp; the configuration and thickness of the skull; the elasticity of the bone at the point of impact; the shape, weight, and consistency of the object; and the velocity at which

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the blow is delivered affect skull fractures’ extension and morphology.12,13 Thus, only experimental data collected using a skull with the same configuration and thickness of the fractured one, stricken with different blunt objects at variable velocities, could simulate the real blow and allow a precise reconstruction.12Y15 Nevertheless, analyzing the fracture pattern (single depression at the vertex with linear radiations to the left frontal and right parietal bones, fracture extension at the base of the skull), it seems quite probable that all the fractures have been produced by a single blow delivered from right to left at the top of the vault with a great amount of kinetic energy.14Y17 The aggressor probably coming from the right side of the victim stroke the blow with his right hand, producing a combination of linear and angular acceleration. The rotational acceleration could partially explain the presence of a bilateral subdural hemorrhage beside a contrecoup contusion at the temporal lobe.12,17 Because of the fracture pattern and the size of the depressed area, even if several variables cannot be considered, we presume that the weapon involved in the assault was a wood or metal baton with a diameter of about 3 cm. This brief case report underlines the importance of reviewing clinical CT scans when secondary changes such as neurosurgical procedures occur after severe cranial trauma. When preoperative CT slices are thinner than 5 mm (minimal resolution), a 3D reconstruction of the skull may yield precious information regarding the etiology of the fractures (ie, a blow vs a fall) and/or the type of weapon used as well as the dynamics of the event.

REFERENCES 1. Bullock AR, Chesnut R, Ghajar J, et al. Guidelines for the surgical management of traumatic brain injury author group. Neurosurgery. 2006;58:S56YS60. 2. Munch E, Horn P, Schurer L, et al. Management of severe traumatic brain injury by decompressive craniectomy. Neurosurgery. 2000;47:315Y322. 3. Winter CD, Adamides AA, Rosenfeld JV. The role of decompressive craniectomy in the management of traumatic brain injury: a critical review. J Clin Neurosci. 2005;12:619Y623. 4. Soukiasian HJ, Hui T, Avital I, et al. Decompressive craniectomy in trauma patients with severe brain injury. Am Surg. 2002;68: 1066Y1071. 5. Faleiro RM, Pimenta NJG, Faleiro LCM, et al. Decompressive craniotomy for the early treatment of traumatic intracranial hypertension. Arq Neuropsiquiatr. 2005;63:508Y513. 6. Skoglund TS, Eriksson-Ritzen C, Jensen C, et al. Aspects on decompressive craniectomy in patients with traumatic head injuries. J Neurotrauma. 2006;23:1502Y1509. 7. Pompucci A, De Bonis P, Pettorini B, et al. Decompressive craniectomy for traumatic brain injury: patient age and outcome. J Neurotrauma. 2007;24:1182Y1188. 8. Aarabi B, Hesdorffer DC, Ahn ES, et al. Outcome following decompressive craniectomy for malignant swelling due to severe head injury. J Neurosurg. 2006;104:469Y479. 9. Bauer M, Polzin S, Patzelt D. The use of clinical CCT images in the forensic examination of closed head injuries. J Clin Forensic Med. 2004;11:65Y70. 10. Schuknecht B, Graetz K. Radiologic assessment of maxillofacial, mandibular, and skull base trauma. Eur Radiol. 2005;15:560Y568.

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particular reference to engineering factors. Am J Surg. 1949;78: 736Y751.

11. Spitz WU. Blunt force trauma. In: Medicolegal Investigation of Death. Springfield, IL: Charles C. Thomas; 1993:199Y257. 12. DiMaio VJ. Trauma to the skull and brain: craniocerebral injuries. In: Forensic Pathology. 2nd ed. Broca Raton, FL: CRC Press; 2001:147Y183. 13. Knight B. Forensic Pathology. New York, NY: Oxford University Press; 1991. 14. Gurdjian ES, Webster JE, Lissner HR. Studies on skull fracture with

15. Reimann W. Zur Mechanik der Scha¨delbasis-Bru¨che. Dt Zs Ges Ger Med. 1961;51:601Y608. 16. Fisher BA, Svennson A, Wendel O. Techniques of Crime Scene Investigation. New York, NY: Elsevier; 1987. 17. Gurdjian ES. Recent advances in the study of the mechanism of impact injury of the headVa summary. Clin Neurosurg. 1972;19:1Y42.

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CASE REPORT

Primary Breast Lymphoma With Sudden Death Luisa Florez, MD,*Þ Carolina Gutierrez, MD,* Kathy Haden-Pinneri, MD,Þ Mario Cervantes, MD,* Maximilian Buja, MD,þ Mary L. Anzalone, MD,Þ and Luis A. Sanchez, MDÞ

Abstract: Primary breast lymphoma is a rare form of extranodal lymphoma. B cells constitute the most common type involving the breast. T cells represents only 3%. Even though lymphomas have a high predilection to metastasize to the heart, there are no specific clinical or radiological findings, and most of the cases are diagnosed at autopsy. We discuss the case of a 49-year-old woman with primary breast lymphoma who presented with sudden death. Autopsy revealed a primary T-cell lymphoma of the breast with tumoral infiltration of the atrioventricular node and transmural myocardial permeation with focal necrosis. Key Words: sudden death, primary breast lymphoma, arrhythmia, heart (Am J Forensic Med Pathol 2011;32: 176Y179)

CASE REPORT We discuss the case of a 49-year-old Vietnamese woman with a primary breast lymphoma (PBL) metastatic to the heart and adrenal glands that presented with sudden death (Fig. 1). This patient had consulted to a local emergency room 2 weeks before her death because of a 2-day history of painful and swollen right breast. Bilateral breast masses were recognized, and a mammography was ordered. This study was never performed because the patient died before it was scheduled. Interestingly, the review of the medical record revealed a mammography done 6 months prior that was reported as normal. In addition, the clinical notes indicated that the patient had dizziness, palpitations, fever, night sweats, and chills in the last month and loss of appetite with weight loss of 20 lb in the last 6 months. There is no mention of nipple discharge or palpable lymphadenopathy. There was no clinical suspicion of cardiac disease during the emergency department visit or before this evaluation. There was no history of previous malignancies; the only medical history was sinusitis and migraines. She had an adopted child but no children of her own. Family history was positive for tumors of liver, lung, prostate, cervix, and ovary, but no details regarding their type were specified. There was also history of breast carcinoma on both sides of the family, and at least 2 of her sisters had a diagnosis of it, the youngest at age 46 years. On autopsy, 7- and 2-cm masses on the right and left breast, respectively, were identified (Fig. 2C). Two lymph nodes were found on the right neck and supraclavicular region measuring 1 cm each. No enlarged lymph nodes were identified in the mediastinum, retroperitoneum, axillas, or inguinal regions. Both adrenal glands were soft, enlarged, and grossly replaced by tumor in their entirety (Fig. 2, A and B). The heart showed Manuscript received June 13, 2008; accepted July 19, 2008. From the *Department of Pathology, Baylor College of Medicine; †Harris County Medical Examiner’s Office; and ‡University of Texas Health Sciences Center, Houston, TX. Reprints: Luisa Florez, MD, 1885 Old Spanish Trail, Houston, TX 77054. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0176 DOI: 10.1097/PAF.0b013e318219c8a2

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multiple, gray-white, soft masses ranging from 0.6 up to 3.5 cm involving the posterolateral wall of the left ventricle and the interventricular septum (Fig. 3A). The atrioventricular node appeared slightly thickened. There was no effusion, pericardial thickening or nodules, or any macroscopic evidence of recent or remote myocardial infarction. The coronary arteries showed no atherosclerosis or stenosis. There was no evidence of pulmonary embolism. There was a single, 4-mm, soft, white nodule in the inferior lobe of the right lung. Liver, spleen, kidneys, and brain had normal weights and revealed no abnormalities. The genital and gastrointestinal systems showed no focal lesions. Microscopic examination revealed a monomorphic population of predominantly large, atypical cells with coarse chromatin and abundant apoptosis comprising both breasts in a diffuse fashion (Fig. 4A). There was entire replacement of both adrenal glands with large areas of necrosis. The heart showed several transmural, diffusely infiltrative tumoral foci with focal necrosis and contained involvement of the atrioventricular node (Fig. 3B). The lung revealed a focal tumoral nodule. There was no involvement of any of the lymph nodes or any other organ. There is no information on peripheral blood smears or bone marrow biopsy. Immunostains were performed to corroborate the suspicion of lymphoma (Fig. 3). CD45 was positive, whereas pancytokeratin was negative, which indicated a lymphoid origin and excluded a carcinoma. CD20 was negative, excluding a B-cell origin. CD3, a specific marker for T-cell derivation, was positive, and CD7, which is usually lost in T-cell lymphomas, was negative. These markers established a T-cell lineage (Fig. 4, BYF).

FIGURE 1. Decedent as found at the scene. Am J Forensic Med Pathol

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FIGURE 2. A, Both adrenal glands completely replaced by tumor nodules. B, Right mammary gland mass measuring 7 cm in diameter.

CD57, which marks NK cells, and ALK1, which stains anaplastic large-cell lymphomas, were completely negative, excluding these 2 subtypes. CD30 was positive in a few cells. CD4 and CD8 were positive in about 10% of the tumoral cells. Epstein-Barr virus was positive.

DISCUSSION Non-Hodgkin PBLs are rare and account for 0.04% to 1.0% of all breast malignancies.1Y5 They represent 1.7% to 2.2% of all extranodal lymphomas.1,3,4,6,7 We consider this case to represent a PBL as there was no nodal involvement denoting that there was no infiltration of lymph nodes, thymus, spleen, or Waldeyer ring; there was no previous diagnosis of lymphoma; and the bulk of the tumor was localized in the breast. Wiseman and Liao8 proposed 4 criteria for PBL that we as well as other authors consider limiting,9,10 as they exclude patients with distant metastases at the time of diagnosis even if the major site of involvement is the breast.5,7,11 According to the Ann Arbor classification of lymphomas, this case corresponds to stage IV.12 We also believe the route of dissemination was hematogenous as there were no pulmonary hilar or mediastinal lymph nodes or masses. Furthermore, the hematogenous spread is characterized by intramyocardial involvement with epicardial infiltration and diffuse myocardial permeation in 66% of cases.13,14 On the other hand, metastatic tumors tend to present with pericardial thickening or nodules as they spread through the subepicardial lymphatics.1,15

The median age at presentation is 50 years (range, 22Y76 years), and more than 95% of the cases affect females.2,7,11,16,17 The vast majority of PBLs are B-cell lymphomas, being the diffuse large cell the most common subtype.2,3,6,7,11,17Y21 T-cell lymphomas of the breast represent only 3% of all PBLs.3,4,11 Primary breast lymphoma tends to be more aggressive and has a poorer prognosis than primary breast carcinoma,22 particularly T-cell lymphoma, of which more than 80% are high grade.2,23 Primary breast lymphomas may be bilateral at the time of presentation in 5% to 25% of cases with or without unilateral or bilateral axillary involvement.11,16 The clinical presentation is indistinguishable from carcinoma,4,16,20 except that they tend to present with a larger mass (4.6 cm in average), the onset is recent (mean duration of symptoms of 2 months), and the growth is rapid.2,7,16,17,19,20 There are no specific mammographic changes,2,17,24 which seem not to play a role in anticipating the diagnosis of PBL. Remarkably, in several reported cases as well as in this patient, mammography performed a few months previously did not reveal any abnormality.4 The heart showed 2 intramyocardial tumoral foci and no pericardial infiltration or effusion. Metastatic cardiac tumors are more frequent than primary, 8.7% to 20%1,15,25Y36 versus less than 0.1% to 1.3%.13,23,32,37Y40 Lymphoma has a high predilection to disseminate to the heart with an incidence of 25%,13,38 comprising the second most common malignancy after lung carcinoma.25,41 Most cases are clinically silent and go undetected until discovered by autopsy.23,28,29,34,36Y39,41

FIGURE 3. A, Multiple tumor nodules involving the heart. B, Atypical cells infiltrating the atrioventricular node. * 2011 Lippincott Williams & Wilkins

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FIGURE 4. A, Hematoxylin-eosinYstained section demonstrating massive breast replacement by atypical lymphoid cells. BYF, Immunohistochemistry panel showing strong and diffuse positivity by CD23 (B), CD45 (C), and CD30 (D) and few stained cells with CD8 (E) and scarce tumor cells highlighted by CD4 (F).

These are cases of patients who can present with sudden death or who apparently died of other causes. Cardiac dysfunction caused by secondary lymphoma is rarely the presenting symptom. A wide variety of symptoms have been reported including dyspnea, palpitations, chest pain, superior vena cava syndrome, heart failure, myocardial ischemia, valvular disease, outflow obstruction, pericardial effusion with tamponade, arrhythmia, heart block, syncope, sick sinus syndrome, and sudden death.28,29,31,33,34,38,39,41Y46 All these manifestations are unspecific and insufficient to raise suspicion of cardiac involvement by lymphoma.35,44 Sinus tachycardias, low voltage, and STsegment and T-wave changes, although nonspecific, can be found in 66%.30,34,38 Atrial arrhythmias can be caused by infiltration of the atria, sinus node, or autonomic fibers. Specific infiltration of the conducting system can produce complete atrioventricular block with sudden death, as we consider that this case exemplifies.15,36Y39,43,44,47Y49 Other contributing mechanisms are invasion of the coronary arteries or diffuse myocardial tumoral infiltration with subsequent infarction, which can generate arrhythmias.33,40,46,50 No laboratory tests or electrocardiographic or echocardiographic tests were performed during the emergency room visit because there was no clinical consideration of cardiac dysfunction. Even though extranodal lymphomas seem to be frequent in immunocompromised patients,23,27,31,32,34,35,39,46 there was never a manifestation of immunosuppressive disorders in this patient; neither was she the receptor of a transplant, nor was she taking any immunosuppressive drugs. Primary Breast Lymphoma has also been reported in association with Sjo¨gren and Hashimoto thyroiditis.4 Although carcinomas represent the vast majority of malignancies comprising the breast, lymphoma constitutes a major potential pitfall and should be considered in the differential diagnosis,6 particularly if there is a large, rapid-growing mass with bilateral axillary nodes.2 Even histologically, lymphoma can mimic lobular carcinoma or poorly differentiated carcinoma.21

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This case demonstrates once again the utility of examining the cardiac conduction system in necroscopy studies of sudden death. We recommend as a routine practice taking a section of the conducting system including the atrioventricular node in all cases of sudden death.18 REFERENCES 1. Baker R, Slayden G, Jennings W. Multifocal primary breast lymphoma. South Med J. 2005;98:1045Y1048. 2. Sabate JM, Gomez A, Torrubia S, et al. Lymphoma of the breast: clinical and radiologic features with pathologic review correlation in 28 patients. Breast J. 2002;8:294Y304. 3. Uesato M, Miyazawa Y, Gunji Y, et al. Primary non-Hodgkin’s lymphoma of the breast: report of a case with special reference to 380 cases in the Japanese literature. Breast Cancer. 2005; 12:154Y158. 4. Vigliotti ML, Dell’Olio M, La Sala A, et al. Primary breast lymphoma: outcome of 7 patients and a review of the literature. Leuk Lymphoma. 2005;46:1321Y1327. 5. Zinzani PL, Alinari L, Stefoni V, et al. Bilateral breast lymphoma: a case of local recurrence. Leuk Lymphoma. 2003;44:737Y738. 6. Ewing CA, Miller MJ, Chhieng D, et al. Nonepithelial malignancies mimicking primary breast carcinoma of the breast. Diagn Cytopathol. 2004;31:352Y357. 7. Park YH, Kim SH, Choi SJ, et al. Primary malignant lymphoma of the breast: clinicopathological study of nine cases. Leuk Lymphoma. 2004;45:327Y330. 8. Wiseman C, Liao KT. Primary lymphoma of the breast. Cancer. 1972;29:1705Y1712. 9. Krol ADG, Le Cessie S, Snijder S, et al. Primary extranodal non-Hodgkin’s lymphoma (NHL): the impact of alternative definitions tested in the Comprehensive Cancer Centre West population-based NHL registry. Ann Oncol. 2003;14:131Y139.

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10. Vignot S, Ledoussal V, Nodiot P, et al. Non-Hodgkin’s lymphoma of the breast: a report of 19 cases and a review of the literature. Clin Lymphoma. 2005;6:37Y42.

31. Ikeda H, Nakamura S, Nishimaki H, et al. Primary lymphoma of the heart: case report and literature review. Pathol Int. 2004;54: 187Y195.

11. Gholam D, Bibeau F, El Weshi A, et al. Primary breast lymphoma. Leuk Lymphoma. 2003;44:1173Y1178.

32. Hayes D, Liles DK, Sorrell VL. An unusual cause of new-onset atrial flutter: primary cardiac lymphoma. South Med J. 2003;96:799Y802.

12. Stein H. Hodgkin lymphomas. In: Jaffe ES, Harris NL, Stein H, et al, eds. Pathology and Genetics of Tumours of Hematopoietic and Lymphoid Tissues. Lyon, France: IARC press; 2001:239. 13. Lam KY, Dickens P, Chan ACL. Tumors of the heart. Arch Pathol Lab Med. 1993;117:1027Y1031. 14. Rolla G, Bertero MT, Pastena G, et al. Primary lymphoma of the heart. A case report and review of the literature. Leuk Res. 2002;26:117Y120. 15. Rolla G, Calligaris-Cappio F. Metastatic tumours of the heart. In: Travis WD, Brambilla E, Muller-Hermelink K, et al, eds. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. Lyon, France: IARC press; 2004:282Y283. 16. Maounis N, Ellina E, Papadaki TH, et al. Bilateral primary lymphoma of the breast: a case report initially diagnosed by FNA. Diagn Cytopathol. 2005;32:114Y118. 17. Pruthi S, Stafyla VK, Phillips SW, et al. Primary mammary (non-Hodgkin) lymphoma presenting as locally advanced breast cancer. Mayo Clin Proc. 2004;79:1310Y1314. 18. Cina S, Smialek J, Burke A, et al. Primary cardiac tumors causing sudden death: a review of the literature. Am J Forensic Med Pathol. 1996;17:271Y281. 19. Fruchart C, Denoux Y, Chasle J, et al. High grade primary breast lymphoma: is it a different clinical entity? Breast Cancer Res Treat. 2005;93:191Y198. 20. Pinheiro RF, Colleoni GWB, Baiocchi OCG, et al. Primary breast lymphoma: an uncommon but curable disease. Leuk Lymphoma. 2003;44:146Y151. 21. Vardar E, Ozkok G, Cetinel M, et al. Primary breast lymphoma cytologic diagnosis. Arch Pathol Lab Med. 2005;129:694Y696. 22. Ogawa T, Mizutani M, Yabana T, et al. A case of Burkitt’s lymphoma involving both breasts. Breast Cancer. 2005;12:234Y237. 23. Giunta R, Cravero RG, Granata G, et al. Primary cardiac T-cell lymphoma. Ann Hematol. 2004;83:450Y454. 24. Mason HS, Johari V, March DE, et al. Primary breast lymphoma: radiologic and pathologic findings. Breast J. 2005;11:495Y496. 25. Abraham KP, Reddy V, Gattuso P. Neoplasms metastatic to the heart: review of 3314 consecutive autopsies. Am J Cardiovasc Pathol. 1990;3:195Y198. 26. Ancalmo N, King T, Mills NL, et al. Lymphoma with large intracavitary metastasis to the heart. J Cardiovasc Surg. 1976;17: 136Y139. 27. Cairns P, Butany J, Fulop J, et al. Cardiac presentation of non-Hodgkin’s lymphoma. Arch Pathol Lab Med. 1987;111:80Y83. 28. Chinen K, Izumo T. Cardiac involvement by malignant lymphoma: a clinicopathologic study of 25 autopsy cases based on WHO classification. Ann Hematol. 2005;84:498Y505. 29. Clifford SM, Guerra SM, Mangion JR. Massive metastatic intracardiac lymphoma presenting with complete heart block with resolution following chemotherapy. Echocardiography. 2003;20: 201Y202. 30. Fujisaki J, Tanaka T, Kato J, et al. Primary cardiac lymphoma presenting clinically as restrictive cardiomyopathy. Circ J. 2005;69:249Y252.

33. McDonnell PJ, Mann RB, Bulkley BH. Involvement of the heart by malignant lymphoma: a clinicopathologic study. Cancer. 1981;49:944Y951. 34. Miyashita T, Miyazawa I, Kawaguchi T, et al. A case of primary cardiac B-cell lymphoma associated with ventricular tachycardia, successfully treated with systemic chemotherapy and radiotherapy. Jpn J Oncol. 2000;64:135Y138. 35. Murphy PT, Sivakumaran M, Coleby P. Primary cardiac lymphoma: death from cardiac asystole after attaining second complete remission. Clin Lab Haem. 1998;20:57Y59. 36. Ottaviani G, Matturri L, Rossi L, et al. Sudden death due to lymphomatous infiltration of the cardiac conduction system. Cardiovasc Pathol. 2003;12:77Y81. 37. Tai CJ, Wang WS, Chung MT, et al. Complete atrio-ventricular block as a major clinical presentation of the primary cardiac lymphoma: a case report. Jpn J Clin Oncol. 2001;31:217Y220. 38. Aleksic I, Herse B, Busch TH, et al. Third degree atrio-ventricular block caused by malignant non-Hodgkin’s lymphoma: an unusual indication for epicardial pacing. Cardiovasc Surg. 1999;3:378Y380. 39. Nagano M, Uike N, Suzumiya J, et al. Successful treatment of a patient with cardiac lymphoma who presented with a complete atrioventricular block. Am J Hematol. 1998;59:171Y174. 40. Thompson MA, Harker-Murray A, Locketz AJ, et al. Unusual lymphoma manifestations: case 2. Myocardial lymphoma presenting as atrial flutter. J Clin Oncol. 2004;22:558Y560. 41. Butany J, Leong SW, Carmichael K, et al. A 30-year analysis of cardiac neoplasms at autopsy. Can J Cardiol. 2005;21(8):675Y680. 42. Araki T, Namura M. Right atrial tumor and sick sinus syndrome. Intern Med. 2003;42:450Y451. 43. Engelen MA, Bruch C, Buerger H, et al. Pericarditis constrictiva and high-degree atrioventricular block as a first manifestation of a cardiac B-cell lymphoma. J Am Soc Echocardiogr. 2005;18(6):694. 44. Kamimura M, Tanabe N, Hojo M, et al. Malignant lymphoma demonstrating sick sinus syndrome. Intern Med. 1998;37:463Y466. 45. Lopez FF, Mangi AA, Strenger R, et al. B-cell bradycardia: carotid sinus massage by a high-grade lymphoma. Am J Hematol. 2000;64:232Y234. 46. Rolla G, Calligaris-Cappio F, Burke AP. Cardiac lymphomas. In: Travis WD, Brambilla E, Muller-Hermelink K, et al, eds. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. Lyon, France: IARC press; 2004:282Y283. 47. Engelen MA, Juergens KU, Breithardt G, et al. Interatrial conduction delay and atrioventricular block due to primary cardiac lymphoma. J Cardiovasc Electrophysiol. 2005;16(8):926. 48. Roh LS, Paparo GP. Primary malignant lymphoma of the heart in sudden unexpected death. J Forensic Sci. 1982;27:718Y722. 49. Takenaka S, Mitsudo K, Inoue K, et al. Successful treatment of primary cardiac lymphoma with atrioventricular nodal block. Int Heart J. 2005;46:925Y931. 50. Werner D, Schmeisser A, Werner GD. Primary cardiac lymphoblastic T-cell lymphoma. Heart. 2001;86:618.

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CASE REPORT

Discrimination Between Human and Animal DNA Application of a Duplex Polymerase Chain Reaction to Forensic Identification Pamela Tozzo, MD,* Elena Ponzano, PhD,* Enrico Novelli, MVD,þ Maurizio Onisto, PhD,Þ and Luciana Caenazzo, PhD*

Abstract: Identification of a report’s species is one of the basic analyses in forensic laboratories. The authors report the case of 6 bone fragments recovered in a wooded area, which were not attributable to 1 animal species on the basis of morphologic examination. The aim of this study was to develop a duplex polymerase chain reaction (PCR) to discriminate human and animal origin of bone fragments. The method is based on the PCR amplification of cytochrome b and a 16S ribosomal mitochondrial DNA fragment, which has never been tested up to now. Our protocol combines a single-round PCR with direct visualization of amplicons in agarose gel, without sequencing analysis of the PCR products. The presence of a single band (359 bp) indicates a nonhuman origin of the sample, whereas 2 bands (157 and 359 bp) indicate a human biologic sample. This method revealed to be useful for forensic purposes because the 16S ribosomal mitochondrial DNA is a small human-specific fragment that is easily amplifiable even with degraded DNA from biologic materials such as old bones. Key Words: cytochrome b, 16S rRNA, DNA extraction, bone fragments, species identification (Am J Forensic Med Pathol 2011;32: 180Y182)

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pecies determination of skeletal specimens is an important component of forensic and anthropological analyses. The problem is often referred to the differentiation of human bone material from nonhuman one. In most such cases, diagnosis based on anatomic features is possible. However, when remains are fragmentary or poorly preserved, species identification can be difficult or unachievable. For the last few years, the analysis of mitochondrial markers has shown a good feasibility for species determination and individual human identification.1,2 The mitochondrial genome is made up of a small, circular, double-stranded DNA molecule that is present in up to several thousand copies per cell. In animals, the mitochondrial genome is approximately 16,500 bp long and possesses 13 genes coding for proteins, 2 genes coding for ribosomal RNA (rRNA), 22 genes coding for transfer RNA, and 1 major noncoding region named d-loop, which contains the origin of replication.3

Manuscript received August 21, 2008; accepted December 12, 2008. From the *Department of Environmental Medicine and Public Health, Legal Medicine Section, University of Padua; †Department of Experimental Biomedical Sciences, University of Padua, Padova; and ‡Department of Public Health, Comparative Pathology and Veterinary Hygiene, University of Padua, Legnaro, Italy. Reprints: Luciana Caenazzo, PhD, Department of Environmental Medicine and Public Health, Legal Medicine Section, University of Padova, Via Falloppio 50, 35121 Padova, Italy. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0180 DOI: 10.1097/PAF.0b013e31820c2bba

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The analysis of cytochrome b (cyt b) is a well-established method for animal species identification.4Y6 Other methods have been proposed for forensic purposes to distinguish human from nonhuman specimens, involving the amplification of different regions of mitochondrial DNA (mtDNA) in 1 round of polymerase chain reaction (PCR).7,8 Among mtDNA genes used for species detection, the cyt b (alone or associated with other markers) has been successfully used in PCR-based method, even if sequence analysis and comparison in BLAST have made this analysis troublesome.4Y8 Another mtDNA marker commonly used for phylogenetic studies is the 16S rRNA gene.9 In a recent case, it was necessary for our laboratory to attempt species identification of 5 small bone fragments (Fig. 1). These tiny fragments were recovered slightly buried by a hunter in a hilly wooded zone in North Italy. The primary concern was whether they were of human origin. The small size of the pieces precluded positive recognition of human versus nonhuman origin based on their morphology and cortical thickness. For the purpose of establishing the species origin of these fragments, we have developed a method based on a duplex PCR products amplified from mtDNA detected in agarose gel electrophoresis. These amplicons correspond to cyt b (359 bp) and to a 16S rRNA (157 bp) fragment that is human specific and which has never been used for this purpose so far. Because 16S rRNA is a small mtDNA fragment that amplifies easily, this method could be very useful for forensic purposes in case of human species identification.

MATERIALS AND METHODS The first step to determine the 16S rRNA primer specificity for human species was to check for minimum primer-dimer and hairpin secondary structures. Then we verified by BLAST analysis the primer sequences and subsequently tested them by PCR amplification. DNA was extracted from the bone of each of the 5 fragments and from bone belonging to human and other species (cattle, sheep, horse, pig, chicken, rabbit, and cat). The 5 fragments of unknown species were treated for 30 minutes with bleach. Each fragment weighed between 1 and 2 g and was pulverized to a fine powder after immersion in liquid nitrogen. Then, it was decalcified and DNA extracted according to the methods of Crainic et al.10 We designed primers for 16S rRNA, considering of prime importance the melting and annealing working temperatures of the already existing cyt b primers.11 The sequences of primers used in a single PCR are reported in Table 1. After an initial denaturation step of 1 minute at 94-C, samples were amplified in a thermocycler (9700; Applied Biosystems, Foster City, Calif), for 40 cycles of 5 seconds at 94-C, 30 seconds at 50-C, and 40 seconds at 72-C, followed by a final elongation step of 3 minutes at 72-C. The PCR mix was as follows: 0.4 KM each of cyt b primers, 0.6 KM each of 16S Am J Forensic Med Pathol

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Discrimination Between Human and Animal DNA

FIGURE 1. Five bone fragments recovery in the wooded zone.

rRNA primers, 1.25 U of Taq DNA polymerase (Applied Biosystems), 0.2 KM each dNTPs, 2.5 KL of 10 Taq buffer, and 5 to 10 ng of DNA in a final volume of 25 KL. Water instead of DNA was used as a negative PCR control. To verify the efficiency of the PCR amplification, 10 ng of human DNA obtained from whole blood was used as a positive control. Control DNA was stored in TrisEthylenediaminetetraacetic acid buffer at j20-C at a final concentration of 100 ng/KL for up to a year. Electrophoresis of 10 KL of PCR was performed in 2.0 % agarose gel in 1 Tris-borate-Ethylenediaminetetraacetic acid buffer with 1 mg/mL of ethidium bromide to directly visualize amplicons under ultraviolet. Furthermore, we performed automated DNA sequencing of the different animal amplicons using BigDye Terminator v1.1 Cycle Sequencing Kit (Applied Biosystems). Sequencing products were analyzed on ABI PRISM 310 Genetic Analyzer (Applied Biosystems).

RESULTS We analyzed 5 bone fragments (Fig. 1) with the aim to establish if they were of human origin. DNA was extracted from a bone fragment of human origin as control, from samples belonging to different animals, and then from the 5 fragments of unknown origin. The DNAs obtained were amplified in a duplex PCR of cyt b (359 bp) and a 16S rRNA (157 bp) mtDNA fragments. Multiplex amplification showed a band of 359 bp for the cyt b and a second band of 157 bp for the 16S rRNA fragment for human biologic samples. Under the same conditions, only the cyt b fragment was evidenced for samples of animals, whereas the 16S rRNA fragment was completely absent (Fig. 2). The 5 fragments of unknown species show all the 2 bands showing a human origin. Primer concentrations and number of

PCR cycles were optimized to avoid preferential amplification; hence, under the reported condition, we did not see marked differences in the intensity of the 2 bands with the 5 bone samples of unknown origin that we have tested (Fig. 3).

DISCUSSION In situations where small fragments of bone are found, it may be impossible by morphologic features alone to confirm or exclude the human origin, and histologic or molecular methods have to be used. Here, we report the case of 5 bone fragments retrieved, whose origins were undetectable. With the aim of distinguishing human from nonhuman bone fragments, we proposed a method involving the amplification of the cyt b region and the never-used 16S rRNA human-specific fragment, without sequencing analysis of the PCR products. The goal of detecting the human origin of the sample can be easily achieved by direct visualization on agarose gel of 2 bands for human biologic samples or only 1 band for all other animal species. The presence of the cyt b band is a demonstration of the animal origin of the specimen, whereas the second band is specific only for the human. No faint or unspecific bands appear in the animal samples tested: cattle, sheep, horse, pig, chicken, rabbit, and cat. This aspect is particularly important because another study reported the presence of faint nonspecific bands

TABLE 1. Oligonucleotide Sequences for PCR Gene

Primer Sequence

cyt.b forward 5¶-CCATCCAACATCTCAGCATGATGAAA-3¶ cyt.b reverse 5¶-GCCCCTCAGAATGATATTTGTCCTCA-3¶9 16S rRNA forward 5¶-CAATTGGACCAATCTATCACC-3¶ 16S rRNA reverse 5¶-GTGAGGGTAATAATGACTTGT-3¶

FIGURE 2. mtDNA amplification of cyt b (359 bp) and 16S rRNA (157 bp) fragments from different animals. Lane 1 indicates cattle; lane 2, sheep; lane 3, horse; lane 4, pig; lane 5, chicken; lane 6, rabbit; lane 7, cat; lane 8, human; M, 100-bp molecular weight marker.

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with a single-round PCR. Because recovery of information from degraded samples is often enhanced by the use of smaller PCR products, we believe that the analysis of the new small 16S rRNA fragment could represent an improvement over the multiplex PCR methods proposed in literature so far. REFERENCES 1. Kocher TD, Thomas WK, Meyer A, et al. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A. 1989;86:6196Y6200. 2. Wolf C, Rentsch J, Hu¨bner P. PCR-RFLP analysis of mitochondrial DNA: a reliable method for species identification. J Agric Food Chem. 1999;47:1350Y1355.

FIGURE 3. mtDNA amplification of cyt b (359 bp) and 16S rRNA (157 bp) of the 5 bone fragments of unknown origin analyzed from lane 1 to 5. Lane 6 indicates human positive control; lane 7, negative control; lane 8, 100-bp molecular weight marker.

in animal samples using other mtDNA fragments for human identification.7 Moreover, to verify the occurred PCR, we suggest the routine use of positive human control DNA to discriminate negative results for the 16S rRNA band. In this case, the lack of 16S rRNA amplicon will be surely due to the presence of biologic material from animals rather than to an error in the experimental conditions. However, special attention must be paid to avoid contamination by carryover of other samples. In our experiment, we did not find differences in the intensity of the 2 bands, which could allow us to identify the sample of human origin. In the case report, all 5 bone fragments result as being of human origin: all 5 DNA samples obtained and amplified show the same pattern of the human bone sample used as a positive control. This assay demonstrates as being useful for identifying nonhuman species by means a simple comparative analysis in BLAST of the cyt b DNA sequence. On the basis of the results obtained in the case reported, we consider the method proposed as straightforward and reliable, which permits the discrimination of human and animal DNA

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3. Boore JL. Animal mitochondrial genomes. Nucleic Acids Res. 1999;27:1767Y1780. 4. Barallon R. Species determination by analysis of the cytochrome b gene. In: Lincoln PJ, Thomson J, eds. Forensic DNA Profiling Protocols. Totowa, NJ: Humana Press; 1998:251Y260. 5. Branicki W, Kupiec T, Pawlowski R. Validation of cytochrome b sequence analysis as a method of species identification. J Forensic Sci. 2003;48:83Y87. 6. Parson W, Pegoraro K, Niederstatter H, et al. Species identification by means of the cytochrome b gene. Int J Legal Med. 2000;114:23Y28. 7. Bataille M, Crainic K, Leterreux M, et al. Multiplex amplification of mitochondrial DNA for human and species identification in forensic evaluation. Forensic Sci Int. 1999;99:165Y170. 8. Bellis C, Ashton KJ, Freney L, et al. A molecular genetic approach for forensic animal species identification. Forensic Sci Int. 2003; 134:99Y108. 9. Noda R, Kim CG, Takenaka O, et al. Mitochondrial 16S rRNA sequence diversity of hominoids. J Hered. 2001;92:490Y6. 10. Crainic K, Paraire F, Leterreux M, et al. Skeletal remains presumed submerged in water for three years identified using PCR-STR analysis. J Forensic Sci. 2002;47:1025Y1027. 11. Meyer R, Ho¨felein C, Lu¨thy J, et al. Polymerase chain reactionYrestriction fragment length polymorphism analysis; a simple method for species identification in food. J AOAC Int. 1995;78:1542Y1551.

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CASE REPORT

Death Secondary to a Donkey’s Bites Ernesto d’Aloja, MD, PhD,* Leonardo Grimaldi, MD, PhD,Þ Fidelia Cascini, MD, PhD,Þ Domenico De Mercurio, MD,Þ and Fabio De-Giorgio, MD, PhDÞ

Abstract: We present a unique case of death due to the assault and bites of a donkey on a 65-year-old man. The farmer, found dead in his farmyard, had a very deep wound in the anterior region of the neck, with a sharp transection of the trachea and severe bleeding by several minor vessels wall disruptions. The cause of death was established to be massive bleeding combined with asphyxia due to aspiration of the blood. Moreover, multiple contusions with associated skin abrasions and perforations were present. The general impression of the injuries was consistent with an animal’s bite marks. Herbivorous or omnivorous bite attacks on humans are rare; instead, these animals attack by kicking, trampling, and kneeling, resulting in secondary blunt injuries. The donkey is usually a docile animal, but its behavior can be aggressive during the mating season, and the possibility of biting should not be underestimated, as illustrated by the 2 cases published previously as well as by the case presented here. Key Words: forensic science, donkey bite, animal attack, bite mark, fatal donkey mauling, forensic autopsy (Am J Forensic Med Pathol 2011;32: 183Y185)

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uman injuries due to animal bites can be considered relatively common. The animals most frequently associated with these assaults are dogs and big cats.1Y18 Fatalities related to animal bites, however, are relatively rare. According to reports from the United States, approximately 1 million to 4.7 million persons sustain dog bites annually,1Y3 whereas 157 and 109 of these events were fatal in 1979Y1988 and in 1989Y1994, respectively.4,5 Carnivorous animals are involved in the great majority of attacks on humans, whereas herbivores or omnivores seldom show this aggressive behavioral pattern. Injuries associated with horses and donkeys are usually produced by animal kicks or by falls during riding. Stavrev19 reported a case of open multiple forearm fractures caused by a donkey bite, and Gomes et al20 reported a case of a minor penile laceration of a 7-year-old boy due to a donkey bite, but fatal bite injuries by a donkey have not been previously published.

property from an adjacent road. The deceased was normally dressed, but the upper right portion of his shirt was torn. Present inside the yard was an adult male donkey, apparently docile and uninterested in the corpse. On its upper lip, a small bloodstain was visible and subsequently collected by the investigators. Settled in the bordering court was a donkey herd, containing both male and female animals. The victim had a very deep wound in the anterior region of the neck, extending from the jugular notch to the upper part of the laryngeal prominence, and to the inner edge of the sternocleidomastoid muscles on both sides (Fig. 1). Through the wound, a sharp transection of the anterolateral wall of the trachea and a composite fracture of the thyroid cartilage were visible. At autopsy, the trachea was found to be almost completely severed, with only a small portion of the posterior membranous wall remaining intact. Severe bleeding by several minor vessels wall disruptions was detected in this area. An intratracheal hemorrhage leading to blood aspiration was observed. Macroscopically, the lungs showed evidence of massive alveolar blood invasion of the inferior lobes. No fractures of the cervical column were detected by either direct inspection or by x-rays. The cause of death was established to be massive bleeding combined with asphyxia due to aspiration of the blood. A deep contusion was visible in the right shoulder area, with an extensive reddish hematoma, and 2 distinct wounds involving metacarpal bone fractures of the right hand were present. These injuries were considered to be defense wounds. Moreover, multiple contusions with associated skin abrasions and perforations, especially in the face, right arm, and thorax, were present. These contusions showed a common pattern, although not always easily recognizable because of the numerous different wounds. Most of the wounds were relatively superficial and limited to muscular tissue, not penetrating into the body cavities. Not all wounds were likely to have been produced at the same time. For example, some abrasions on the chest had a brownish color and a papyrus-like consistency; they were considered to be inflicted postmortem. The general impression of the injuries was consistent with an animal’s bite marks. Therefore, a dental impression of the

CASE REPORT A 65-year-old man was found dead in his farmyard. His body was lying supine under a tree near the fence separating his

Manuscript received October 27, 2008; accepted May 27, 2009. From the *Institute of Legal Medicine, University of Cagliari, School of Medicine, Cagliari; and †Institute of Legal Medicine, Catholic University of the Sacred Heart, School of Medicine, Rome, Italy. Reprints: Fabio De-Giorgio, MD, PhD, Institute of Legal Medicine, Catholic University of the Sacred Heart, School of Medicine, Largo Francesco Vito, 1, 00168 Rome, Italy. E-mail: [email protected]; [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0183 DOI: 10.1097/PAF.0b013e318219cfce

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FIGURE 1. The bite wound on the neck (arrow).

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FIGURE 2. A and B, The donkey’s dental impression.

donkey was made. In this impression, 6 elements were identified showing an average length of 2 cm. The anterior dental formula of a donkey, as well as of a horse or other equines, is characterized by 6 incisors and a diastematic canine tooth (Fig. 2, A and B). All clearly detectable bite marks had 2 opposite semicircular arches, 12 cm in length, each showing a semicontinuous line with 5 minor incisions. Two puncture wounds with undamaged skin between them, each with a depth of 2 cm, were visible, but in only 1 of the 2 semiarches. Comparison between the donkey’s dental formula and the bite marks showed a complete match. In particular, the wound elements corresponded to the anterior teeth of the donkey. A better match was achieved for wounds in which a compact structure (eg, metacarpal bones or thoracic wall) was underlying the skin surface. Furthermore, the bloodstain collected from the upper lip of the donkey was human blood and was matched to the victim’s blood using the SilverSTR III STR system (Promega Corporation, Madison, Wis). According to the toxicological analysis of the victim’s samples, the blood ethanol concentration was 0.03 g/L; no therapeutic drugs or drugs of abuse were detected.

DISCUSSION Various animals inflict bite injuries on humans, but in Western countries, most animal bite wounds are inflicted by dogs and cats, dogs alone being responsible for up to 90% of these wounds.21,22 Most frequently, bite and scratch injuries are caused by mammals,21,22 and mammalian bites account for 1% of all visits to emergency departments.23,24 However, most animal bite injuries are minor, and the rate of hospitalization is only

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about 5%.22 The main medical concern with animal bites is that the wounds are prone to become infected, requiring adequate antibiotic therapy and rabies prophylaxis.1,25,26 Only a very small proportion of animal bite injuries lead to death. Herbivorous or omnivorous bite attacks on humans are rare; instead, these animals attack by kicking, trampling, and kneeling, resulting in secondary blunt injuries.17,18,27 Other typical injuries related to large domestic animals are falls during riding. The donkey is usually a docile animal, but its behavior can be aggressive during the mating season. Its attack pattern is generally represented by trampling or kicking the human enemy, but the possibility of biting should not be underestimated, as illustrated by the 2 cases published previously19,20 as well as by the case presented here. In animal bite fatalities, bite wounds on the head and neck, as in the present case, are typical, especially in children.6,10,12,22,28 The mechanism of death in our case was a combination of external bleeding and aspiration of blood. Neck injuries can also lead to asphyxia14 or air embolism,28 neither of which occurred here. According to the publications we reviewed, the most frequent causes of death associated with animal bites are exsanguination and infection.1,4,10,13,29Y32 It cannot be excluded that the victims may sometimes provoke the animal attack with their own behavior.6,18,33,34 For instance, alcohol, which was detected in our case, can modify human behavior, and the odor of alcohol can affect an animal’s behavior.16 In 92 animal-related deaths reported by Langley,18 the level of alcohol was ascertained in 41 cases; alcohol was detected in 10 cases. We illustrate here a rare case of an apparently docile donkey inflicting a fatal bite on his master. Although domestic animals do attack human beings, assaults by herbivorous animals are exceptional. In our case, the event was clarified in a medicolegal investigation with a detailed autopsy, including a bite mark analysis that revealed a complete match between the donkey’s dental formula and the bite marks on the victim. REFERENCES 1. Bux RC, McDowell JD. Death due to attack from chow dog. Am J Forensic Med Pathol. 1992;13:305Y308. 2. Mathews JR, Lattal KA. A behavioral analysis of dog bites to children. J Dev Behav Pediatr. 1994;15:44Y52. 3. Centers for Disease Control and Prevention. Dog-biteYrelated fatalitiesVUnited States, 1995Y1996. MMWR Morb Mortal Wkly Rep. 1997;46:463Y467. http://www.cdc.gov/mmwr/PDF/wk/mm4621.pdf. Accesssed April 4, 2011. 4. Lauridson JR, Myers L. Evaluation of fatal dog bites: the view of the medical examiner and animal behaviorist. J Forensic Sci. 1993;38:726Y731. 5. Sacks JJ, Lockwood R, Hornreich J, et al. Fatal dog attacks, 1989Y1994. Pediatrics. 1996;97:891Y895. 6. Pinckney LE, Kennedy LA. Traumatic deaths from dog attacks in the United States. Pediatrics. 1982;69:193Y196. 7. Wright JC. Severe attacks by dogs: characteristics of the dogs, the victims, and the attack settings. Public Health Rep. 1985;100:55Y61. 8. Weiss HB, Friedman DI, Coben JH. Incidence of dog bite injuries treated in emergency departments. JAMA. 1998;279:51Y53. 9. Avis SP. Dog pack attack: hunting humans. Am J Forensic Med Pathol. 1999;20:243Y246. 10. De Munnynck K, Van de Voorde W. Forensic approach of fatal dog attacks: a case report and literature review. Int J Legal Med. 2002;116:295Y300.

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11. Wright JC. Reported cat bites in Dallas: characteristics of the cats, the victims and the attack events. Public Health Rep. 1990;105: 420Y424. 12. Cohle SD, Harlan CW, Harlan G. Fatal big cat attacks. Am J Forensic Med Pathol. 1990;11:208Y212. 13. Rollins CE, Spencer DE. A fatality and the American mountain lion: bite mark analysis and the profile of the offending lion. J Forensic Sci. 1995;40:486Y489. 14. Wiens MB, Harrison PB. Big cat attack. J Trauma. 1996;40: 829Y831. 15. Vogel JS, Parker JR, Jordan FB, et al. Persian leopard (Panthera pardus) attack in Oklahoma: case report. Am J Forensic Med Pathol. 2000; 21:264Y269. 16. Chapenoire S, Camiade B, Legros M. Basic instinct in a feline. Am J Forensic Med Pathol. 2001;22:46Y50. 17. Karkola K, Mo¨tto¨nen M, Raekallio J. Deaths caused by animals in Finland. Med Sci Law. 1973;13:95Y97.

Death Secondary to a Donkey’s Bites

scratch injuries by vertebrate animals in Switzerland. Eur J Epidemiol. 1998;14:483Y490. 23. Goldstein EJ. Bite wounds and infection. Clin Infect Dis. 1992;14: 633Y638. 24. Galloway RE. Mammalian bites. J Emerg Med. 1988;6:325Y331. 25. Feder HM Jr, Shanley JD, Barbera JA. Review of 59 patients hospitalized with animal bites. Pediatr Infect Dis J. 1987;6:24Y28. 26. Hermann CK, Hansen PB, Bangsborg JM, et al. Bacterial infections as complications of dog bites. Ugeskr Laeger. 1998;160:4860Y4863. 27. Bush HM Jr, Cogbill TH, Landercasper J, et al. Blunt bovine and equine trauma. J Trauma. 1986;26:559Y560. 28. De Giorgio F, Rainio J, Pascali VL, et al. Bear attack: a unique fatality in Finland. Forensic Sci Int. 2007;173:64Y67. 29. Yanai O, Goldin L, Hiss J. Fatal rat bites [in Hebrew, abstract in English]. Harefuah. 1999;136:611Y613, 658Y659.

18. Langley RL. Fatal animal attacks in North Carolina over an 18-year period. Am J Forensic Med Pathol. 1994;15:160Y167.

30. Nathwani D, McIntyre PG, White K, et al. Fatal human rabies caused by European bat Lyssavirus type 2a in Scotland. Clin Infect Dis. 2003;37:598Y601.

19. Stavrev V. A case of open multiple fractures of both forearms caused by a donkey bite. Folia Med. 1998;40:77Y80.

31. Byard RW, Gilbert JD, Brown K. Pathologic features of fatal shark attacks. Am J Forensic Med Pathol. 2000;21:225Y229.

20. Gomes CM, Ribeiro-Filho L, Giron AM, et al. Genital trauma due to animal bites. J Urol. 2000;165:80Y83.

32. Woolgar JD, Cliff G, Nair R, et al. Shark attack: review of 86 consecutive cases. J Trauma. 2001;50:887Y891.

21. Rainio J, De Giorgio F, d’Aloja E, et al. Deaths due to animal assault. Proceedings of the 8th Cross Channel Conference Forensic ScienceVRecent Developments: April 20Y24, 2004; Bruges, Belgium.

33. Shattock FM. Injuries caused by wild animals. Lancet. 1968;1(7539): 412Y415.

22. Matter HC, Arbeitsgemeinschaft S. The epidemiology of bite and

34. Durrheim DN, Leggat PA. Risk to tourists posed by wild mammals in South Africa. J Travel Med. 1999;6:172Y179.

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Death of a Scuba Diver Caused by Vomiting and Panic A Case Report Nadan M. Petri, MD, PhD,* Hrvoje Stipancevic, MD,* Davorka Sutlovic, PhD,Þ and Marija Definis Gojanovic, MD, PhDÞ Abstract: Scuba diving fatalities are rare and sometimes extremely difficult to explain. A thorough forensic investigation, conducted by a qualified team, helps avoid possible later questions and doubts, family concerns and judicial matters, since a significant body of evidence is lost after the body of the victim is buried or the equipment is reused. We report about a death of a scuba diver who was drowned while diving to the depth of 30 meters. Before being assisted to the surface, the diver panicked and removed the regulator from his mouth. The technical expertise of the scuba gear and the chemical analysis of the air from the high-pressure cylinder revealed no irregularities. Homicide, suicide, nitrogen narcosis, oxygen toxicity, and regulator malfunction were ruled out as possible causes of death. The most probable cause that triggered the event was vomiting into the regulator, as confirmed nearly 4 years later by the toxicological analysis of the traces of matter found in the dry chamber of the breathing regulator. Such an analysis should be considered when investigating suspicious diving related deaths and could be undertaken even after a significant time delay if the equipment is kept properly stored. Key Words: autopsy, diving, drowning, forensic medicine (Am J Forensic Med Pathol 2011;32: 186Y189)

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nderwater diving is a potentially dangerous activity. The hostile underwater environment, increased pressure, consecutively increased nitrogen load, toxicity of gases at increased pressure, low water temperature, underwater currents, dangerous marine life, psychologic load, low visibility, and specific physiological response represent a frame for a specific underwater stress to which various persons react in a different manner. In a dangerous situation, the majority of divers will most probably remain calm and react in a reasonable way, but some divers will panic and endanger or even kill themselves or their diving buddies.1,2 In the constantly growing scuba diving community, specific diving related diseases and injuries are not rare.3Y5 The majority of injuries is mild in nature and is very often unreported, neglected or even go undetected by the divers. Various national and international agencies and organizations collect, summarize and analyze data about the most serious incidents, ie, decompression sickness, pulmonary barotrauma and fatalities, to determine the frequency, trends, patterns, and most probable

Manuscript received December 17, 2009; accepted June 11, 2009. From the *Naval Medicine Department, Military Medical Center Split, and University of Split School of Medicine, Split, Croatia; and †Forensic Medicine Department, Clinical Hospital Center Split, and University of Split School of Medicine, Split, Croatia. The opinions expressed herein are of the authors and do not necessarily reflect the views of Military Medical Center of the Croatian Military Support Command or Ministry of Defense of the Republic of Croatia. Reprints: Nadan M. Petri, MD, PhD, 21000 Split, P.O. Box 196 (HRM), Naval Medicine Department, Military Medical Center, Split, Croatia. E-mail: npetri)mefst.hr. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202-0186 DOI: 10.1097/PAF.0b013e3181d3de7a

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causes, but also to establish the basis for preventive measures and treatment. However, there are neither registries nor reports covering the morbidity or mortality of all the divers in the world. Unlike diseases and injuries, diving related fatalities are rare. Some 160 diving fatalities are reported annually to Divers Alert Network and 90 of them include US citizens diving in the United States and abroad.6 The total number of diving related deaths worldwide every year remains unknown. Investigation of diving related deaths is impossible without including experts in diving medicine.7Y9

SOME EPIDEMIOLOGICAL DATA FROM CROATIA In Croatia, approximately 100,000 divers perform at least 1,000,000 single-man dives per year.10 More than 90% of divers are inexperienced foreign tourists from nonmaritime countries, who dive mostly from June to September. There is no national registry of diving diseases and fatalities, but it is estimated that 20 to 25 divers die annually while diving in Croatia (Neven Lukas, Croatian Diving Federation, personal communication, 2008). Their deaths are usually classified as drowning. Most often, if no injuries or signs of violence were detected during the external examination of a body, the investigation team would not even appear at the site of death, which is often at remote diving locations. Under these conditions, no lessons are learned, possible errors in investigations remain unknown, responsible persons go unrevealed, and families are left with doubts.

CASE REPORT The Fatality We report the case of a scuba diver who was drowned during a routine dive trip at a shipwreck, in a calm and warm sea (17-C at the bottom). The deceased victim was a male Caucasian, 27 years old, properly trained, apparently healthy, fairly experienced, and completely equipped for the dive. After several minutes near the depth of 30 meters, a diving buddy noticed the victim kicking his fins in obvious panic. He immediately approached him but the victim signaled that everything was well. After a few seconds, the victim dropped his breathing regulator. The diving buddy later reported that the victim was probably unconscious, with his jaws firmly closed, a couple of seconds after dropping the regulator. The efforts to assist the victim with the reserve regulator of the rescuer failed, both at the diving depth and during the ascent. Resuscitation measures that were provided on the dive boat for some 20 minutes failed.

The Post Mortem Findings The autopsy, performed in accordance with the recommendations for diving fatalities,7Y9 revealed drowning as the cause of death. No alcohol was found in the blood of the deceased. No signs of pulmonary barotrauma and cerebral arterial gas embolism were found, although could have been expected in accordance with Boyle_s Law (at constant temperature, the volume is inversely proportional to the absolute pressure). The post mortem findings were in accordance with the statement of Am J Forensic Med Pathol

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and oxygen toxicity were also ruled out as possible triggers of the event. The rapture of the deep could have occurred at 30 meters,12 although some nitrogen narcosis was indeed described even in much shallower air diving, even at 10 meters.13 The deceased was a fairly experienced diver and should have recognized early warning signs of narcosis and should have sent signals to his diving buddy in case of problems, then would have merely ascent for a couple of meters and not necessarily abort the dive. None of the described was the case. Kicking with fins in panic was not typical for the rapture of the deep, since its signs at 30 meters would most probably resemble mild alcoholic intoxication.12 Oxygen toxicity is theoretically possible in air diving, since air contains 21% of oxygen. If such toxicity would occur at all, the lowest partial pressure of oxygen would have to be at least 1.3 bars, the corresponding depth on air 52 meters, and a diver would have to spend at least 180 minutes under water, which was not the case in this fatality.14

The Gear FIGURE 1. Scuba diving regulatorYsecond stage valve assembly. Reproduced from United States Navy Diving Manual, Vol. 2, Revision 6.17 The diaphragm divides ‘‘dry’’ (low pressure chamber) and ‘‘wet’’ chambers of a regulator. During underwater breathing, the diaphragm moves towards the mouthpiece driven by inhalatory pressure generated by breathing muscles. At the same time, the diaphragm pushes a ‘‘horseshoe’’ that opens intermediate pressure valve and enables air entry to the ‘‘dry chamber,’’ ie, the mouthpiece and lungs.

the rescuer who said that the ascent to the surface BI was slow to avoid pulmonary overpressureI,[ but dive computer data was not available for the analysis. Conjunctival hemorrhage was in accordance with the drowning scenario. Some 100 mL of semi-digested food was found in the stomach. No other details significant for the investigation were noted at that time.

The Investigation The investigation team, which included specialists in diving and forensic medicine and a forensic biochemist, was a precedent investigation of diving fatalities rather than an example of the usual investigation of diving fatalities practiced in Croatia. Several sworn witnesses described the event with minor differences, but all of them blamed the Croatian dive guide for not coming to rescue by being some 10 to 15 meters away when alerted by the victim_s buddy. The investigation team was also ordered to determine if such assistance could have saved the victim_s life. The Croatian dive guide stated that he indeed saw the signals but understood them as everything was under control and that the buddy will assist the casualty to the surface. The nationals of the deceased had a lot of complaints referring to the entire organization of the dive, which included the statement that the deceased was afterward charged 50% of the usual fee for the trip. Although a significant emotional load and some diplomatic pressure were also felt as part of the entire event, the investigation team focused efforts towards the cause of the incident, technical and functional characteristics of scuba gear and general safety aspects of the dive.

The scuba gear, consisting of a 20 L high-pressure cylinder, neoprene diving suit, face mask, snorkel, fins, lead belt, dive watch, pressure gauge and 2 regulators, both primary and reserve, was kept locked, but not sealed, at a local police station for almost 4 years before it was sent for expert analysis. In many countries, such a body of evidence would be rejected in courts as unacceptable, regardless of the results of an investigation, since a reasonable doubt would necessarily emerge. In that sense, it could have been speculated that the quality of air stored in the high-pressure cylinder had originally not been in accordance with quality requirements15 and could have been deliberately replaced after the event, to misguide the investigation. It could have been also speculated that one or both regulators, possibly malfunctioning, could have been replaced. We do not have any knowledge of any tampering of evidence, suspicions or speculations of that kind in the present case. Changes of equipment that occur with time, especially affecting rubber parts, corrosive effect of salt and loss of pressure from the cylinder, making air analysis impossible, were also expected. All of that could have made the investigation difficult and impossible to reach reliable conclusions. After some 4 years, no one remembered which of the 2 regulators the deceased was using at the time of death.

The Most Unlikely Causes of Death Although possible, homicide9 and suicide11 are extremely rare in diving and were easily excluded as possible causes of death. The deceased was a member of a group and none of the activities, including those of the deceased, would have gone undetected. Nitrogen narcosis (the rapture of the deep)

FIGURE 2. Membrane from a diving regulator (‘‘dry’’ side), with traces of dried matter, analyzed in the investigation of a death in diving, allegedly caused by vomiting and panic.

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FIGURE 3. Comparison of results of gas chromatography of 3 samples analyzed during forensic investigation of a death in diving, allegedly caused by vomiting and panic. Total ion chromatogram of: top line = silicone grease; middle line = organic matter found on the dry side of the membrane and in the dry chamber of the primary regulator with esters of oleinic acid (arrow) and traces of silicone grease; bottom line = swab of the secondary (reserve) regulator (negative control). X-axis indicates time (minutes); y-axis, signal intensity.

Since the victim_s regulators were not used on the way to the surface, their possible malfunction could not have been evident during the ascent. However, neither regulator showed signs of malfunction when the diving buddies manually purged them on the deck of the dive boat, soon after the accident.

The Results Technical expertise revealed no technical irregularities of regulators even after 4 years of being stored in a locker. Breathing performance of both regulators was found to be in accordance with the requirements set forth by the European Union for open-circuit scuba apparatuses.16 The high-pressure cylinder contained 55 bars of air, ie, more than 25% of the maximum charge (200 bars), so the deceased was not facing the low-on-air situation and could have safely ascended to the surface and completed the dive. Chemical analysis revealed that the quality of air was in accordance with the requirements for oilfree air.15 Breathing problems that could have occurred due to possible regulator malfunction, leakage of water into the mouth or leakage of air from the regulator, labored ventilation, regulator_s increased breathing resistance or air contamination were therefore excluded as possible triggers of the event. The investigation then focused on the statements of the witnesses who claimed that the deceased had a meal approximately 2 hours before the fatal dive. If the deceased would have vomited into the regulator, that could have caused panic and drowning. This suspicion could be confirmed if fragments of vomited content could be found in the Bdry chamber[ of the regulator (Fig. 1).17 Although the dry chamber must have been washed out, first when the regulator was removed from the mouth and then during the ascent, the fragments of vomited content could have somehow remained on the diaphragm or in the corners of the Bdry chamber.[ Both regulators were carefully disassembled and traces of dry matter were found in the dry chamber, at first appearing to be of organic nature, especially on the Bdry[ side of the diaphragm of the primary regulator (Fig. 2). Such a material was not found on the Bwet[ side of the diaphragm, in the wet chamber of the primary regulator, nor anywhere in the reserve regulator. Toxicological analysis was performed on gas chromatograph with mass detector (Model GC/MS 2010, Schimadzu, Tokyo, Japan), which revealed that the dry matter contained

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esters of oleinic acid. It was concluded that the matter found on the diaphragm and in the dry chamber of the primary regulator represented remains of vomited gastric content since no other explanation for such traces in the dry chamber could have been found. The same analysis of swab sampled from the membrane of the secondary regulator was negative as well as of the silicone grease used in the same dive locker to lubricate regulator rubber parts (Fig. 3).

DISCUSSION Traces of esters of oleinic acid in the dry chamber of the primary regulator were most probably the remains of vomited content. Other food compounds were most probably washed out by seawater, unlike greasy and sticky oil content. The only matter that could have also come in contact with the membrane and the dry chamber of the regulator was silicone grease, but it contained no esters of oleinic acid, as proven by gas chromatography (Fig. 3). DNA analysis was not attempted in this case. Besides many technical difficulties, there were also concerns connected with legal reliability of conclusions that could have been only loosely based on DNA analysis. If tissue cells belonging to the deceased had been found in the dry chamber of the regulator, DNA analysis would have had identified the deceased as the person who probably vomited the content found in the regulator, but positive DNA match could have also been interpreted merely as a proof of contact of the deceased with the regulator, which was never in doubt. It seems that the dive guide_s intervention would not have helped even if he had come to the rescue. It is hard to believe that he would have been able to open the mouth of the victim to provide air using the reserve regulator. As described by the rescuer, the jaws of the victim were already firmly closed at that time. It could only be speculated that trying to use a knife as a lever might have been successful, but it remains unclear if the guide would have arrived in time to provide any effective assistance. A meal, taken recently before a dive, could cause burping, heartburn, or esophageal reflux. An increase of gastroesophageal pressure gradient during submersion predisposes a diver to esophageal reflux. In this case, higher intragastric pressure and * 2011 Lippincott Williams & Wilkins

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lower intraesophageal pressure could have caused at least some regurgitation of the gastric content and an extremely unpleasant sensation but also vomiting and panic, possibly after a swallow of seawater. Divers learn about this problem and usually avoid hardly digestible food. How long to wait after a meal before diving varies from person to person and is also a matter of a particular meal, but a large meal containing hardly digestible food represents greater risk. Recommendations found on dive web sites agree on a 2-hour predive interval.18Y20 Certain drugs, such as anticholinergics, calcium channel blockers, ethanol, progesterone, theophylline, tricyclic antidepressants and nitrates, could diminish distal esophageal sphincter pressure by its inappropriate relaxation and should be avoided in diving.21 It remains unknown if the deceased diver was taking any such drugs. There was some 200 mL of vomited content noted near the victim_s body on the deck of the dive boat, and some additional 100 mL of semi-digested food was found during post mortem in the stomach, suggesting that the victim had an ample meal before the dive. Problems caused by esophageal reflux could be easily overcome on the surface, but can represent an extremely unpleasant situation under the water and could cause problems using the regulator and panic. This is also why persons who experience significant dyspepsia, regurgitation, pyrosis and reflux esophagitis should be carefully examined for professional diving.22,23 Nausea and vomiting during diving are not rare, especially after a meal taken recently before a dive, and seem to have caused quite a number of fatalities so far.6,9,24 Vomiting under the water while scuba diving is a potential threat not only in cases when gastric content is actually vomited into the dry chamber of a regulator but also when just some reflux happens. Although a few seconds of breath holding would be enough to clear the mouth and the regulator, this might be a trigger of panic in some divers, especially if vomiting would occur at the end of an expiration. Some divers just may not have enough diving skills to overcome the situation. It seems that the same could have happened in this case. Based on toxicological analysis of the identified matter found in the dry chamber of the primary regulator, the most probable scenario in this fatality would be: vomiting, panic, loss of regulator, apnea, unconsciousness, inhalation and/or swallowing of sea water, assisted ascent, and death due to drowning. This scenario is in accordance with the post mortem findings and the witnesses_ statements, although we admit that some other details could have remained undetected. Recently, a case of a death in diving gained much public interest, since the suspect was accused of a homicide although vomiting under the water was also presumed.25 Proper technical and toxicological analysis could most probably exclude many reasonable doubts in similar cases. It is our opinion that a dead diver_s body is never just a silent witness, but a very loud witness that should be listened to. The present case report confirms that each and every diving fatality must be carefully investigated to find out the most probable cause of death.5,7Y9,24 Searching the Internet and using diving, fatality, death, vomiting and regulator as key words, we did not find any previous reports describing forensic analysis of vomited content from a scuba regulator. REFERENCES 1. Anegg U, Dietmaier G, Maier A, et al. Stress-induced hormonal and mood responses in scuba divers: a field study. Life Sci. 2002;70: 2721Y2734. 2. Morgan WP. Anxiety and panic in recreational scuba divers. Int J Sports Med. 1995;20:398Y421.

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3. Najayama H, Smerz RW. Descriptive epidemiological analysis of diving accidents in Hawaii from 1983 to 2001. Hawaii Med J. 2003;62:165Y170. 4. Andersen HL. Decompression sickness during construction of the Great Belt Tunnel, Denmark. Undersea Hyperb Med. 2002;29:172Y188. 5. O_Connor P, O_Dea A, Melton J. A methodology for identifying human error in U.S. Navy diving accidents. Hum Factors. 2007;49:214Y226. 6. Pollock NW, Vann RD, Denoble PJ, et al. Annual Diving Report 2007 Edition. Durham, NC: Divers Alert Network; 2007. 7. Goldhahn RT. Scuba diving deaths: a review and approach for the pathologist. Legal Med Annu. 1977;1976:109Y132. 8. Findley TP. An autopsy protocol for skin and scuba diving deaths. Ann J Clin Pathol. 1977;67:440Y443. 9. Caruso JL. The pathologist_s approach to SCUBA diving deaths. Available at: http://rubicon-foundation.org. Accessed November 20, 2008. 10. Andric D, Petri NM, Stipancevic H, et al. Change of occurrence of type 1 and type 2 decompression sickness of divers treated at the Croatian Naval Medical Institute in the period from 1967 to 2000. Int Marit Health. 2004;54:127Y134. 11. Petri NM, Definis-Gojanovic M, Andric D. Scuba diver with a knife in his chest: homicide or suicide. Croat Med J. 2003;44:355Y359. 12. Bennett PB, Rostain JC. Inert gas narcosis. In: Brubakk AO, Neuman TS, eds. Physiology and Medicine of Diving. 5th ed. Edinburgh, GB: Saunders; 2003:300Y322. 13. Petri NM. Change in strategy of solving psychological tests: an evidence of nitrogen narcosis in shallow air-diving. Undersea Hyperb Med. 2003;30:293Y303. 14. Joiner JT, ed. NOAA Diving Manual. 4th ed. Flagstaff, AZ: Best Publishing; 2001:15Y5. 15. Anonymous. United States Navy Diving Manual. Rev 6, Vol 2. Washington, DC: Naval Sea Systems Command; 2008:10Y11. 16. Anonymous. Respiratory equipment. Open-circuit self-contained compressed air diving apparatuses. Brussels, Belgium: European Committee for Standardization; 1999. 17. Anonymous. United States Navy Diving Manual. Rev 6, Vol 2. Washington, DC: Naval Sea Systems Command; 2008:7Y3. 18. Campbell E. Nutrition and scuba diving. Available at: http://www.scuba-doc.com/Nutrition.htm. Accessed December 5, 2008. 19. Anonymous. Scuba diving/Things to consider. Available at: http://www.iexplore.com/activity/Scuba+Diving/Things+to+Consider. Accessed December 5, 2008. 20. Young D. Scuba diving do_s and don_ts (You might have overlooked). Available at: http://ezinearticles.com/?Scuba-Diving-Dos-and-Donts(You-Might-Have-Overlooked)&id=1233708. Accessed 5, 2008. 21. Tolstoi LG. Drug-induced gastrointestinal disorders. Available at: http://bcbsma.medscape.com/viewarticle/437034. Accessed November 20, 2008. 22. McIver NK. Dental, gastro-intestinal and genito-urinary fitness. In: Elliott DE, Elliott DH, ed. Medical Assessment of Fitness to Dive. Proceedings of an International Conference at the Edinburgh Conference Center, 8thY11th March 1994. Ewell, United Kingdom: Biomedical Seminars; 1995:199Y202. 23. Elliott DH. Medical evaluation of working divers. In: Bove AA, ed. Diving Medicine. 4th ed. Philadelphia, PA: Saunders; 2004:533Y545. 24. Caruso JL. Pathology of diving accidents. In: Brubakk AO, Neuman TS, eds. Physiology and Medicine of Diving. 5th ed. Edinburgh, United Kingdom: Saunders; 2003:729Y743. 25. Dive magazine. US diver formally charged for wife_s murder. Available at: http://www.divemagazine.co.uk/news/article.asp?uan=4910. Accessed December 2, 2008.

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An Unusual Case of Smothering Secondary to Ingesting Raw Pet Cat Margaret Redpath, MD* and Anny Sauvageau, MD, MSc*Þ Abstract: Smothering is defined as an obstruction of the air passages above the level of the epiglottis, including the nose, mouth, and pharynx. This is in contrast to choking, which is considered to be due to an obstruction of the air passages below the epiglottis. The manner of death in smothering can be homicidal, suicidal, or an accident. Accidental smothering is considered to be a rare event among middle-aged adults, yet many cases still occur. Presented here is the case of a 39-year-old woman with a history of bipolar disease who was found dead on her living room floor by her neighbors. Her hands were covered in scratches and her pet cat was found disemboweled in the kitchen with its tail hacked off. On autopsy her stomach was found to be full of cat intestines, adipose tissue, and strips of fur-covered skin. An intact left kidney and adipose tissue were found lodged in her throat just above her epiglottis. After a complete investigation, the cause of death was determined to be asphyxia by smothering due to animal tissue. Key Words: asphyxia, smothering, cat, case report (Am J Forensic Med Pathol 2011;32: 190Y192)

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mothering is defined as an obstruction of the air passages above the level of the epiglottis, including the nose, mouth, and pharynx.1 This is in contrast to choking, which is considered to be due to an obstruction of the air passages below the epiglottis.1 According to textbooks, the majority of cases of smothering are homicidal, whereas cases of choking are generally determined to be accidental.2,3 However, a recent 6-year retrospective study conducted at a provincial forensic center of all autopsies performed on victims of suffocation has demonstrated that contrary to general belief, suicide was the main manner of death declared in 59% of the cases of smothering.4 The majority of these suicidal smothering deaths were caused by placing an airtight plastic bag over the head. Furthermore, textbooks have traditionally described accidental smothering as a rare event mostly limited to young children.2,3 The previously mentioned study, however, demonstrates that accidental smothering is probably not as rare as those textbooks claim.4 Presented here is an unusual case of smothering in an adult female.

CASE REPORT A 39-year-old woman was found dead by her neighbors who used a copy of her key to get into her home because they were concerned about the noise that was coming from her residence. They described meowing and running followed by a big Manuscript received July 21, 2009; accepted July 28, 2009. From the *Laboratoire de sciences judiciaires et de medicine le´gale, 1701 Parthenais street, Montreal (Quebec), Canada; and †Office of the Chief Medical Examiner, Edmonton (Alberta) Canada. Reprints: Anny Sauvageau, MD, MSc, Office of the Chief Medical Examiner Office, 7007, 116 St, Edmonton (Alberta) Canada, T6H 5R8. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0190 DOI: 10.1097/PAF.0b013e3181d3dbef

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thud that sounded like someone fell. The victim was found in the supine position on the floor of her living room. There was blood around her mouth and dripping down her leg. Her pants were around her ankles and her underwear was soiled with blood and feces and was found half-way down her thighs. Intubation was not possible because there was a Bmass[ blocking her throat. In her kitchen, a cat was found dead on the floor next to a large knife. Its tail had been hacked off and placed on the stove. The cat was disembowelled and there was blood on the floor and water tap. There were no obvious signs of foul play, forced entry, or a struggle. It had snowed the night before and there were no signs of footprints leading up to the apartment. The victim lived with several cats and the unfortunate animal belonged to her. The victim had been diagnosed with bipolar disease 2 years earlier. She had attempted suicide twice before, once with medication and once with a knife. She was being followed up by a psychiatrist and was prescribed lithium and olanzapine. According to her friends, the victim_s behavior over the past few days was declining and she had a scheduled appointment with her psychiatrist the morning her corpse was found. On autopsy, external examination revealed multiple linear erosions on the dorsal sides of both hands and on her lower left leg. These lesions were consistent with cat scratches. Her interior lower lip was also lacerated. There was mild cyanosis of her face and no petechiae were observed. Examination of the external genital area was unremarkable. No other significant trauma was apparent. Internal examination revealed the presence of a large piece of adipose tissue and an intact left cat kidney molded to the laryngeal opening, thus obstructing it. There was no soft tissue injury to the neck and there were no cranial fractures or intracerebral hemorrhages. The trachea and bronchi were clear. The lungs were congested and edematous (750 g and 730 g). The heart revealed no evidence of coronary or valvular disease. The stomach contained strips of fur-covered skin, intestines, and fat. The cause of death was determined to be asphyxia by smothering due to animal tissue. A toxicology screen revealed the presence of olanzapine and lithium at therapeutic levels in her blood. No alcohol, drugs, or other medication were detected. Autopsy of the male cat (5 kg) revealed a large incision of the abdomen measuring 20 by 18 cm. Skin was missing as well as multiple internal organs including half the stomach, the intestines, the mesentery, the left kidney, and the spleen. Other injuries included several broken claws and multiple stab wounds to the thorax and abdomen, with injuries to the left lung, diaphragm, and liver. There was no evidence of trauma to the head or neck. The tail had been chopped off and the proximal third was Bwet[. Preliminary analysis of the tail revealed the presence of amylase.

DISCUSSION This case report describes the occurrence of an unusual fatal smothering. There is much variety in the literature as to the exact definition of smothering and how it is to be distinguished from choking. Smothering has been defined as (a) an obstruction at the level of the nose and mouth, (b) an obstruction of the external airways, and (c) an obstruction of the upper airways.1 Am J Forensic Med Pathol

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Definitions of choking vary even more widely: (a) a synonym of food or foreign body inhalation regardless of the anatomic location, (b) obstruction at the level of the mouth, oropharynx, and larynx, (c) obstruction of the larynx, trachea or bronchi, (d) obstruction of the airways, (e) obstruction of the internal airways, ( f ) obstruction of the upper airways, and ( g) obstruction of the upper internal airways.1 This lack of uniformity in the definition of terms causes a lot of confusion in the literature of case reports and case series. For example, 2 very similar cases of asphyxiation by toilet paper in the laryngopharynx were published in the same year and one author referred to the cause of death as choking and the other as smothering.5,6 To avoid such confusion, a standardization of definitions is urgently required. A recent article written by Sauvageau & Boghossian proposed that the epiglottis is an ideal anatomic landmark to serve as a boundary between the definitions of smothering and choking.1 Accordingly, the present case report was classified as a smothering since the animal tissue was found lodged just above the epiglottis. The manner of death in the majority of cases of smothering is homicide or suicide.2Y4 The most common method of inducing death by smothering is by placing a plastic bag over the head, which is especially common in cases of suicidal smothering.3 Accidental smothering is generally considered to be a rare event.2,3 However, a recent analysis of the manner of death in smothering demonstrated that it may not be as rare as the literature suggests: in this study, accidents accounted for 17.2%, while 20.7% were homicidal acts and the majority of smothering cases were a result of suicidal acts (58.6%).4 Children are generally considered to be more vulnerable to accidental smothering.2,3 Infants can become entangled under pillows and blankets.2 Young children are at risk for accidentally suffocating on plastic bags or balloons as they do not recognize the danger in playing with them.7 Aspiration of foreign objects is a significant cause of morbidity and mortality among children less than 4 years old, with a peak incidence between 2 and 3 years old.7Y10 Small objects, especially of spherical or cylindrical shape, pose the largest threat for this age group.7,9 Both edible objects, such as nuts, seeds, hotdogs, grapes, and berries and inedible objects such as marbles, pen caps, balloons, and coins are potential culprits.7Y10 Elderly individuals are also susceptible to smothering, especially while eating. Younger adults tend to asphyxiate on a single piece of food, whereas the elderly are more likely to asphyxiate on complex boluses of food and food of semi-solid texture.11 Dentures have also been shown to be the obstructing agent.2,11 Several important medical antecedents increase the risk of asphyxia during eating. Cognitive impairment secondary to cerebrovascular accidents, neurologic or motor impairment, acute alcohol intoxication, and poor dentition are all implicated as contributing factors to the risk of smothering.3,11 Intoxication by alcohol or other sedatives has been shown to increase the risk of smothering during eating,11 but whether or not this can be generalized to all forms of smothering is considered more controversial. Some argue that the amount of alcohol required to inhibit the body_s reaction to asphyxia in cases where the victim was found face-down in a pillow is at the level of an alcoholic coma, and thus it is more likely that alcohol intoxication is the main cause of death.3 Psychiatric patients are particularly vulnerable because many of the commonly prescribed antipsychotic drugs are central nervous system depressants that can lead to decreased arousability of the patient as well as suppression of the gag reflex.2 Accidental smothering among healthy adults is thought to be rare. However, enough accidents were described in a recent 6-year retrospective study to challenge this assumption.4 Sev-

Smothering Secondary to Ingesting Raw Pet Cat

eral cases of soil filling the mouth during a motor vehicle accident are described in one article.12 Placement of a gag in the mouth can also lead to death if the object is aspirated or pushed far enough down the throat to cause occlusion of airflow; although death is often unintentional in these cases, gagging is not considered an accident if it occurs during the commission of a crime. There have been several case reports describing unusual objects that people have asphyxiated on after either intentionally or unintentionally attempting to Bswallow[ them. Small objects can become trapped in the larynx or tracheobronchial tree depending on the size and consistency of the foreign body.9 Larger objects, like the 4  4 cm kidney in the present case, have also been described and tend to obstruct the air passages at a higher level. There was a case of a young man who had too much to drink and tried to swallow a pool ball, which subsequently became lodged between the 2 palatal arches, thus smothering him.13 Another example involves criminals attempting to evade arrest who died in the process of trying to swallow drug packets that became lodged in the back of the throat instead.14 Swallowing live fish is an occupational hazard for fisherman reported both while holding a fish in the mouth to liberate the fisherman_s hands to perform other duties,15 and while holding up a fish to examine it, which subsequently fell into the victim_s mouth.16 The bizarre nature of the smothering presented in this case report, renders it difficult to determine the motive behind the unusual actions. There were no signs of forced entry or a struggle, and after a complete police investigation, homicide was excluded. The victim had a history of manic-depressive disease and 2 previous suicide attempts so the idea of suicide was entertained but investigation of the scene and the autopsy results led more towards the hypothesis of an accident. The possibility that this case is an autoerotic accident has to be considered. An auto-erotic death is defined as an accidental death that occurs during solitary sexual activity in which a device, apparatus or prop used to enhance sexual pleasure in some way causes unintentional death.17,18 In the presented case, the victim_s neighbors were delayed in seeking help because they heard noises that resembled sexual activity. There was evidence suggestive of recent sexual activity at the scene because her pants and underwear were lowered and there was a clear substance in her underwear. There were no obvious sexual props found at the scene but the literature suggests that paraphernalia may not be a common finding in female autoerotic deaths.19Y21 A review comparing the features of male and female autoerotic asphyxial deaths showed that men tend to use a lot more props during autoerotic behavior, which indirectly serves to facilitate the forensic team_s ability to discern what has taken place by observing the scene of death.19 Women, in contrast, rarely use pornographic material, dress in unusual attire such as cross-dressing or use bizarre props and devices to induce pain, thus their presentation is more subtle. For a death to be classified as autoerotic, it is important to establish that the victim was not only involved in a solitary sexual activity, but also that the device or prop used to enhance sexual pleasure was directly involved in the accidental death. In other words, the victim must not simply die of natural causes during autoerotic activity. For example, there is a case of a man who died while engaged in masturbation with a vacuum cleaner.22 On autopsy he was shown to have died of a fatal cardiac event, and thus his death was declared as natural. This case was initially published as an autoerotic death but this classification was later challenged by Byard et al in an article on the definition of autoerotic death.17 In the present case, it is difficult to deduce what activities were going on before the victim died.

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Assuming she was engaged in auto-erotic behavior, animal fetishism may have played a role in her sexual fantasy. Some animal parts, such as the cut tail, may have been used as sexual props. Ingesting raw cat tissue may also have been part of a sexual scenario that unfortunately lead to her death. However, whether or not she was engaging in autoerotic behavior cannot be determined because not enough evidence was found during the full investigation to support this theory beyond a hypothesis. Given her psychiatric history and the recent report of decline in her behavior by friends, a psychotic delirium could also help explain some of her peculiar behavior. REFERENCES 1. Sauvageau A, Boghossian E. Classification of asphyxia: the need for standardization. J Forensic Sci. In press. 2. Spitz WU. Asphyxia. In: Spitz WU, Spitz DJ, eds. Spitz and Fisher_s medicolegal investigation of death: guidelines for the application of pathology to crime investigation. 4th ed. Springfield, IL: Charles C. Thomas; 2006:783Y845. 3. DiMaio VJ, DiMaio D. Asphyxia. In: Geberth VJ, ed. Forensic Pathology. 2nd ed. Boca Raton, FL: CRC Press; 2001:229Y277. 4. Boghossian E, Tambuscio S, Sauvageau A. Non-chemical suffocation deaths in forensic setting: a 6-year retrospective study of environmental suffocation, smothering, choking and traumatic/positional asphyxia. J Forensic Sci. 2010;55:646Y651. 5. Sauvageau A, Yesovitch R. Choking on toilet paper: an unusual case of suicide and a review of the literature on suicide by smothering, strangulation, and choking. Am J Forensic Med Pathol. 2006;27: 173Y174. 6. Saint-Martin P, Bouyssy M, O_Byrne P. An unusual case of suicidal asphyxia by smothering. J Forensic Leg Med. 2007;14:39Y41. 7. Baker SP, Fisher RS. Childhood asphyxiation by choking or suffocation. JAMA. 1980;244:1343Y1346. 8. Byard RW, Tsokos M. Infant and early childhood asphyxial deaths. Diagnostic issues. In: Tsokos M, ed. Forensic Pathology Reviews. Vol 2. Totowa, NJ: Humana Press Inc; 2005;101Y123.

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9. Gregori D, Salerni L, Scarinzi C, et al. Foreign bodies in the upper airways causing complications and requiring hospitalization in children aged 0Y14 years: results from the ESFBI study. Eur Arch Otorhinolaryngol. 2008;265:971Y978. 10. Bhana BD, Gunaselvam JG, Dada MA. Mechanical airway obstruction caused by accidental aspiration of part of a ballpoint pen. Am J Forensic Med Pathol. 2000;21:362Y365. 11. Berzlanovich AM, Fazeny-Do¨rner B, Waldhoer T, et al. Foreign body asphyxia: a preventable cause of death in the elderly. Am J Prev Med. 2005;28:65Y69. 12. Hanson KA, Gilbert JD, James RA, et al. Upper airway occlusion by soilYan unusual cause of death in vehicle accidents. J Clin Forensic Med. 2002;9:96Y99. 13. Fernando GC. A case of fatal suffocation during an attempt to swallow a pool ball. Med Sci Law. 1989;29:308Y310. 14. Seymour A, Black M, McFarlane JH, et al. Death by obstruction: sudden death resulting from impromptu ingestion of drugs. Am J Forensic Med Pathol. 2003;24:17Y21. 15. Pinheiro J, Cordeiro C, Vieira DN. Choking death on a live fish (Dicologoglossa cuneata). Am J Forensic Med Pathol. 2003;24: 177Y178. 16. Pritchard JR. Sudden death by Lepomis macrochirus (the killer fish). Am J Forensic Med Pathol. 1989;10:245Y246. 17. Byard R, Bramwell N. Autoerotic death. A definition. Am J Forensic Med Pathol. 1991;12:74Y76. 18. Sauvageau A, Racette S. Autoerotic deaths in the literature from 1954 to 2004: a review. J Forensic Sci. 2006;51:140Y146. 19. Byard RW, Hucker SJ, Hazelwood RR. A comparison of typical death scene features in cases of fatal male and female autoerotic asphyxia with a review of the literature. Forensic Sci Int. 1990;48:113Y121. 20. Gosink P, Jumbelic M. Autoerotic asphyxiation in a female. Am J Forensic Med Pathol. 2000;20:114Y118. 21. Byard RW, Hucker SJ, Hazelwood RR. Fatal and near-fatal autoerotic asphyxial episodes in women. Characteristic features based on a review of nine cases. Am J Forensic Med Pathol. 1993;14:70Y73. 22. Imami R, Kemal M. Vacuum cleaner use in autoerotic death. Am J Forensic Med Pathol. 1988;9:246Y248.

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CASE REPORT

Cause of Death Conundrum With Methadone Use A Case Report Michael C. Letsky, PharmD,*Þ Ross E. Zumwalt, MD,þ§ Steven A. Seifert, MD,*§ and Blaine E. Benson, PharmD*Þ

Abstract: Deaths caused by a methadone intoxication or overdose are becoming more frequent. We report a case involving a patient who had extremely high methadone blood concentrations but whose cause of death may have been unrelated to the drug. A 51-year-old woman was found deceased in bed by her daughter. At the scene were numerous bottles of methadone, with the chronic dosage of 240 mg 3 times a day. There was no history of prior suicide attempts, there were no reports of suicidal ideation having been voiced and there was no suicide note. At autopsy, there were no pills found in the stomach. Microscopic tissue examination revealed lobar pneumonia of the right lower lobe. Postmortem lung cultures grew out Streptococcus pneumoniae. Femoral blood contained methadone, 5.7 mg/L; EDDP, 2.1 mg/L; oxycodone, 0.017 mg/L; doxylamine, 0.022 mg/L; and ethanol, 13.0 mg/dL. The postmortem methadone concentration was consistent with her known dose, plausible pharmacokinetics and conditions of discovery. Various causes of death, such as a methadone-related arrhythmia from QTc prolongation or the contribution of methadone to the development of the pneumonia, cannot be ruled out and may well have caused or contributed to death, but the pneumonia was felt to be a competent cause of death. Ultimately, the most likely cause(s) of death, is a decision left to the individual medical examiner. This case is illustrative of the growing number of similar cases facing forensic pathologists. The cause of death cannot be solely based on drug concentrations and it may not be possible to come to a conclusion as to Bthe[ cause of death and the forensic pathologist must be content with Ba[ cause of death. Key Words: methadone, toxicity, medical investigator, forensic pathology, cause of death (Am J Forensic Med Pathol 2011;32: 193Y196)

D

eaths caused by a methadone intoxication or overdose are becoming more frequent as patients use this medication for pain resolution in place of traditional pain management medications. Case reports of methadone-associated deaths indicate doses as low as 10 mg in children and 45 mg in adults may cause fatal respiratory depression,1,2 and blood concentrations as low as 0.06 mg/L have been considered lethal.3 In contrast, individuals on long-term methadone maintenance develop tolerance and can maintain high blood concentrations that would be fatal in a naive user. We report a case involving a patient who had extremely high

Manuscript received July 24, 2009; accepted November 22, 2009. From the *New Mexico Poison and Drug Information Center, Albuquerque, NM; †University of New Mexico College of Pharmacy, Albuquerque, NM; ‡Office of the Medical Investigator, Albuquerque, NM; and §University of New Mexico School of Medicine, Albuquerque, NM. Reprints: Steven A. Seifert, MD, New Mexico Poison Center, MSC09 5080, 1 University of New Mexico, Albuquerque, NM 87131. E-mail: [email protected]. Copyright * 2011 by Lippincott Williams & Wilkins ISSN: 0195-7910/11/3202Y0193 DOI: 10.1097/PAF.0b013e3181d3de94

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methadone blood concentrations but whose cause of death may have been unrelated to the drug.

CASE REPORT A 51-year-old obese woman was found unresponsive by her daughter on the floor of her bedroom in the early afternoon approximately one hour after last being seen alive. That morning the decedent_s daughter delivered a box of Nyquil (Procter & Gamble, Cincinnati OH) to treat complaints of flu-like symptoms including chills and a high fever. Her medical history included seizures of unknown etiology, chronic back pain, major depressive disorder, and generalized anxiety disorder. The type and duration of her seizure disorder was not clear and diagnostic tests had never been undertaken. In addition, there was no indication that she had ever had an electrocardiogram. Per medical records and family interviews, she had stopped smoking and drinking 15 years prior to her death. Investigators from the medical examiner_s office responded to the death. The patient had been found lying face-up in bed. There was no foam in the airway or airway occlusion. Fourteen unopened bottles of 100 count 10 mg methadone tablets and one opened bottle containing 18 tablets of methadone 10 mg were found. The prescription label on the methadone bottles indicated a dosage of 240 mg 3 times a day (Fig. 1). Also found in the home were legitimate prescription bottles for the decedent containing bupropion extended release 150 mg, oxycodone 80 mg, gabapentin 800 mg, lorazepam 2 mg, and venlafaxine 75 mg. In addition, investigators found Zantrex, an herbal medication containing niacin 25 mg, yerbamate, caffeine, guarana, damiana, green tea, piper nigrum, ginseng, and kola nut, a medication bottle with no label containing a beige powdery substance, 10 Nyquil gel capsules, and a half-full bottle of tequila. Located in the trash found inside the decedent_s bedroom were 15 empty bottles of one hundred count 10 mg tablets of methadone, one empty ibuprofen bottle and an empty unlabeled medication bottle. In the decedent_s purse was another empty one hundred count methadone 10 mg bottle. There were no reports of suicidal ideation having been voiced and there was no suicide note. Medical records from the decedent_s treating physician indicated that methadone had been prescribed for her for at least 3 years. Her dose of methadone had varied between 170 mg a day (combined with 720 mg a day of oxycodone extendedrelease) and 760 mg a day. Her dosage at the time of death was 720 mg a day. She was described as alert and oriented on office visits while on this dosage. A methadone serum level drawn approximately one year prior to her death, while on a methadone dose of 760 mg every day, was reported as 1.353 mg/L. No new medications or changes in dose or dose regimens, other than the decedent_s apparent self-dosing of Nyquil, had occurred in the recent past. One week before her death she was found unresponsive on her kitchen floor by the daughter but was quickly revived, and

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FIGURE 1. Prescription methadone label found at the scene indicating a dose of 720 mg a day, written for 2160 tablets.

she did not seek medical care. The cause of her unresponsiveness was not established.

AUTOPSY FINDINGS The autopsy was performed approximately 24 hours after the death. There were early postmortem changes as evidenced by clouded cornea and internal autolysis. She weighed 250 pounds and measured 70 inches in length (BMI 36). Internally there were no injuries. The brain weighed 1410 g and was not swollen. The heart weighed 340 g. The coronary arteries were involved with mild nonocclusive arteriosclerosis. The right and left lungs weighed 840 and 570 g, respectively. There was lobar pneumonia (gray hepatization stage) of the right lower lobe. The liver was enlarged, pale and weighed 2130 g. There were chronic pyelonephritis changes of the right kidney. Microscopic examination revealed lobar pneumonia of the right lower lobe, fatty changes of the liver, mild coronary arteriosclerosis, chronic pyelonephritis, and chronic bronchitis. Postmortem lung cultures grew out Streptococcus pneumoniae. Analysis of femoral blood by GC/MS showed the following concentrations: methadone concentration of 5.7 mg/L, EDDP 2.1 mg/L, oxycodone 0.017 mg/L, with doxylamine 0.022 mg/L and ethanol 13.0 mg/dL.

DISCUSSION Methadone has been used as a maintenance treatment option for opioid dependence, heroin addiction, and chronic pain for over 50 years.4 By binding to mu-receptors, methadone inhibits ascending pain pathways, dampens response to pain, and produces generalized CNS depression.5 Administration also prevents withdrawal symptoms from cessation of other opioids. Methadone exists as 2 isomers that differ in pharmacologic activity and in their metabolism. Methadone pharmaceutical products are comprised of a racemic (50:50) mixture. The (R)-isomer produces the major therapeutic effects at the mu-receptors as well as the opioid adverse effects, such as CNS and respiratory depression. (R)-methadone also has a longer elimination half-life (38 hours) compared with (S)-methadone (28 hours).6,7 Methadone is metabolized by cytochrome P450 enzymes 1A2, 2B6, 2C9, 2C19, 2D6, and 3A4 to EDDP (2-ethylidene-1,5-dimethyl-3,3-diphenylpyrrolidine) and EMDP (2-ethyl-5-methyl-3,3-diphenyl-1-pyrrolidine).8Y10 Ultrarapid metabolizers, those with increased 2D6 or 2C19 enzymes and/or with altered alleles coding for these enzymes, may have lower blood concentrations of drug at steady state, leading to therapeutic failure and patient dissatisfaction.10,11 In these patients,

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higher doses and/or increased dosing frequency may be required to provide therapeutic benefit.12 Plasma methadone half-lives vary greatly among individuals ranging from less than 5 hours to 55 hours,13 with a population mean of 33 to 37 hours,14 and can vary according to endogenous CYP enzyme activity,15 urine pH and other factors.16,17 Because of its generally long half-life it can usually be dosed once per day. Methadone also has a relatively large volume of distribution, 4 L/kg (range, 2 to 13 L/kg), distributing widely and concentrating in organ tissues.9Y11 Methadone shows postmortem redistribution out of tissues into the blood, therefore providing the potential for blood levels of methadone to be artificially elevated in postmortem analysis.8,9,18 However, the extent of postmortem redistribution of methadone appears to vary considerably from individual to individual.19 Consistent with the large variability in pharmacokinetics, as well as the development of tolerance typical to opioids, a large range in methadone doses and dose intervals can be seen in a clinical setting. A typical starting dose of methadone in opioid dependence maintenance programs is 60 mg per day, with typical regimens ranging from 80 to 100 mg per day.10 However, doses as high as 1,200 mg a day have been reported.20 Volumes of distribution and half-lives may vary considerably in methadone maintenance patients leading to complex relationships between dose, blood levels, and clinical effects. In a 2006 study,21 methadone doses in methadone maintenance patients varied from 40 to 290 mg a day, with 111 (80.4%) patients receiving more than 120 mg a day, and of those, 90 patients received greater than 150 mg a day. In this study sample, the mean serum methadone level ranged between 0.110 and 2.350 mg/L. Four patients_ blood concentrations exceeded 1.50 mg/L. A patient receiving 360 mg of methadone a day was reported to have a plasma concentration of 2.800 mg/L.22 A separate study of 62 living methadone maintenance subjects revealed an average whole blood concentration of 0.11 mg/L (range, 0.03Y0.56 mg/L), and contrasted it with 59 deceased drug addicts whose whole blood methadone concentrations averaged 0.28 mg/L (range, 0.06Y3.09 mg/L).3 Case reports of methadone-associated deaths indicate that doses as low as 10 mg in children and 45 mg in adults may cause respiratory depression and arrest.1,2 Deaths are most likely to occur early in the titration of the dose regimen, when tolerance has not developed. In addition, high doses or rapid escalation of methadone dosing have been associated with prolonging the QTc interval, placing the patient at risk for developing a potentially fatal episode of Torsade de Pointes.23 In one report, postmortem blood methadone concentrations in eleven methadone maintenance patients who died of accidental methadone overdose averaged 0.47 mg/L (range, 0.03Y1.24 mg/L), while 11 maintenance patients whose deaths were not felt to be drug-related had blood methadone concentrations averaging 0.27 mg/L (range, 0.03Y0.99 mg/L).3 In another study of patients who died while on a methadone maintenance program for chronic pain, methadone concentrations ranged from 0.05 to 3.99 mg/L (mean, 0.87 mg/L).24 Those whose deaths were determined to be caused by a drug overdose had methadone concentrations that ranged from 0.18 to 3.99 mg/L (mean, 1.31 mg/L); whereas methadone concentrations ranging from 0.18 to 3.03 mg/L (mean, 1.16 mg/L) in those who died of a nondrugrelated cause. In another series of cases, one patient taking 180 mg/d had a postmortem methadone level of 1.40 mg/L, a second patient taking 45 mg/d had a level of 0.50 mg/L, a third taking 120 mg/d had a level of 1.90 mg/L, a fourth taking 80 mg/d had a level of 0.80 mg/L, and a fifth taking 80mg/d had a level of 1.40 mg/L.2 A 2002 retrospective review of methadone * 2011 Lippincott Williams & Wilkins

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concentrations in deaths in a medical examiner_s office showed a higher mean concentration of methadone (0.66 mg/L) in deaths certified as not caused by drug toxicity than the mean concentration (0.53 mg/L) in those where methadone toxicity caused or contributed to death.25 Deaths that result from an idiosyncratic effect, such as a ventricular dysrhythmia (Torsades de Pointes secondary to QTc prolongation, ventricular tachycardia, or ventricular fibrillation), may not exhibit, or may obscure, a dose-response relationship. The highest previously reported serum methadone concentration in a patient who was judged not to have died a drug-related death was 4.26 mg/L26; whereas the highest concentration in a methadone-related death was 7.4 mg/L.27 Because of variability in pharmacokinetics and tolerance, there is considerable overlap in serum methadone concentrations in those taking the drug therapeutically, those who died presumably as a result of methadone toxicity, and in those who died of other causes while taking methadone. Variation in methadone postmortem redistribution creates another layer of complexity when examining the relationship between the clinical pharmacological effect of serum concentrations at steady state in living patients and the pharmacological contribution to death of a similar concentration in those who died. In this case, we conclude the decedent_s postmortem blood concentration was consistent with her known dose, given the patient_s tolerance, methadone_s variable pharmacokinetics and the possibility of postmortem redistribution. Likewise, the serum methanol, ethanol, oxycodone, and doxylamine concentrations were consistent with the decedent_s doses and dose schedules, plausible pharmacokinetic parameters, postmortem ethanol generation, and conditions of discovery. There are at least 5 plausible possibilities regarding this woman_s cause and/or manner of death: (1) She may have acutely overdosed on her methadone and died of acute respiratory depression. However, although this decedent_s postmortem femoral blood methadone concentration was higher than any previously reported in a nonmethadone-related fatality, there is good evidence that she was, in fact, taking her prescribed dose for a prolonged period without adverse effects. She did not appear to be clinically intoxicated on the morning of her death shortly before being found dead and the amount of methadone at the scene was also consistent with her taking the drug as prescribed. She had no prior history of suicide attempts, had not voiced suicidal thoughts, left no note and had no pills in the GI tract; (2) She may have had a fatal, methadone-related ventricular arrhythmia secondary to a prolonged QTc. Her collapse the week before her death could have been from a ventricular dysrhythmia that spontaneously terminated. There was no history of long QTc, however, and her condition of discovery in repose on the bed, however, is consistent with an acute or nonacute mechanism; (3) She may have developed her pneumonia as a result of methadone-related chronic respiratory depression or, in a slight variation, a ventricular arrhythmia related to methadonerelated pneumonia-induced hypoxia, thus making methadone a contributing factor. But her ability to take this dose for prolonged periods without having previously developed pneumonia makes this less likely. She had been on this medication at these doses for many months (and on similar doses in previous years) without prior incident; (4) She may have had a seizure from her preexisting seizure disorder, which ultimately resulted in death, unrelated to her methadone or pneumonia; or (5) She may have developed the pneumonia unrelated to her methadone use and died as a complication of this illness. Depending on how one combines the various findings (prior history, condition of discovery, pill bottles, blood levels, etc.), different individuals can

Methadone Use and Death

construct different, potentially equally valid, scenarios. But in the end, the pneumonia itself was a competent cause of death. Whether one adds methadone as a contributing factor or, indeed, whether one decides that a seizure or methadone or other condition was the most likely cause of death, is a decision left to the individual medical examiner.

CONCLUSION In this case, we can conclude that the lobar pneumonia in and of itself was a competent cause of death; however, we cannot exclude that such a high concentration of methadone contributed to death by making her vulnerable to the development of lobar pneumonia or by triggering a ventricular dysrhythmia. The difficulty in determining with reasonable certainty the cause and contributing causes of death in this case is illustrative of the growing number of similar cases facing forensic pathologists in the face of an epidemic of prescription drug use and abuse.28 This case emphasizes the well established principal in forensic pathology that determining the cause of death cannot be solely based on a laboratory analysis of drug concentrations. In particular, postmortem blood methadone concentrations must be integrated in context of the decedent_s dose and dose regimen, medical history, known and plausible pharmacokinetic tolerance models, postmortem changes, and circumstances of death before assigning a cause of death. In many cases, as in this case, it may not be possible to come to a conclusion as to Bthe[ cause of death and the forensic pathologist must be content with Ba[ cause of death. REFERENCES 1. Drummer OH, Opeskin K, Syrjanen M, et al. Methadone toxicity causing death in ten subjects starting on a methadone maintenance program. Am J Forensic Med Pathol. 1992;13:346Y350. 2. Perret G, De´glon JJ, Kreek MJ, et al. Lethal methadone intoxications in Geneva, Switzerland, from 1994 to 1998. Addiction. 2000;95: 1647Y1653. 3. Worm K, Steentoft A, Kringsholm B. Methadone and drug addicts. Int J Leg Med. 1993;106:119Y123. 4. Me´garbane B, Decle`ves X, Bloch V, et al. Case report: quantification of methadone-induced respiratory depression using toxicokinetic/ toxicodynamic relationships. Crit Care. 2007;11:R5. 5. Linderbeck LR. Update of the clinical issues regarding methadone (Dolophine) therapy in pain management. AACN Adv Crit Care. 2008;19:253Y257. 6. Corkery JM, Schifano F, Ghodse AH, et al. The effects of methadone and its role in fatalities. Hum Psychopharmacol Clin Exp. 2004;19:565Y576. 7. Kristensen K, Blemmer T, Angelo HR, et al. Stereoselective pharmacokinetics of methadone in chronic pain patients. Ther Drug Mon. 1996;18:221Y227. 8. Boulton DW, Arnaud P, DeVane CL. Pharmacokinetics and pharmacodynamics of methadone enantiomers after a single oral dose of racemate. Clin Pharmacol Ther. 2001;40:48Y57. 9. Eap CB, Broly F, Mino A, et al. Cytochrome P450 2D6 genotype and methadone steady-state concentrations. J Clin Psychopharmacol. 2001;21:229Y234. 10. Eap CB, Buclin T, Baumann P. Interindividual variability of the clinical pharmacokinetics of methadone: implications for the treatment of opioid dependence. Clin Pharmacokinet. 2002;41:1153Y1193. 11. Hersberger M, Marti-Juan J, Rentsch K, et al. Rapid detection of the CYP2D6*3, CYP2D6*4, and CYP2D6*6 alleles by tetra-primer

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PCR and of the CYP2D6*5 allele by multiplex long PCR. Clin Chem. 2000;46(8 Pt 1):1072Y1077. 12. Pe´rez de los Cobos J, Sin˜ol N, Trujols J, et al. Association of CYP2D6 ultrarapid metabolizer genotype with deficient patient satisfaction regarding methadone maintenance treatment. Drug Alcohol Depend. 2007;89:190Y194. 13. Verebely K, Volavka J, Mule´ S, et al. Methadone in man: pharmacokinetic and excretion studies in acute and chronic treatment. Clin Pharmacol Ther. 1975;18:180Y190.

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receiving chronic methadone therapy. J Pain Symptom Manage. 2005;29:385Y391. 21. Peles E, Bodner G, Kreek MJ, et al. Corrected-QT intervals as related to methadone dose and serum level in methadone maintenance treatment (MMT) patients: a cross-sectional study. Addiction. 2007;102:289Y300. 22. Wolff K, Hay A, Raistrick D. High-dose methadone and the need for drug measurements in plasma. Clin Chem. 1991;37:1651Y1654. 23. Krantz MJ, Lewkowiez L, Hays H, et al. Torsade de Pointes associated with very-high-dose methadone. Ann Intern Med. 2002;137:501Y504.

14. Dale O, Hoffer C, Sheffels P, et al. Disposition of nasal, intravenous, and oral methadone in healthy volunteers. Clin Pharmacol Ther. 2002;72:536Y545.

24. Gagajewski A, Apple FS. Methadone-related deaths in Hennepin County, Minnesota: 1992Y2002. J Forensic Sci. 2003;48:668Y671.

15. Karch SB, Stephens BG. Toxicology and pathology of deaths related to methadone: retrospective review. West J Med. 2000;172:11Y14.

25. Caplehorn JR, Drummer OH. Fatal methadone toxicity: signs and circumstances, and the role of benzodiazepines. Aust N Z J Public Health. 2002;26:358Y362; discussion 362Y363.

16. Baselt RC, Casarett LJ. Urinary excretion of methadone in man. Clin Pharmacol Ther. 1972;13:64Y70. 17. Bellward GD, Warren PM, Howald W, et al. Methadone maintenance: effect of urinary pH on renal clearance in chronic high and low doses. Clin Pharmacol Ther. 1977;22:92Y99. 18. Wolff K. Characterization of methadone overdose: clinical considerations and the scientific evidence. Ther Drug Monit. 2002;24:457Y470. 19. Caplehorn JR, Drummer OH. Methadone dose and post-mortem blood concentration. Drug Alcohol Rev. 2002;21:329Y333. 20. Cruciani RA, Sekine R, Homel P, et al. Measurement of QTc in patients

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26. Baker DD, Jenkins AJ. A comparison of methadone, oxycodone, and hydrocodone related deaths in Northeast Ohio. J Anal Toxicol. 2008;32:165Y171. 27. Gordon AM, Loew S, Logan BK. Methadone concentrations and concurrent drug finding in three populations; methadone treatment patients, impaired drivers, and death investigation cases. Proc Am Ac Forensic Sci. 2004;10:368Y369. Abstract K39. 28. Centers for Disease Control (CDC). QuickStats: age-adjusted death rates per 100,000 population for the three leading causes of injury deathVUnited States, 1979Y2006. MMWR Morb Mortal Wkly Rep. 2009;58:675.

* 2011 Lippincott Williams & Wilkins

BOOK REVIEW

‘‘Beating the Devil’s Game: A History of Forensic Science and Criminal Investigation’’ Katherine Ramsland, PhD. Beating the Devil_s Game: A History of Forensic Science and Criminal Investigation. New York: Berkley Books

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atherine Ramsland_s book, Beating the Devil_s Game: A History of Forensic Science and Criminal Investigation, takes the reader on a scintillating journey revealing the history and development of the forensic sciences. The journey starts with ancient Egypt and carefully weaves through time, sharing a who_s who of international scientific investigators who contributed to

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the various specialties in medicolegal investigations. Along the way, the reader is introduced to the criminals and their victims that highlight the application of the sciences to legal proceedings at that time. The famous, infamous, and not so well-known persons mentioned make this book interesting and very easy to read despite the amount of information shared. Characters such as Francois Eugene Vidocq, who was born in France in 1775, started as a petty criminal and enjoyed escaping prisons but later worked with the police and started the first undercover detective agency. Did you know that Mary Ann BPolly[ Nichols and Annie Chapman were Jack the Ripper_s first known victims? You may recognize the names Watson and Crick

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for their work identifying the structure of DNA but did you know that Frederick Miescher, a Swiss biologist, isolated DNA for the first time in 1869? Or that the first private scientific crime detection laboratory was created by Calvin Goddard as a result of the St. Valentine_s Day Massacre in 1929 and preceded the FBI_s crime laboratory? Her extensive research is evident in the substantial bibliography that one may find useful in preparation for lectures and individual publication projects or as a guide for future personal reading.

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Ruth E. Kohlmeier, MD El Paso County Coroner_s Office Colorado Springs, CO, USA [email protected]

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LETTER TO

Proposed Ocular Autopsy Protocol To the Editor: aving heard Gilliland’s presentation entitled, ‘‘Use of the Triad of Scant Subdural Hemorrhage, Brain Swelling, and Retinal Hemorrhages to Diagnose Nonaccidental Injury Isn’t Scientifically Valid,’’ concluding ‘‘use of the triad to diagnose shaken baby syndrome is unscientific’’ (NAME 2006 annual meeting. Copy of abstract available from horacebgardner@ yahoo.com), it was surprising to see so many articles references in the recently proposed ‘‘Guidelines,’’1 which are contaminated by just such cases and thus also ‘‘unscientific.’’ Although more complete pathology is a laudable goal, costeffectiveness is also important. Because

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no ocular hemorrhage has been produced by indirect mechanical methods (shaking, acceleration/deceleration), much less a unique pattern of hemorrhage (hemorrhage in multiple ocular tissuesVorbital, intraocular, optic nerveVhas been shown to occur without such mechanical forces2), it is unwise to target the eye pathology at any particular pattern of hemorrhage. Noting we have no adequate experimental models, Emerson et al3 conclude ‘‘much of what we think we know about the systemic and ocular findings of child abuse will continue to be the result of speculation rather than based on sound evidence.’’ The protocol suggested by Gilliland et al1 is likely to muddy the waters even more rather than clarify them. Without definite cases of ‘‘abuse’’ and adequate controls, speculating that any autopsy finding or set of findings to be diagnostic of nonaccidental injury may lead to more problems than it will

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solve. These guidelines may be very helpful in just such a controlled, scientific study, but their use should not be used to diagnose ‘‘abuse.’’ Horace B. Gardner, MD Manitou Springs, CO [email protected]

REFERENCES 1. Gilliland MGF, Levin AV, Enzenauer RW, et al. Guidelines for postmortem protocol for ocular investigation of sudden unexplained infant death and suspected child abuse. Am J Forensic Med Pathol. 2007;28:323Y329. 2. Walsh FB, Hedges TR. Optic nerve sheath hemorrhage. Am J Ophthalmol. 1951;34:509Y527. 3. Emerson MV, Jakobs E, Green WR. Ocular autopsy and histopathologic features of child abuse. Ophthalmology. 2007;114: 1384Y1394.

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LETTER TO

Russian Roulette Deaths

To the Editor: e read with interest the article by Shields et al,1 ‘‘Russian Roulette and Risk-Taking Behavior.’’ They describe 24 Russian roulette deaths and provide an insightful discussion of the challenge of certifying the manner of these deaths. For the sake of achieving uniformity, the authors recommend that all Russian roulette deaths be certified as suicides. We respectfully disagree. Russian roulette deaths should be evaluated individually and certified accordingly. Certain guidelines should be followed to maintain consistency and objectivity, but

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this is not a substitute for good judgment. Consistency is best maintained by adherence to the definition of suicide. The key factor in determining that a death is suicidal is not just that the act was intentional, but that the decedent performed this act with the intent to cause his/her death.2 This hurdle is what makes suicide one of the most challenging manners to certify. In our experience, some deaths from Russian roulette do not meet the defining criterion of ‘‘intentional self-destruction.’’ Even the authors acknowledge that the intent to die is not present in some cases. Deaths that do not meet this criterion are appropriately certified as accidents or, in some instances, left undetermined. The authors equate extreme risk-taking behavior

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with suicidal intent. One hazard of this approach is that the definition of ‘‘extreme risk-taking behavior’’ is open to interpretation and ultimately may result in nonuniform, seemingly arbitrary decisions. James R. Gill, MD Charles S. Hirsch, MD New York City Office of Chief Medical Examiner New York, NY [email protected]

REFERENCES 1. Shields LBE, Hunsaker JC, Stewart D. Russian roulette and risk-taking behavior. Am J Forensic Med Pathol. 2008;29:32Y39. 2. Rosenberg ML, Davidson LE, Smith JC, et al. Operational criteria for the determination of suicide. J Forensic Sci. 1988;33:1445Y1456.

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LETTER TO

In Response to ‘‘Suicide and Ethnicity in Malaysia’’ Reply: he source population for the study arose from deaths due to suicide being brought to University Malaya Medical Centre for autopsy. It may be possible that these deaths resulted from a community that had predominant majority of Chinese, Indians, and Malaya in that order, and hence the authors might have got correlations of suicide rates as they got in their study.1 At the best, it might be inferred that this correlation might establish some association but would not confer any validity to make causal associations akin to what has been tried in the article. I strongly disagree with the statement ‘‘in contrast, some races, like Indian, glorified the act of suicide in the form of ‘sati,’’’ mentioned in the discussion section of the article for reasons mentioned below. First, it is unclear on how authors can make detailed discussions of ethnicity/ race as a factor and yet quote Quran for low incidence of suicides in Malay population. I presume that ethnicity, race, and religion are used as interchangeable terms in this study, which cannot be acceptable. This is because each of these terms has distinct definitions depicting their inherent risk pattern due to various determinants.2 If the authors really mean ‘‘religion’’ as a factor, it has to be noted that India (and not Malaysia) has the second largest Muslim population in the world next to Indonesia.3 The authors fail to demonstrate composition of various religions among their study autopsies and yet discuss the holy Quran as a preventive remedy for suicide. It is

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also not known whether referring the Indians is synonymous with terming them as Hindus or whether some proportion of Indians were also Muslims residing in Malaysia. Their argument that Indian race glorifies suicide fails from even religious point of view. Second, ‘‘the suicidal behavior in India seems to be less common than in many other nations in Asia, lower than the rate in China, and much lower than the rate in neighboring Sri Lanka.’’ Furthermore, ‘‘based on the results of conducting interviews with Indian professionals by Tousignant, Seshadri, and Raj, it was found that Indian society was not very tolerant of suicide, viewing it as an act of cowardice and betrayal of friends and relatives.’’4 Finally, the reasons and methods adopted for suicide are different for males and females in India.5Y8 The reasons include financial burden, marital disharmony, and many others apart from the otherwise emphasized sati system.5Y8 But the authors report that hanging was a predominant reason for suicide among Indians in Malaysia, indicating that the sample was not representative of Indians in their study population. According to their study, the authors did not find any reporting of sati being reason for committing suicide by Indians in Malaysia. Based on the data they have, it is unclear how sati practice practiced in ancient times in India is a reason for influencing modern-day Indians in committing suicide by hanging. Hence, it might be highly biased to infer that Indian race encourages and glorifies suicides. In the absence of data on reasons for suicides, authors have resorted to present biased, quasi-philosophical, and one-sided opinion in generalizing their study, which suffers from lack of precise source popu-

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lation, marred by small numbers resulting in distortion of associations. Giridhara R. Babu, MBBS, MPH MBA, PhDc Department of Epidemiology University of California Los Angeles, CA and Public Health Foundation of India Indian Institute of Public Health - Hyderabad Hyderabad, India [email protected]

REFERENCES 1. Om Prakash M, Lo Boon C, Pangie Anak B, et al. Suicide and ethnicity in Malaysia. Am J Forensic Med Pathol. 2008;29(1):19Y22. 2. Bhopal R. Glossary of terms relating to ethnicity and race: for reflection and debate. J Epidemiol Community Health. 2004;58: 441Y445. 3. Zissis C. India’s Muslim population. Council on Foreign Relations. Available at: www.cfr.org/publication/13659/ indias_muslim_population.html. Accessed April 12, 2008. 4. Lester D, Agarwal K, Natarajan M. Suicide in India. Arch Suicide Res. 1991;5(2): 381Y1118. 5. Girdhar S, Dogra TD, Leenaars AA. Suicide in India, 1995Y1999. Arch Suicide Res. 2003;7(4):389Y393. 6. Mohanty S, Sahu G, Mohanty MK, et al. Suicide in IndiaVa four year retrospective study. J Forensic Legal Med. 2007;14(4): 185Y189. 7. Gajalakshmi V, Peto R. Suicide rates in rural Tamil Nadu, South India: verbal autopsy of 39 000 deaths in 1997Y1998. Int J Epidemiol. 2007;36(1):203Y207 8. Joseph A, Abraham S, Muliyil JP, et al. Evaluation of suicide rates in rural India using verbal autopsies, 1994Y9. BMJ. 2003;326: 1121Y1122.

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