Frequency of Sternal Variations and Anomalies Evaluated by MDCT

M u s c ul o s kel et a l I m ag i n g • C l i n i c a l O b s e r v a t i o n s

Yekeler et al. Frequency of Sternal Variations and Anomalies

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C E N T U R Y

MEDICAL

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IMAGING

Ensar Yekeler1 Mehtap Tunaci Atadan Tunaci Memduh Dursun Gulden Acunas Yekeler E, Tunaci M, Tunaci A, Dursun M, Acunas G

Frequency of Sternal Variations and Anomalies Evaluated by MDCT OBJECTIVE. Our objective was to reveal the frequency and MDCT appearances of sternal variations and anomalies in subjects without sternal deformities. SUBJECTS AND METHODS. One thousand consecutive patients who underwent thoracic MDCT examination were enrolled in the study. All MDCT data, including multiplanar and curved-planar reconstructed images, were evaluated for detection of sternal variations and anomalies. Various kinds of sternal variations and anomalies, such as suprasternal bones and tubercles, manubriosternal and sternoxiphoidal fusions, sternal clefts and foramina, and sternal sclerotic bands were documented. RESULTS. In 1,000 subjects, the frequencies of main sternal variations and anomalies were as follows: suprasternal bone in 4.1%, suprasternal tubercle in 4%, complete manubriosternal fusion in 19.6%, complete sternoxiphoidal fusion in 30.3%, sternal foramen in 4.5%, and sternal sclerotic band in 37.1%. Xiphoidal foramen was seen in 27.4%, and the most common type was single foramen. Xiphoid process mostly ended as a single process (71%). Double-ended xiphoid process was also frequent (27.2%). Pseudocleft and pseudoforamen at the sternoxiphoidal junction were detected in 3.3% and in 3.6% of subjects, respectively. CONCLUSION. MDCT exhibited various sternal variations and anomalies. Sternal foramen is a frequent minor anomaly and generally associated with sternal sclerotic bands. Early manubriosternal and sternoxiphoidal fusions can be seen in early adulthood without osteodegeneration. Double-ended xiphoid process and single xiphoidal foramen are frequent sternal variations. Awareness of MDCT appearances of sternal variations and anomalies provides a better differential diagnosis with pathologic conditions. uman skeletons have many variations that may occasionally necessitate distinction from pathologic changes. The sternum is one of the skeleton parts with frequent variation in appearances on images or autopsy series. In living subjects, sternal variations are frequently detected incidentally on cross-sectional images. Knowledge of radiologic appearances of sternal variations and anomalies is useful so as to not confuse those with pathologic conditions. Awareness of a sternal foramen is important in acupuncture practice and sternal marrow aspiration because of the danger of heart damage [1]. The largest series evaluating sternal variations and anomalies were based on macroscopic [2] and radiographic [3] appearances of the sternum in autopsy populations. The frequencies of sternal anomalies in living subjects have been described based on their radiograph [4, 5], helical CT [6, 7], or MRI

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Keywords: anomalies, developmental, MDCT, musculoskeletal imaging DOI:10.2214/AJR.04.1779 Received November 17, 2004; accepted after revision February 9, 2005. 1All authors: Department of Radiology, Istanbul University,

Istanbul Faculty of Medicine, Millet Cad. Capa, Istanbul 90, Turkey 34390. Address correspondence to E. Yekeler ([email protected]). AJR 2006; 186:956–960 0361–803X/06/1864–956 © American Roentgen Ray Society

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[8] appearances. In those studies, the number of subjects and the kinds of investigated variations and anomalies are limited. Threedimensional imaging by helical CT was used in the evaluation of anterior chest wall deformities during childhood without focusing on the sternum by 3D or multiplanar imaging [9]. Three-dimensional CT images of the sternum were obtained in a few cases with sternal anomalies, such as complete sternal cleft [10]. Multiplanar and 3D reconstructed CT images are useful in the evaluation of the human skeleton, especially in complex parts such as the skull base, shoulder, and sternum. To our knowledge, the sternum has not been studied by MDCT for variations and anomalies. The purpose of this investigation was to reveal the frequency and MDCT appearances of sternal variations and anomalies in an adult population with no obvious sternal deformities.

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Fig. 1—40-year-old man with suprasternal bone. Coronal maximum-intensity-projection MDCT image shows suprasternal bones fused with each other in midline (arrow).

Fig. 2—70-year-old man with suprasternal tubercle and manubriosternal and sternoxiphoidal fusions. Coronal curved-planar reconstructed MDCT image reveals complete manubriosternal and sternoxiphoidal fusions and right suprasternal tubercle (arrow).

Fig. 3—48-year-old man with manubrial cleft and sclerotic band. Coronal multiplanar reconstructed MDCT image shows superior manubrial cleft (arrowheads), continuing inferiorly with sclerotic band (arrows).

Subjects and Methods Patient Population

bronchoscopic evaluations, thinner collimation and slice thickness values were selected. All patients underwent imaging from the thoracic inlet superiorly to the level of the adrenal glands inferiorly, including the sternum within the imaging area.

and cleft, xiphoidal ligament calcification, and pseudocleft and pseudoforamen due to incomplete manubriosternal or sternoxiphoidal fusion.

Over an 8-month period, patients who underwent thorax MDCT examination were included in the study. Medical records of the patients were available at the time the MDCT examination was performed. The study protocol was approved by the institutional review board, and informed consent was obtained from the patients who enrolled in the study. Thorax MDCT examinations were performed for many reasons, such as to investigate primary or metastatic tumors, vascular and airway pathologies, to follow up on known pulmonary lesions, or to evaluate lung opacities detected on chest radiography. After excluding patients with sternal deformity, a history of thoracic trauma or surgery, sternal mass, or infiltration, MDCT images of 1,000 consecutive patients (582 men and 418 women; age range, 20–92 years; mean age, 54 years) were evaluated for detection of incidental sternal variations and anomalies. Patients who underwent repeated thoracic MDCT examinations were enrolled in the study only once.

MDCT Protocol MDCT imaging was performed with a four-detector row CT scanner (Somatom Sensation 4, Siemens Medical Solutions). Common scanning parameters for all patients were as follows: 120 kVp, 90 mAs, 0.5-sec gantry rotation, 4 × 2.5-mm collimation, pitch of 6 (4 × 1.5), 30-mm/sec table feed, and 2-mm axial and 3-mm multiplanar reconstruction image thicknesses. For CT angiographic and

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Image Analysis Analyses of the image data were based on axial and reformatted images. All data were postprocessed with a commercially available workstation (Leonardo, Siemens Medical Solutions). In all subjects, after evaluation of axial images, sagittal and coronal multiplanar reconstruction and maximum intensity projection (MIP) images were obtained. Since the sternum is angulated at manubriosternal and sternoxiphoidal junctions, coronal curved-planar multiplanar reconstruction and MIP images were also obtained in all subjects to show the sternum at full length. Two radiologists evaluated the images at the same time with a consensus for the presence of sternal variations and anomalies in the following areas: suprasternal bone (accessory ossicle at the superior margin of the manubrium), suprasternal tubercle (suprasternal bone fused with the manubrium), manubriosternal and sternoxiphoidal fusion, sternal sclerotic band at the junction of fused sternal pairs, sternal cleft (congenital vertical defect of the sternum), sternal foramen (round defect at the lower third of the sternum), focal defect of sternal cortex and sternal notch, types of xiphoidal ending (absence; single, double, or triple ending), types of xiphoidal ossification (superior, complete, or partial), xiphoidal foramen

Results The sternal variations and anomalies depicted on axial and multiplanar reconstructed images were documented. Suprasternal Bone and Suprasternal Tubercle Suprasternal bones were found in 41 (4.1%) subjects (22 bilateral, 18 unilateral, one midline). Suprasternal bones fused with each other in the midline were seen in only one subject (Fig. 1). Suprasternal tubercle was detected in 40 (4%) subjects (27 bilateral and 13 unilateral) (Fig. 2). Manubriosternal and Sternoxiphoidal Fusions Manubriosternal and sternoxiphoidal fusions were determined as partial or complete. Manubriosternal fusion was partial in 100 (10%) subjects and complete in 196 (19.6%) subjects (Fig. 2). Incomplete and complete sternoxiphoidal fusions were found in 324 (32.4%) and 303 (30.3%) subjects, respectively. Complete fusion at both manubriosternal and sternoxiphoidal junctions was encountered in a patient as young as 20 years, without findings of osteodegeneration; 20% of the subjects with partial or complete manubriosternal and sternoxiphoidal fusion were younger than 45 years (Fig. 2).

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Fig. 4—60-year-old woman with sternal foramen and sclerotic band. Coronal multiplanar reconstructed MDCT image shows sternal foramen in inferior sternal body associated with sternal sclerotic band (arrows).

Fig. 5—21-year-old man with sternal foramen and cleft. Coronal maximum-intensity-projection MDCT image depicts sternal foramen in inferior sternal body, continuing inferiorly with sternal cleft (arrows).

Fig. 6—60-year-old woman with sternal notch. Axial MDCT image shows notch at posterior cortex of inferior sternal body similar to recently closed sternal foramen (arrow).

Sternal Sclerotic Band and Cleft Vertical sclerotic bands seen at the junction of the fused sternal pairs were highly frequent (37.1%; 11.1% in the manubrium, 17.8% in the corpus, and 8.2% in both the manubrium and corpus). Manubrial sclerotic bands were mostly (61.6%) located in the superior portion (Fig. 3). The majority (77.3%) of the sternal bands in the corpus were located in the inferior part (Fig. 4). Sclerotic band was not found in the xiphoid process. Manubrial cleft was depicted in six subjects (0.6%). All were in the superior portion of the manubrium and five (83.3%) were associated with a manubrial sclerotic band just inferior in relation to the cleft (Fig. 3). Sternal cleft located in the corpus was detected in eight (0.8%) subjects (size range, 5–26 mm; mean size, 13 mm) and all were in the inferior part of the sternal body (Fig. 5).

Focal Defect of Sternal Cortex and Sternal Notch Focal defect or notch of the sternal cortex was found in 77 (7.7%) subjects. The majority (68.8%) of those were seen in the posterior cortex of the inferior sternal body. In one subject with a sternal notch in the inferior portion of the sternal body, the appearance was similar to a recently closed sternal foramen (Fig. 6).

Xiphoidal Ligament Calcification Unilateral or bilateral xiphoidal ligament calcification was detected in 101 (10.1%) subjects (Fig. 10). In five subjects with xiphoidal ligament calcification, xiphoidal ossification was not completed. The majority of the xiphoidal ligament calcifications (79.2%) were identified in patients older than 50 years.

Xiphoidal Ending and Ossification Xiphoid was absent in 11 subjects (1.1%; age range, 20–53 years; mean age, 27 years). Xiphoidal endings were three types: a single(71%), double- (27.2%), or triple-ended (0.7%) xiphoid process (Fig. 7). In five subjects with a single-ended xiphoid process, the xiphoid was longer than usual (Fig. 8). Xiphoidal ossification was not depicted in 23 subjects (2.3%; age range, 20–86 years; mean age, 39 years). The majority of the subjects without xiphoidal ossification (61%) were under 30 years. Xiphoidal ossification was total in 70.3%, superior in 23.9%, superior and inferior but partial in 4.8%, and middle in 1%.

Sternal Pseudoclefts and Pseudoforamina Because of incomplete fusion at manubriosternal and sternoxiphoidal junctions, one pseudoforamen at the manubriosternal junction and 33 (3.3%) pseudoclefts and 36 (3.6%) pseudoforamina at the sternoxiphoidal junction were depicted (Figs. 11 and 12). Mild tilt of the sternum was found in 34 (3.4%) subjects. Asymmetric concavity of the sternal contours was depicted in only one subject. Nonfused superior and inferior sternal pairs were observed in nine subjects.

Sternal Foramen None of the subjects had a foramen in the manubrium. Sternal foramen located in the corpus was found in 45 (4.5%) subjects. All were present in the inferior part of the sternal body. The size of sternal foramina ranged between 2 and 16 mm (mean, 6.5 mm). Sternal cleft adjacent to the foramen was identified in only one case (Fig. 5). However, vertical sclerotic band just superior or inferior in relation to the sternal foramen was identified in 33 (73%) of 45 subjects (Fig. 4).

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Xiphoidal Foramen and Cleft Xiphoidal foramina were more frequent than those located in the sternal corpus. In 274 (27.4%) subjects, a total of 305 xiphoidal foramina (one foramen in 246 subjects, two foramina in 25 subjects, and three foramina in three subjects) were found (Fig. 9). Xiphoidal cleft was found in 19 (1.9%) subjects.

Discussion The sternum develops from a pair of longitudinal mesenchymal condensations, the sternal bars that form in the ventrolateral body wall. As most cranial ribs make contact with them in the seventh week, the sternal bars meet along the midline and begin to fuse. Fusion commences at the cranial end of the sternal bars and progresses caudally, finishing with the formation of the xiphoid process in the ninth week. Like the ribs, the sternal bones ossify from car-

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Fig. 7—35-year-old man with triple-ended xiphoid processes. Coronal maximum-intensity-projection MDCT image shows triple ending of xiphoid processes.

Fig. 8—60-year-old man with long xiphoid process. Coronal maximum-intensity-projection MDCT image shows xiphoid process longer than usual.

Fig. 9—54-year-old man with xiphoidal foramina. Coronal maximum-intensity-projection MDCT image illustrates xiphoid process with three foramina.

tilaginous precursors. The sternal bars ossify in the craniocaudal succession from the fifth month until shortly after birth, producing the definitive bones of the sternum: the manubrium, the body, and the xiphoid process [11]. Any failure in this developmental process results in various sternal anomalies, such as fissure or foramen [1–3]. Fusion of the inferior end of the sternum is sometimes incomplete, resulting in a bifid or perforated xiphoid process [12]. Serious complications after sternal puncture for bone morrow biopsy [13, 14] or acupuncture [14] have been reported in the literature. Fatal cardiac tamponade resulting from a congenital sternal foramen located in the inferior part of the sternum [13, 15] and thin sternal body [14] was seen during the sternal puncture. Therefore, the awareness of the presence of sternal variations and anomalies is important to prevent these fatal complications by avoiding the inferior part of the sternal body during bone marrow aspiration. To be familiar with the imaging appearances of the sternal variation and anomalies, it is necessary to differentiate those from pathologic conditions, such as traumatic fissure or fracture and lytic lesions. Absence of cortical irregularity, expansion, and soft-tissue mass can be taken into consideration in the differentiation. It is difficult to visualize sternal variations and anomalies by radiography. Therefore, cross-sectional imaging such as CT and MRI is generally required to describe the findings detected on radiography and to reveal the addi-

tional minor changes. CT with multiplanar reconstruction may show relevant anatomic detail of sternal variations and anomalies. The largest series describing sternal anomalies examined 2,016 plastron radiographs in an autopsy population [3] and 562 radiographs in living subjects [4]. In the largest living subject series using CT as a cross-sectional imaging method, 140 subjects were evaluated to determine the incidence of sternal foramen [6]. The superiorities of the current study to previous studies are as follows: describing multiplanar MDCT appearances of sternal variations and anomalies, studying the largest living subject population (1,000 living subjects), and comprehensively evaluating sternal variations and anomalies. Multiplanar reconstructed MDCT images were helpful in wholly revealing sternal anatomy. Curved-planar coronal multiplanar reconstruction images nicely showed manubriosternal and sternoxyphoidal fusions, sternal bands and clefts, sternal and xiphoidal foramina, the types of xiphoidal ending, and xiphoidal ossification. Suprasternal bone is an unfamiliar normal variation in the vicinity of the sternoclavicular joint. It may occur singly or paired at the superior margin of the manubrium. Suprasternal tubercle is considered to be the osseously fused type of suprasternal bone [4]. In a study by Ogawa et al. [4], eight (10.8%) suprasternal bones and 14 (18.9%) suprasternal tubercles were found in 74 cadavers. Among them, three had suprasternal bone and tubercle on each side.

In the same study including 562 living subjects, 39 cases (6.9%) had suprasternal bones and eight cases (1.4%) had suprasternal tubercles. Among them, three had both on each side. The incidence of suprasternal bones was lower in our study than their study result (4.1% vs 6.9%). The frequency of suprasternal tubercles in our subjects was lower than in their cadaver population (4% vs 18.9%) but markedly higher than their living subject population (4% vs 1.4%). We did not detect suprasternal bone and tubercle on each side. However, suprasternal bones fused with each other are described to our knowledge for the first time in our study (Fig. 1). In the present study, 20% of the subjects with complete manubriosternal and sternoxiphoidal fusion were younger than 45 years, and complete fusion in both locations was detected in patients as young as 20 years without osteodegeneration at the junction. These findings suggest that the complete fusion without osteodegeneration could be due to the developmental fusion of manubriosternal and sternoxiphoidal junctions similar to those of vertical sternal pairs. Sternal cleft is a rare congenital defect of the anterior chest wall and is the result of a failed midline fusion of the sternum. There are complete and incomplete forms depending on the degree of separation. The clinical significance is that it leaves the heart and great vessels unprotected [1]. In the present study, complete sternal cleft was not observed. All incomplete sternal clefts were lo-

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Fig. 10—58-year-old man with xiphoidal ligament calcification. Coronal maximum-intensity-projection MDCT image depicts bilateral xiphoidal ligament calcifications (arrows).

Fig. 11—58-year-old woman with sternoxiphoidal pseudocleft. Coronal multiplanar reconstructed MDCT image shows pseudocleft at incomplete fused sternoxiphoidal junction (arrow).

Fig. 12—56-year-old man with sternoxiphoidal pseudoforamen. Coronal multiplanar reconstructed MDCT image shows complete fusion at sternoxiphoidal junction except small pseudoforamen (arrow).

cated in the inferior part of the sternal body as the sternal foramina. Sternal foramen is a round defect at the lower third of the sternum and the result of incomplete fusion of multiple ossification centers. It is usually asymptomatic and could be detected by CT incidentally [7]. Cooper et al. [2] found sternal foramina in 6.7% of a large contemporary autopsy population. These sternal foramina were usually solitary and located in the body of the sternum. They also detected a foramen in the manubrium. Similar results were found by Moore et al. [3]. They detected 135 (6.6%) sternal foramina on plastron radiographs from 2,016 radiographs in an autopsy population. Stark [6] detected six (4.3%) cases of a midline sternal foramen on the chest CT of 140 cases. The percentage of sternal foramina detected in our subjects was slightly higher than in Stark’s study result (4.5% vs 4.3%). Triple-ended xiphoid process (Fig. 7) and three xiphoidal foramina (Fig. 9) were first described in the present study. Sternal sclerotic bands at the fusion site of sternal pairs were highly frequent in those subjects with a sternal foramen (Fig. 4). Pseudocleft and pseudoforamen terms for the sternum were first used in our study because these clefts or foramina depicted on reconstructed MDCT images were observed at the incomplete fused manubriosternal or sternoxiphoidal junctions.

In conclusion, the sternum has various variations and anomalies. The sternal foramen is a frequent minor anomaly and generally associated with sternal sclerotic bands. Early manubriosternal and sternoxiphoidal fusions can be seen in early adulthood without osteodegeneration. A double-ended xiphoid process is a frequent variation and a triple-ended xiphoid process has been described for the first time to our knowledge in the present study. A xiphoidal foramen is a highly frequent variation and a single foramen is the most common type. Multiplanar and curved-planar reconstructed MDCT images are useful in revealing sternal anatomy and describing sternal variations and anomalies. Awareness of MDCT appearances of sternal variations and anomalies provides a better differential diagnosis with pathologic conditions.

Seikeigeka Gakkai Zasshi 1979; 53:155–164 5. Keats TE, Anderson MW. Atlas of normal roentgen variants that may simulate disease, 7th ed. Chicago, IL: Year Book, 2001:438–449 6. Stark P. Midline sternal foramen: CT demonstration. J Comput Assist Tomogr 1985; 9:489–490 7. Schratter M, Bijak M, Nissel H, Gruber I, SchratterSehn AU. The foramen sternale: a minor anomaly— great relevance [in German]. Rofo 1997; 166:69–71 8. Haje SA, Harcke HT, Bowen JR. Growth disturbance of the sternum and pectus deformities: imaging studies and clinical correlation. Pediatr Radiol 1999; 29:334–341 9. Donnelly LF, Frush DP, Foss JN, O’Hara SM, Bisset GS 3rd. Anterior chest wall: frequency of anatomic variations in children. Radiology 1999; 212:837–840 10. Biswas G, Khandelwal NK, Venkatramu NK, Chari PS. Congenital sternal cleft. Br J Plast Surg 2001; 54:259–261 11. Larsen WJ. Human embryology, 2nd ed. New York, NY: Churchill Livingstone, 1997:77–78 12. Moore KL, Parsaud TVN. The developing human, 5th ed. Philadelphia, PA: Saunders, 1993:360 13. Wolochow MS. Fatal cardiac tamponade through congenital sternal foramen. Lancet 1995; 346:442 14. Bhootra BL. Fatality following a sternal bone marrow aspiration procedure: a case report. Med Sci Law 2004; 44:170–172 15. Halvorsen TB, Anda SS, Naess AB, Levang OW. Fatal cardiac tamponade after acupuncture through congenital sternal foramen. Lancet 1995; 345:1175

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