International Journal of Osteopathic Medicine- Volume 14, Issue 1 (March 2011)

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Author: Nicholas Lucas | Robert Moran & Steven Vogel

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Find us on the web: www.intl.elsevierhealth.com/journals/ijos For the complete Guide for Authors please visit www.elsevier.com/ijos Editorial Office: [email protected]

Editors Nicholas Lucas BSc(ClinSci), MHSc(Osteo), MPainMed, Grad Dip Clin Epi Sydney School of Public Health, The University of Sydney, Sydney, Australia Robert Moran BSc, BSc(ClinSci), MHSc(Osteo) Department of Osteopathy, Unitec New Zealand, Auckland, New Zealand Steven Vogel DO The Research Centre The British School of Osteopathy London, UK Editorial Advisor Ann Moore PhD, Grad Dip Phys, Dip TP, FCSP, FMACP, Cert Ed, ILTM School of Health Professions, University of Brighton, East Sussex, UK Editorial Office Journal Manager, International Journal of Osteopathic Medicine, Health Sciences, Elsevier, The Boulevard, Langford Lane, Kidlington, Oxford, OX5 1GB, UK Fax: +44 (0) 1865 843923 Email: [email protected] Book Review Editor Carol Fawkes DO, Lic Ac University of Brighton, East Sussex, UK Editorial Board Peter Gibbons MBBS, DO, DMS-Med, MHSc School of Health Sciences, Victoria University, Melbourne, Australia Janine Leach BSc, PhD, ND, DO, HonMFPH, School of Health Professions, University of Brighton, East Sussex, UK

Michael Patterson PhD College of Osteopathic Medicine (Retired), NOVA Southeastern University, Florida, USA Tamar Pincus BSc, MSc, MPhil, PhD Department of Psychology, Royal Holloway University of London, London, UK International Advisory Board J Louise Adam (NSW, Australia) Peter Baziotis (NSW, Australia) Leon Chaitow (London, UK) Brian Degenhardt (CO, USA) Vincent Di Stefano (VIC, Australia) Ian Drysdale (London, UK) Jorge Esteves (Oxford, UK) David Evans (Birmingham, UK) Ryan Everitt (NSW, Australia) Paula Fletcher (Kent, UK) Nadine Foster (Staffordshire, UK) Christian Fossum (Kent, UK) Gary Fryer (VIC, Australia) Grégoire Lason (Gent, Belgium) Eyal Lederman (London, UK) John Licciardone (TX, USA) Torsten Liem (Hamburg, Germany) Brad McCutcheon (Ontario, Canada) Christopher McGrath (Dunedin, New Zealand) John McPartland (VT, USA) Massimo Musicco (MiIan, Italy) Kate Nash (Ottawa, Canada) Elizabeth Niven (Auckland, New Zealand) Nicholas Penney (QLD, Australia) Graham Sanders (QLD, Australia) Florian Schwerla (Gating, Germany) Peter Sommerfeld (Korneuburg, Austria) Clive Standen (Auckland, New Zealand) Andrew Stewart (Auckland, New Zealand) Philip Tehan (VIC, Australia) Martin Underwood (Warwick, UK) Brett Vaughan (VIC, Australia) Nick Walters (London, UK) Heather Wheat (VIC, Australia) Frank Willard (ME, USA)

Official journal of the Australian Osteopathic Association, the General Osteopathic Council (UK) and the Ontario Association of Osteopaths, and recognised by the British Osteopathic Association. Amsterdam • Boston • London • New York • Oxford • Paris • Philadelphia • San Diego • St Louis

International Journal of Osteopathic Medicine 14 (2011) 1–2

Contents lists available at ScienceDirect

International Journal of Osteopathic Medicine journal homepage: www.elsevier.com/ijos

Editorial

Bringing fresh perspective to muscle energy technique

Seven years ago, we wrote an editorial called “The Seven Year Itch”. Another seven years later and our message is the same: the profession of osteopathy and the patients it serves would beneﬁt from a greater understanding of how to provide accurate diagnoses more of the time, and how to implement treatment that is as efﬁcacious as possible. While keeping that goal in mind the journal also continues to publish a wide variety of papers and the contents of this issue are a typical example of the broad interests present within the readership.

experience. Those familiar with the literature will know that studies have shown palpation of the CRI to be unreliable, and this study, while not a study of diagnostic reliability, reports that each group tended to record a different CRI rate. For those readers who employ treatment based on OCF concepts, this paper will be of interest for its redeﬁning of normative rate. For those readers who prefer their palpatory phenomenon served up with a basis of objective measurement the paper is unlikely to move them any closer towards acceptance of the model.

Masterclass – an evidence informed update on muscle energy technique

Helical tensegrity and the geometry of anatomy

Fryer’s masterclass on muscle energy technique in this edition is a great example of the profession organising itself and its knowledge base. While it is difﬁcult to change the everyday behaviour of practising osteopaths, it is (perhaps) an easier task to help them understand how current knowledge does, or does not, support that behaviour. We are fortunate to have members of the profession who are dedicated to synthesising the current knowledge for us and providing us with interpretation. In his article, which we highly recommend that you read, Fryer provides a straightforward summary of ‘evidence informed practice’ - a concept that we believe many readers will appreciate as it strikes a balance between what is possible and what is practical. He then applies his description of evidence informed practice to the topic of muscle energy technique. While this paper only reﬂects a snapshot of the detailed information that applies to this area, it is sufﬁciently deep to quickly bring you up to date. The paper also includes a few direct challenges to the status quo for anyone involved in teaching MET and we hope readers will enjoy the absence of the familiar dogma often associated with MET teaching texts and the freshness of statements such as “Sacroiliac dysfunctions proposed by Mitchell are clinical constructs, rather than deﬁnitive clinical entities” or “Practitioners should not assume every asymmetrical pelvis is dysfunctional and warrants treatment”. A revised look at normative rate in OCF.more fuel for the debate? We also publish the ﬁndings of a study investigating the rate of the cranial rhythmic impulse. Sergueef and colleagues performed a retrospective review of 734 study participants, examined by practitioners with different levels of experience. The results are presented in terms of the palpated rate of the CRI reported by the examiners in three groups, being 1, 2, or 3 to 25-years of 1746-0689/$ – see front matter Ó 2011 Published by Elsevier Ltd. doi:10.1016/j.ijosm.2011.02.001

Also in this issue is a critical review of helical tensegrity as it relates to human anatomy by Scarr. ‘Tensegrity’ (a portmanteau of ‘tension-integrity’) seems to be attracting growing interest amongst authors from the manual therapy and bodywork disciplines interested in the structural biology of connective tissues – particularly those investigating the biological and clinical significance of fascia. Tensegrity has also been mentioned in various osteopathic texts and may provide a useful approach to viewing the musculoskeletal system other than classical Newtonian mechanics. Scarr reviews the structural mechanism of tensegrity as a potential explanation for the integration of anatomy from the molecular level to the whole body. In this detailed review, Scarr highlights many examples of anatomical structures that contain helical patterns. Photographs of Scarr’s elegant handmade models illustrate the text and readers should access the online version of this paper to fully appreciate the elegance of the models. Studying the effectiveness of strategies to encourage a rural workforce in the health professions Workforce planning for osteopathy in the UK, Australia and NZ continues to be of interest to the professional bodies and regulatory authorities and there has been some concern and anecdotal reporting about difﬁculties encouraging new graduates to consider moving outside of the major metropolitan areas where they trained. It’s quite common to hear of rural and provincial practitioners reporting of difﬁculties attracting associates despite good remuneration and working conditions. Of course, this problem is not unique to osteopathy and the same issues are also common to a range of health professions internationally. In the United States there is a well-documented shortage of physicians working in rural areas, particularly in family medicine and primary care. Many osteopathic medical schools in the United States aim to produce

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Editorial / International Journal of Osteopathic Medicine 14 (2011) 1–2

graduates who will work in rural areas and use a range of strategies to meet this aim. In this issue, we publish a paper by Whitacre and colleagues that explores the effectiveness of some of these strategies in inﬂuencing the practice location of graduates. Although the paper will be of most direct interest to those involved in health provision in the United States, their method provides a useful approach to investigating this problem that could be employed in any country.

Nicholas Lucas Sydney, Australia E-mail address: [email protected] (N. Lucas) Robert Moran Department of Osteopathy, Unitec Institute of Technology, Auckland, New Zealand E-mail address: [email protected] (R. Moran)

International Journal of Osteopathic Medicine 14 (2011) 3e9

Contents lists available at ScienceDirect

International Journal of Osteopathic Medicine journal homepage: www.elsevier.com/ijos

Masterclass

Muscle energy technique: An evidence-informed approach Gary Fryer a, b, * a b

School of Biomedical & Health Sciences; ISEAL, Victoria University, Melbourne, Australia A.T. Still Research Institute, A.T. Still University of Health Sciences, Kirksville, MO, USA

a r t i c l e i n f o

s u m m a r y

Article history: Received 16 February 2010 Received in revised form 30 March 2010 Accepted 9 April 2010

This article describes the principles of evidence-based medicine and how these principles may be implemented in osteopathic practice and applied to the use of muscle energy technique. Because the feasibility of strict adherence to ‘evidence-based’ principles is debated, an approach of ‘evidenceinformed practice’ is recommended. The principles and diagnostic and treatment practices associated with muscle energy technique are re-examined in light of recent research. Implications for the application of muscle energy are outlined, and recommendations are made regarding clinical practice. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Muscle energy technique Isometric Manipulation Evidence-based medicine Osteopathic medicine

1. Introduction Muscle energy technique was developed by osteopathic physician, Fred Mitchell, Sr. It was reﬁned and systematised by Fred Mitchell, Jr., and has continued to evolve with contributions from many individuals. Muscle energy technique (MET) is used by practitioners from different professions and has been advocated for the treatment of shortened muscles, weakened muscles, restricted joints, and lymphatic drainage. In addition to using muscle effort to mobilise joints and tissues, MET is considered by some to be a biomechanics-based analytic diagnostic system that uses precise physical diagnosis evaluation procedures to identify and qualify articular range of motion restriction.1 Recent research suggests a revision of MET concepts and practices is required, particularly considering the trend towards evidence-based medicine (EBM). 2. Evidence-based medicine and evidence-informed practice Medical and allied health practitioners have been encouraged to practice according to the principles of EBM.2 However, some practitioners raise concern that EBM may be applied for economic reasons rather than best care.3,4 Others argue that EBM does not account for other kinds of medical knowledge5 and that EBM * Osteopathic Medicine Unit, School of Biomedical and Health Sciences, Victoria University, P.O. Box 14428 MCMC, Melbourne 8001, Australia. E-mail address: [email protected] 1746-0689/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ijosm.2010.04.004

studies, primarily randomised controlled trials (RCTs), address average results from large groups instead of data applicable to individual patients.6 A treatment effective for the majority may not always be effective for an individual for a variety of reasons, including the aetiology of their condition, past experience (negative or positive), and expectations of treatment outcome. Some approaches may be more effective in the hands of particular practitioners because of skill and experience. Certain treatments may also have larger non-speciﬁc (placebo) effects, and these effects should not be dismissed. The adoption of ‘best’ evidence may unintentionally limit practice, so balance between external clinical evidence and clinical experience is necessary. In manual therapy, strict adherence to EBM is not possible due to a lack of high-quality evidence on which to base decisions. EBM was originally intended to integrate clinical expertise with the best available clinical evidence,10 but many have argued that a narrow interpretation of EBM is prevalent, where treatment must be based on high-quality evidence and the role of clinical experience is devalued.3e6 Given that many professions are not able to base treatment on evidence, it has been argued that a preferred terminology is ‘evidence-informed practice’7 or ‘evidence-informed osteopathy’,8,9 which more accurately reﬂects the realty of the use of evidence in osteopathic practice. Evidence-informed practice has been deﬁned as the process of integrating research evidence when available but including personal recommendations based on clinical experience, while retaining transparency about the process used to reach clinical decisions.7

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2.1. Implementing evidence-informed principles into osteopathic practice Given the paucity of high-quality research evidence related to osteopathic practice, it can be difﬁcult to see how implementing EBM principles may make a difference to practice. However, adopting practices consistent with evidence-informed practice e using evidence when available to guide decision making e may shift the practice culture to improve patient care. While Strauss11 described 5 steps of EBM (asking a question, ﬁnding the evidence, applying information in combination with clinical experience and patient values, and evaluating the outcomes), a practitioner must start this approach with a ‘spirit of inquiry’.12 2.1.1. Spirit of inquiry Osteopaths should have a spirit of inquiry,12 a curiosity about the best evidence to guide clinical decision making. If a practitioner believes they already know everything or that clinical secrets can only be obtained from esoteric experiential practices, that modern research has nothing to offer, then the practitioner is unlikely to embrace evidence-informed practice. Willingness to change when there is good reason to do so is important for clinicians as well as the profession. 2.1.2. Search for evidence Keeping informed can be daunting for those unaccustomed to searching electronic databases and reading papers. For osteopaths, subscriptions to relevant journals (membership of many professional associations provides electronic access to osteopathic and manual therapy journals) are a place to start. Practitioners should regularly sight journal contents, skim the abstracts of interesting articles, and read further if there is relevance to clinical practice. Many osteopathic and manual therapy journals provide evidence summaries, comment on clinical guidelines, and review articles, which may offer evidence to guide decision making. Practitioners should ask questions and research patient problems. When presented with a new or a difﬁcult problem, practitioners should spend time researching the problem. In addition to consulting textbooks, practitioners are also able to access information using the free PubMed service or Google Scholar, which have links to primary research articles or other clinical information. When searching electronic databases, the PICOT (population, intervention, comparison, outcome, timeframe) approach is useful for identifying keywords and phrases.11,13 Osteopaths should develop a culture of seeking knowledge, looking at every patient encounter as a challenge to learn more. 2.1.3. Integrate evidence with clinical experience Critical appraisal of research involves determining if the results are valid, if they are important, and if they will improve patient care. Critical appraisal may initially be difﬁcult for those unfamiliar with this approach, and osteopaths are encouraged to participate in journal clubs to discuss articles and learn about the process of article critique. Evidence-informed practice involves assessing the relevance of existing evidence with the needs of the patient and integrating this knowledge with our own experience, other forms of evidence (expert opinion, physiological rationale, etc.), and the patient’s expectations and needs during treatment. In short, evidenceinformed practice uses evidence to make informed decisions and guide treatment for the beneﬁt of patients. Working within evidence-based guidelines, treatments should be consistent with current research, but the ﬂexibility to use treatments according to the judgement of the clinician (based on previous experience, awareness of patient values or preferences) should be utilized.

Practitioners may use research evidence and clinical guidelines to add techniques to what they use for best patient care, rather than removing treatments with anecdotal or theoretical rationale, but this will depend on the available evidence relevant to the patient presentation. 2.1.4. Evaluate outcomes By evaluating the effect of a change in practice approach, an osteopath can assess whether the change has been beneﬁcial. This may be difﬁcult to determine because of the heterogeneity of patients and their complaints, however, if standard outcome measures are used (validated self-reported questionnaires, visual analogue pain scales, the Oswestry Disability index, Neck Disability index, etc.) then evaluation becomes more objective.

3. Evidence-informed approach to muscle energy Like many manual therapeutic approaches, the efﬁcacy and effectiveness of MET technique are under-researched, and there is little evidence to guide practitioners in the choice of the most useful technique variations (such as number of repetitions, strength of contraction, duration of stretch phase), causing frustration for those endeavouring to integrate relevant evidence into practice. A limited but growing number of studies show positive change following MET intervention. Studies that demonstrate an increase in the extensibility of muscles14e19 and spinal range of motion20e24 support the rationale of treating patients with reduced mobility, although research involving clinical outcomes is scarce. One case study series25 and one RCT26 for the treatment of acute low back pain (LBP) are the only English language studies that examined MET as the sole treatment using clinical outcomes. Both reported decreased pain following treatment. The lack of clinically relevant research is not surprising given that MET is typically used in conjunction with other techniques. Several clinical trials investigating osteopathic management of spinal pain have included MET as a treatment component, and given that treatment signiﬁcantly reduced the reported pain and disability in these trials, they provide further support for the effectiveness of muscle energy, at least as part of a treatment package.27e29 While there is need for further investigation of muscle energy, available evidence supports the use of this approach to treat restricted mobility and spinal pain. Although limited evidence exists for the efﬁcacy of muscle energy, the current research literature indicates a need to reconsider the clinical diagnostic methods and the physiological mechanisms causing therapeutic effect. The mechanisms underlying the possible therapeutic effects are largely speculative, but evidence supports the plausibility of several modes of action. An understanding of the likely mode of action may inform and inﬂuence the application of muscle energy.

3.1. Diagnostic concepts Drs. Mitchell, Sr. and Jr., integrated clinical and anatomical observations and developed their approach based on Fryette’s physiological spinal coupling concept30 and a pelvic biomechanical model developed in conjunction with Paul Kimberley.1 Their approach has been adopted by most North American authors of MET texts1,31e35 although authors elsewhere have not always linked the technique to these models.36 Recent evidence casts doubt on the predictability of spinal coupled motion and raises questions about the validity and reproducibility of many of the recommended diagnostic tests.

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3.1.1. Assessment of the spine The traditional paradigm for diagnosis and treatment is mechanical, where multiple planes of motion loss are determined and each restrictive barrier is engaged to increase motion in all restricted planes.1,31e35 The identiﬁcation of motion restriction has been based on the spinal coupled motion model proposed by Fryette,30 which describes two types of coupled motion restriction: Type 1 (rotation and sidebending to opposite sides) is based on spinal asymmetry detected in neutral postures, while Type 2 (rotation and sidebending to the same side) is based on asymmetry in non-neutral spinal postures. Fryette’s model has been criticized for its prescriptive diagnostic labelling and dubious inferences from static positional assessment.37,38 Further, it allows only three combinations of multiple plane motion restrictions: a neutral Type 1, a non-neutral Type 2 with ﬂexion, or a non-neutral Type 2 with extension. The model does not allow for other combinations, such as rotation and sidebending to opposite sides with extension, and techniques for these combinations of motion restriction are not found in texts. Osteopathic texts advocate detection of dysfunctional spinal segments by using the diagnostic criteria of segmental tenderness, asymmetry, restricted range of motion, and altered tissue texture.1,31e33,39,40 The validity, reliability, and speciﬁcity of these criteria have been questioned,41e43 given only palpation for tenderness and pain provocation has acceptable interexaminer reliability. Using a combination of criteria (as suggested by osteopathic texts) that include tenderness or pain may improve the reliability of osteopathic examination. MET texts commonly suggest the assessment of static positional asymmetry of the spinal transverse process or sacral base with the spine in neutral, ﬂexion, and extension. Implicit to this approach is an assumption that a transverse process posterior or resistant to posterioreanterior springing represents a restriction of rotation to the opposite side, and inferences about coupled sidebending are made according the spinal posture. Although muscle asymmetry and anatomical vertebral asymmetry are complicating factors, they are not considered. Additionally, assessment of segmental static asymmetry has been shown to be unreliable,44 and spinal coupled motion in the lumbar, thoracic, and cervical spine is inconsistent between spinal levels and individuals.38,45e50 Coupled motion in the upper cervical region is relatively consistent,51 but inconsistencies in the lumbar and thoracic regions invalidate the Fryette model when predicting triplanar motion restrictions based on static asymmetry or single plane motion restriction, as recommended in many texts.1,31e35 3.1.2. Assessment of the pelvis Sacroiliac motions are small and complex, involving simultaneous rotation and translation.52,53 The sacroiliac joint has no primary motion but acts passively to accommodate torsional stress during ambulation,52 and the axes of motion are dependent upon the surface topography of the joints, which vary between individuals. Mitchell and others1,31e35 advocate sacroiliac motion testing during standing and seated ﬂexion to determine landmark asymmetry and the type of dysfunction, however, the usefulness of these tests is not supported by the literature.54e57 Forward ﬂexion tests have poor reliability and lack construct validity.58e60 The reliability of pelvic landmark asymmetry is poor,60e63 unless substantial asymmetry exists.64 Clusters of sacroiliac tests, mainly pain provocation, appear to have clinical utility,54,55,57 but are generally not recommended by MET texts, having utility for detecting a symptomatic joint, rather than sacroiliac dysfunction. The construct validity of pelvic asymmetry as an indicator of dysfunction is also lacking, but some evidence suggests asymmetry may have functional implications.65,66 Although pelvic torsion

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appears unrelated to LBP or positive clinical tests,67,68 subtle pelvic torsion may create an asymmetrical load on the lumbar and thoracic tissues.65,66 Sacroiliac motion in healthy volunteers is typically symmetrical, and asymmetrical motion (hypermobility rather than restricted motion) may be predictive for pelvic pain.69e72 Sacroiliac dysfunctions proposed by Mitchell are clinical constructs, rather than deﬁnitive clinical entities. The absence of objective indicators of mechanical dysfunction of the sacroiliac joint and poor reliability of the motion tests used to detect it make sacroiliac dysfunction difﬁcult to validate. Nevertheless, variability of sacroiliac anatomy and motion may cause the described dysfunctions in susceptible individuals. Pelvic asymmetry, however, may be secondary to myofascial imbalance. One study73 found electrical activation of the pelvic ﬂoor muscles produced a large effect on pelvic alignment. MET techniques involve contraction and stretch of myofascial structures and if muscle imbalance and altered tone has a role in producing pelvic asymmetry, it is possible that MET may inﬂuence pelvic alignment and functional symmetry by affecting myofascial tissues, rather than directly affecting the sacroiliac joint. 3.1.3. Implications for assessment in clinical practice With dubious reliability and validity for many tests of spinal and pelvic dysfunction, practitioners following an evidence-informed approach will be frustrated. Until we have tests with better clinical usefulness, the practitioner should use those tests with face validity and clinical utility based on experience, be cautious about making ﬁrm conclusions based on single clinical ﬁndings, and use a variety of tests that support a logical clinical reasoning process. Due to the unpredictability of coupled motions in the spine, practitioners should address motion restrictions that present on palpation (despite issues of reliability), rather than assumptions based on biomechanical models and static palpatory ﬁndings. If corrective motion is introduced in the primary planes of restriction, spinal coupling (in whatever direction) will occur automatically e due to the nature of conjunct motion ewithout being intentionally introduced by the practitioner. Therefore, the pragmatic approach addresses the primary motion restriction(s); coupled motion will occur without the aid of the practitioner. Despite the shortcomings of many of the pelvic and sacroiliac assessment methods, a pragmatic approach uses a cluster of tests, incorporating motion and provocative testing, not relying on a single isolated ﬁnding. Practitioners should not assume every asymmetrical pelvis is dysfunctional and warrants treatment. For ﬂexion tests, a difference between standing and seated observations may be signiﬁcant, but indicating asymmetry in the pelvis and/or lower extremity, rather than sacroiliac dysfunction. Practitioners should consider that pelvic asymmetry may be caused by myofascial imbalance (asymmetry of length, strength or activation pattern) articular dysfunction, and attention should be given to assessment and treatment of these tissues. 3.2. Therapeutic mechanisms The proposed mechanisms underlying the possible therapeutic effects of MET have been largely speculative. Research examining the physiological mechanisms of MET is ongoing, however the current evidence challenges some of the proposed therapeutic concepts. The underlying therapeutic action may involve a variety of neurological and biomechanical mechanisms, including hypoalgesia, altered proprioception, motor programming and control, and changes in tissue ﬂuid.75e77 MET may also have physiological effects regardless of presence or absence of dysfunction.22,23 An understanding of the likely physiological therapeutic mechanisms

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underlying manual techniques may assist an evidence-informed approach for technique selection. Reﬂex muscle relaxation is commonly cited as a mechanism for length, range of motion (ROM), and tissue texture changes following muscle energy.1,31,36,78 However, studies support increased tolerance to stretching (hypoalgesia), not reﬂex relaxation, as the mechanism for increasing muscle extensibility.14,16,76,79 Although reﬂex relaxation appears plausible from studies examining muscle contraction with electrophysiological parameters,80e82 no study has shown a decrease in electromyographic (EMG) activity following muscle energy. On the contrary, MET and similar techniques have increased the low-level EMG activity during and following stretching, despite an increase in muscle length.16,17,83,84 Evidence of EMG disturbance in the paraspinal muscles of patients with LBP exists,85,86 but no study has investigated MET and EMG activity in the spine. Thus, factors other than reﬂex muscle relaxation seem responsible for muscle extensibility and ROM following these techniques. Applications of MET to stretch and increase myofascial tissue extensibility seem to affect viscoelastic and plastic tissue property,87,88 autonomic-mediated change in extracellular ﬂuid dynamics,89 and ﬁbroblast mechanotransduction,89,90 but few lasting changes in human muscle properties have been found.76 Studies measuring pre- and post-force (torque) show little viscoelastic change after passive or isometric stretching and indicate that muscle extensibility is due to increased tolerance to an increased stretching force.14,16,79 Although short- and medium-term application of stretching and MET may alter the perception of pain, it does not appear to affect the biomechanics of healthy muscle, but studies are required for injured and healing muscle tissue. MET may inﬂuence pain mechanisms and promote hypoalgesia. Studies suggest MET and related post-isometric techniques reduce pain and discomfort when applied to the spine26 or muscles.14,16 The mechanisms are not known, but may involve central and peripheral modulatory mechanisms, such as activation of muscle and joint mechanoreceptors that involve centrally mediated pathways, like the periaqueductal grey (PAG) in the midbrain, or nonopioid serotonergic and noradrenergic descending inhibitory pathways. Animal and human studies have shown sympathoexcitation and localised activation of the lateral and dorsolateral PAG from induced or voluntary muscle contraction,91,92 and activation of non-opioid descending inhibitory pathways from peripheral joint mobilization.93,94 Additionally, MET may increase ﬂuid drainage and augment hypoalgesia. Rhythmic muscle contraction increases muscle blood and lymph ﬂow rates,95 and mechanical forces acting on ﬁbroblasts in connective tissues change interstitial pressure and increase transcapillary blood ﬂow.96 MET application may reduce pro-inﬂammatory cytokines and desensitize peripheral nociceptors. MET may also produce changes in proprioception, motor programming, and control. Spinal pain disturbs proprioception and motor control, causing decreased awareness of spinal motion and position97e101 and cutaneous touch perception.102,103 Spinal pain affects motor programming, inhibiting the stabilizing paraspinal musculature, while causing superﬁcial spinal muscles to overreact to stimuli.85,86 No study has investigated the effect of MET on proprioception or motor control, but limited evidence suggests beneﬁt from other manipulative treatments.104e108 Since MET produces joint motion while actively recruiting muscles, it may affect proprioceptive feedback, motor control, and motor learning; this should be investigated in the future. Authors of MET texts have proposed that the technique improves lymphatic ﬂow and reduces edema,1,109 and evidence from muscle contraction and physical activity studies support this.95,98,110,111 Muscle contraction increases interstitial tissue ﬂuid

collection and lymphatic ﬂow,95,111 and physical activity increases lymph ﬂow peripherally in the collecting ducts, centrally in the thoracic duct, and within the muscle during concentric and isometric muscle contraction.98,110 MET may assist lymphatic ﬂow and clearance of excess tissue ﬂuid to augment hypoalgesia, changing intramuscular pressure and the passive tone of the tissue. The mechanisms outlined above may explain some of the therapeutic action of MET technique, but are not likely to be speciﬁc to this technique and will possibly be activated by any physical activity that produces muscle contraction. It is argued that MET applied speciﬁcally to a painful and dysfunctional region may produce local changes in circulation, inﬂammation and proprioception, and although these proposed mechanisms appear plausible they are still largely speculative. The relative efﬁcacy of speciﬁcally applied MET compared to general physical activity has not been explored and would help to determine the usefulness of MET for regional pain and dysfunction. 4. Evidence-informed application of muscle energy The implications of the current research literature are more pertinent for theoretical concepts of MET than to its use in clinical practice. As discussed previously, MET may be useful for increasing muscle extensibility and spinal range of motion and for low back and neck pain. However, clinicians should be circumspect about the structural diagnosis process and not rely on isolated diagnostic tests and ﬁndings. While studies have examined the efﬁcacy of technique variations,23,112,113 few recommendations can be made. The mechanisms underlying MET are uncertain and based on inference from related studies, but some appear plausible, allowing speculation on their clinical implications. Consistent with an evidence-informed approach, these inferences from research should be balanced with clinical experience. 4.1. Muscle energy for increasing muscle length Evidence suggests MET (or similar isometric stretching techniques) is more effective than passive stretching for increasing muscle extensibility. Due to lack of studies or conﬂicting evidence, little information exists about the optimal number of isometric contractions, the duration and intensity of contraction, or the force of the stretch.76 Evidence for the most effective direction of contraction to increase ﬂexibility in healthy muscle does exist. To gain maximum ROM and muscle extensibility, the use of isometric variations that include recruitment of the agonist muscle is suggested. Agonistcontract (AC) and contract-relax agonist-contract (CRAC) are variants of proprioceptive neuromuscular facilitation, where the patient actively pushes further into the barrier (AC) or where isometric contractions away from and into the barrier are alternated. These techniques have been consistently effective for increasing ﬂexibility76 but are appropriate where muscles are not painful. It is not recommended for muscles or joints that are painful because pushing into the painful barrier would likely produce protective muscle guarding and apprehension. The duration of the stretch phase for maximum gains in ﬂexibility should be considered. Many recommend only a few seconds of relaxation before re-engaging the new barrier,1,31e35 but Chaitow recommends a duration of up to 60 s for chronically shortened muscles.36 Studies reporting that duration of stretch inﬂuences the amount and longevity of ROM gains support this recommendation.114e117 Further, longer stretching durations are more effective than short durations, with 15 s more effective than 5114 and 30 s more effective than 15 but no different than 60.115,116 Feland et al.117 reported a 60-s stretch produced greater gains in

G. Fryer / International Journal of Osteopathic Medicine 14 (2011) 3e9

ROM that lasted longer than lesser durations for elderly people with tight hamstrings, and their subjects may be representative of those with chronically shortened ﬁbrotic muscles. Although no studies suggest the best application for stretching painful muscles, healing muscles, or active trigger points, gentle contraction and stretching forces with shorter durations should be used to recruit sensitised ﬁbres (as suggested for myofascial trigger points), avoid further tissue damage, and promote repair and healing. An evidence-informed approach for painless, chronic, ﬁbrotic muscles indicates moderate contraction and stretching forces, maintain the stretch phase up to 60 seconds, and use AC or CRAC where appropriate. 4.2. Muscle energy for spinal dysfunction The unpredictability of coupled motions in the thoracic and lumbar spine has been discussed, and practitioners should address motion restrictions that present on palpation in as many planes as identiﬁed. If motion is introduced in the primary plane(s) of restriction, coupled motion will occur automatically. If multiple plane motion restrictions are identiﬁed that do not conform to the Fryette model, technique should be adapted to accommodate the motion restrictions identiﬁed. If segments do not respond to treatment, then the diagnosis should be reassessed and clinical judgement used regarding appropriate further treatment. The chronicity of spinal dysfunction may inﬂuence the choice of technique and approach. The aetiology of segmental dysfunction is speculative, but acute dysfunction may arise from minor trauma, producing minor strain and inﬂammation in the spinal unit. In acute spinal conditions, zygapophysial joint sprain and effusion may produce local pain and limited motion (active and passive). Following strain and inﬂammation, nociceptive pathways may be activated and initiate a cascade of events, including the release of neuropeptides from involved nociceptors that promote tissue inﬂammation. This neurogenic inﬂammation may outlast the tissue damage and contribute to tissue texture abnormality. Additionally, central nervous system motor strategies may be altered to inhibit deep paraspinal muscles and produce excitation of more superﬁcial muscles, which may further altering tissue texture and quality of motion.74,77 With acute dysfunction, techniques should promote ﬂuid drainage, hypoalgesia, and proprioceptive input. MET should be applied to the ‘ﬁrst’ barrier (ﬁrst sense of increasing resistance to motion) as described by Mitchell,1 with repeated gentle isometric contractions. Repetitive mid-range articulation may assist transsynovial ﬂow and lymphatic drainage, and indirect techniques (techniques that place the joint or tissues in a position of ease or relaxation) may have a role in reducing the secretion of proinﬂammatory peptides to minimise pain and inﬂammation.118 Chronic dysfunction is characterised by restricted range of motion, thickened tissues, and relatively little localised pain or tenderness at the site of dysfunction. Following acute injury (and probably ongoing repetitive trauma due to deﬁciencies in proprioception, motor control, and stabilisation), degenerative changes occur in the intervertebral disc and zygapophysial facet joints, periarticular connective tissue undergoes proliferation and shortening, and these degenerative changes act as co-morbid conditions that continue to affect the spinal unit. Sensitised nociceptive pathways may interfere with proprioceptive processing, creating deﬁcits in proprioception and affecting segmental muscle control, which may disrupt the dynamic stability of the segment and predispose it to ongoing mechanical strain.74,77 For segmental dysfunctions that suggest a chronic condition, the most beneﬁcial techniques may be those that stretch and mobilise tissues and improve proprioception and motor control. When

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applying MET to a chronic and restricted joint, engaging the barrier at the point of elastic end-range (rather than the ﬁrst barrier) will load and stretch the shortened capsule and peri-capsular structures to produce viscoelastic and possibly plastic changes. Provided the localisation is maintained, more moderate contraction forces can be used to enhance post-isometric hypoalgesia and stretch tolerance and allow adequate post-contraction loading on the tissues. Isometric contraction will help proprioceptive feedback and recruitment, but controlled isotonic (eccentric) contraction e allowing the muscle to shorten over the range of motion e may also be beneﬁcial. High-velocity, low-amplitude (HVLA) thrust technique might be used with end-range articulation, given HVLA creates cavitation and increases joint separation in the short-term, allowing end-range articulation to optimally stretch the pericapsular tissues. 4.3. Muscle energy for pelvic dysfunction As discussed, many diagnostic tests have dubious value, and a pragmatic approach uses a cluster of tests, incorporating motion and provocative testing, and does not rely on a single isolated ﬁnding. Pelvic asymmetry may be caused by myofascial imbalance (asymmetry of length, strength or activation pattern) rather than articular dysfunction, and attention should be given to treatment of these tissues. Osteopaths have emphasised sacroiliac dysfunction as a hypomobility lesion, but should also consider hypermobility as an aetiology for the painful joint,119 considering that asymmetrical joint laxity is associated with pelvic pain in pregnant women.69e72 In addition to improving perceived pelvic symmetry and function, MET may enhance motor recruitment and stability by using isotonic (eccentric) contraction to improve motor recruitment for pelvic and hip muscle weakness and atrophy.1 The addition of motor control and stability training for these patients should be considered.120 5. Conclusion Evidence-informed practice uses research evidence when available, followed by personal recommendations based on clinical experience, while retaining transparency about the process used to reach clinical decisions. There is a lack of high-quality research regarding the efﬁcacy and effectiveness of MET, as well as the therapeutic mechanisms, but emerging evidence supports the clinical usefulness of this technique. However, reassessment of the recommended assessment practices associated with the technique is required, and additional evidence should establish plausible therapeutic mechanisms to guide therapeutic decisions about application of the technique for different conditions. Acknowledgements The author wishes to thank Deborah Goggin, MA, Scientiﬁc Writer, A.T. Still Research Institute, A.T. Still University, for reviewing this manuscript. This manuscript was based, in part, on a previous article published in Franke H., ed. Muscle Energy Technique: HistoryeModeleResearch (Monograph). Ammersestr: Jolandos; 2009:57e62.75 Statement of competing interests Gary Fryer is a member of the Editorial Board of the Int J Osteopath Med but was not involved in review or editorial decisions regarding this manuscript.

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International Journal of Osteopathic Medicine 14 (2011) 10e16

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Research report

The palpated cranial rhythmic impulse (CRI): Its normative rate and examiner experience Nicette Sergueef, Melissa A. Greer, Kenneth E. Nelson*, Thomas Glonek Department of Osteopathic Manipulative Medicine, Chicago College of Osteopathic Medicine, Midwestern University, 555 31st Street, Downers Grove, IL 60515, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 March 2009 Received in revised form 12 November 2009 Accepted 25 November 2010

This retrospective review study aims to contribute data regarding the normal range of the palpated cranial rhythmic impulse (CRI) rate from a population of 734 healthy subjects, each determined by a different examiner. Experience levels ranged from 1 to 25 years training/practice in cranial osteopathy. This study reports an overall CRI rate range (mean SD) of 6.88 4.45 cpm for all subjects (valid N ¼ 727). The examiner population was subdivided into three groups based upon the level of examiner experience. The rates obtained from each subgroup, from least experienced to most experienced, are as follows: Level 1 (one year of experience), 7.39 4.70; Level 2 (two years of experience), 6.46 4.10; Level 3 (three-twenty ﬁve years of experience), 4.78 2.57. Both group mean values of the reported palpated CRI rates and their standard deviations showed an inverse relationship with the level of examiner experience, i.e., as experience increases, the mean CRI rate and its deviation decreases. In the light of the ﬁndings of this study, the currently accepted range of the palpated CRI, 8e14 cycles/minute, should be reconsidered to be as low as 2e7 cycles/minute. Précis: CRI rate means and ranges as assessed by experienced examiners are, respectively, lower and narrower. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Osteopathic Medicine Osteopathic Manipulative Medicine Osteopathy in the Cranial Field Cranial Osteopathy Medical education Teaching psychomotor skills Cranial rhythmic impulse CRI rate Primary Respiratory Mechanism

1. Introduction In the paradigm of cranial osteopathy, a controversial rhythmicity, the cranial rhythmic impulse (CRI), has been described, discussed, and debated.1e5 It is deﬁned in the Glossary of Osteopathic Terminology6 as “a palpable rhythmic ﬂuctuation believed to be synchronous with the primary respiratory mechanism.” The fact that the CRI is debatable and incompletely understood makes it subject to question and, therefore, of interest for corroboration of its normative parameters. In 1939, William G. Sutherland ﬁrst proposed cranial osteopathy and, what he suggested was a means of holistically coordinating the approach to patient care, the primary respiratory mechanism (PRM).7 He described it as a biphasic phenomenon, independent of pulmonary respiration, with an “inspiratory” and an “expiratory” phase. It is interesting to note that nowhere in the early descriptions of the cyclic PRM is there speciﬁc mention of its rate or normative range. In fact, it wasn’t until 1961, well after Sutherland’s

* Corresponding author. Tel.: þ1 630 515 6039/1 630 515 7123 (OMM departmental ofﬁce), fax: þ1 630 515 6949. E-mail addresses: [email protected] (N. Sergueef), melissa.greer@ mwumail.midwestern.edu (M.A. Greer), [email protected] (K.E. Nelson), [email protected] (T. Glonek). 1746-0689/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ijosm.2010.11.006

death, that Woods and Woods ﬁrst published the term cranial rhythmic impulse and a normative rate for it (10e14 cpm).8 The establishment of normative parameters for the rate of the CRI subsequently has been controversial due to: (1) the lack of an accepted objective approach, (2) the esoteric nature of the phenomenon, (3) the subjective nature of the CRI’s detection through palpation, (4) the relatively low number of researchers experimentally measuring the rate, and (5) the comparatively low subject population numbers in many of the published studies. Recognized osteopathic textbooks5,9,10 cite the rate in the range of 8e14 cpm, consistent with the original, 1961, Woods and Woods study.8 This range still is often cited as deﬁnitive even though a much lower range has been reported repeatedly.11e18 Past reported measured rates for the palpated rate of the CRI are presented for comparison in Table 1, along with the values from this study. The aims of this study were (1) to deﬁne the normative rate of the CRI and (2) to compare palpated CRI rates obtained by practitioners at three experience levels. 2. Methods The study was organized around the teaching activities of one of the authors (NS) in compliance with the legal requirements of the Commission Nationale de l’Informatique et des Libertés (CRIL) and

N. Sergueef et al. / International Journal of Osteopathic Medicine 14 (2011) 10e16 Table 1 Reported cranial rhythmic impulse (CRI) rate ranges. Authors

CRI Rate (Range or Values)

Subjects in Study (N)

Year Reported

Woods and Woods8 Norton et al.11 Wirth-Pattullo and Hayes12 McAdoo and Kuchera13 Hanten et al.14 Rogers et al.15 Sommerfeld16 Moran and Gibbons17 Nelson et al.18 This Study All subjects 1 year experience 2 years experience 3e25 years experience

10e14 3.2e4.1 3e9 6.63e9.37 3.6 & 4.2 3.28 & 4.83 2.3e3.6 2.92e4.17 2.46e6.62 (mean SD) 2.43e11.33 2.69e12.09 2.36e10.56 2.21e7.35

62 24 12 128 40 28 49 11 44

1961 1992 1994 1995 1998 1998 2004 2004 2006 2009

727 463 190 74

the Helsinki Accord. Students who participated in the academic program were taught to palpate the CRI and tested to establish their ability to monitor it. The data for this study were taken from these evaluations. The participants of this study (N ¼ 734) were practicing clinicians (predominantly physical therapists, with some nurses, midwives and medical doctors). They were undergraduate and postgraduate students of osteopathy. Most were studying at, or graduates of, La Maison de la Thérapie Manuelle, an osteopathic school that holds classes in different European cities. Their formal two year course of study in cranial osteopathy consisted of 225 contact hours, including 150 h of didactic and 75 h of laboratory work. It was presented within an extensive academic osteopathic curriculum, typically after two years of general osteopathic studies. The Level 1 individuals participated at the end of their ﬁrst year of cranial osteopathic study. The Level 2 individuals participated upon completion of the course at the end of their second year of study. The Level 3 individuals, having successfully completed the two year cranial program, participated as attendees of postgraduate courses in cranial osteopathy. The demographics of the study population, with respect to the city and year in which the course was given, the level of participants, and their number at that site and year, are as follows: 60.2% (of the total enrolment) at Biscarrosse, France: [2001] Level 1, 86; [2002] Level 1, 50, Level 2, 32, Level 3, 35; [2003] Level 1, 48, Level 2, 31; [2004] Level 2, 52; [2005] Level 1, 59, Level 2, 49. 29.3% at Paris, France: [2002] Level 1, 42; [2003] Level 1, 15, [2004] Level 1, 74, [2006] Level 1, 58, Level 2, 26. 5.2% at Lyon, France: [2003] Level 1, 16, [2004] Level 1, 22. 5.3% at Padova, Italy: [2003] Level 3, 39. The % of the total number of subject/examiners at each level were 64.0% level 1, 25.9% level 2, 10.1% level 3. Data collection occurred at the end of the course at the same time in the academic schedule of each program. The time of day was variable depending upon each separate program’s schedule. The data were collected in the teaching laboratory with the subjects always being examined in the same position, supine upon the examination table. The data were collected in each instance by the same individual (NS). All participants palpated CRI rates on each other (734 different healthy individuals) within the controlled environment of the teaching laboratory. The groups were divided in half, with half of the group being examiners and the other half subjects. Upon completion of the protocol, the pairing was maintained and the individuals changed places, with the examiners becoming subjects and the subjects becoming examiners. With this structure, every participant was an examiner one time and a subject one time. At no time during and between both sessions was any communication between participating individuals permitted. The examiners were

11

asked to begin palpating the CRI using the classically described vault hold5,9 and given enough time, ca. 2 min, to sense the oscillation. Following this acclimatisation period, they were told when to start and when to stop counting the CRI. They were not told how long they would be palpating, only to count the number of complete biphasic CRI cycles that they palpated during the acquisition period. They were timed, using a wristwatch with a sweep second hand for a predetermined number of minutes (all trials, 3 min) known only to the individual conducting the protocol. It was determined by our previous work18e20 that this relatively brief time measurement window is sufﬁcient to provide a good CRI sampling number without introducing error that could come with longer measurement periods. Following the data acquisition period, the investigator passed among the examiners and had them silently record their measured rate on a roll of paper after which that section of paper was torn from the roll and placed into an envelope. The reported number-of-cycles were kept private, and palpating participants were not aware of the rates that other participants reported. The investigator then moved to the next examiner and repeated the process until the rates acquired from all examiners had been gathered. Following this, the pairs exchanged positions, and the protocol was repeated. The numbers recorded on the paper fragments were tabulated on a spreadsheet identifying the experiential group and site. The CRI rate was then calculated in cycles/ min for each recorded value by dividing the total number of CRI cycles counted per subject by 3, the time in minutes allowed at each measurement session. 3. Statistical analysis Palpating participants were analyzed in three groups based upon their level of training and clinical experience: Level 1 (N ¼ 463) consisted of students with 1 year of experience who successfully palpated the CRI; Level 2 (N ¼ 190), 2 years of experience; Level 3 (N ¼ 74), 3e25 years of experience. Although 734 individuals participated in the study, seven Level 1 students did not palpate a CRI rate, yielding a valid subject population of 727 volunteers. Data frequencies and descriptive statistics were computed using the SPSS statistical package (SPSS, Inc., SPSS 10.1).21 The One-Way Analysis of Variance (one-way ANOVA) was used to assess whether a signiﬁcant difference existed among the three experimental groups. In addition, pair-wise comparisons (of means) were performed among the three groups using both the Scheffé and the Least-Signiﬁcant Difference range tests, with an alpha of .05 accepted as signiﬁcant. Formal tests of normality were computed using the ShapiroeWilk and the KolmogroveSmirnov tests. The distributions obtained (histograms) were analyzed further for their deviations from normality using Normal QeQ plots and Detrended Normal QeQ plots. 4. Results Seven Level I participants (1.5%) were unable to perform the CRI rate determination, while all participants in Levels 2 and 3 successfully performed the CRI rate determination. The valid examiner/ subject population of the 734 potential pairings, therefore, was 727. The mean reported CRI rate (N ¼ 727) was (mean SD) 6.88 4.45 cycles per minute (Fig. 1 and Tables 2 and 3). Skewness (2.510 .091) and Kurtosis (11.389 .181) provide measures of the distribution (Table 2). (Skewness, or third moment, will take on the value of zero when the distribution is a completely symmetric bellshaped curve. Kurtosis, or fourth moment, is a measure of relative peakedness or ﬂatness of the curve. A normal distribution will have a kurtosis of zero.21) The mean (SD) for each subgroup (Tables 1 and 3) is as follows: Level 1, 7.39 4.70; Level 2, 6.46 4.10; Level 3, 4.78 2.57 (Fig. 2).

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N. Sergueef et al. / International Journal of Osteopathic Medicine 14 (2011) 10e16 Table 3 Cranial Rhythmic Impulse (CRI) rate partitioned by experience level: Descriptive Statistics.

140 120

Level N

100

Mean Std. Std. Deviation Error

80 1 463 7.392 4.700 2 190 6.458 4.102 3 74 4.775 2.570 Total 727 6.882 4.446

Frequency

60 40

.218 .298 .299 .165

95% Conﬁdence Interval for Mean Lower Bound

Upper Bound

6.963 5.871 4.179 6.558

7.822 7.045 5.370 7.205

Minimum Maximum

1.00 1.33 1.33 1.00

39.33 33.67 13.33 39.33

All values except Level and N are reported as cycles per minute for data collection times of 3 min.

20 0 .9 38 .8 34 .7 30 .5 26 .4 22 .2 18 .1 14 .0 10 8 5. 7 1.

Observed CRI Value Fig. 1. Frequency histogram of cranial rhythmic impulse (CRI) rates. Each bar represents a CRI range of 1.38 cycles/minute (cpm); frequency is the number of the 727 participants in a given range (mean SD ¼ 6.882 4.446; N ¼ 727). The solid line depicts the standard deviation (SD) curve derived from the histogram. Note; because of the skewed nature of the CRI data, the normal distribution curve presented in the ﬁgure is truncated on the left because it is impossible to palpate a rate lower than zero.

One-way analysis of variance for levels 1, 2 and 3 was signiﬁcant (P < 0.001). The Scheffé post hoc test showed that all three groups were different, one from the other (Fig. 2 and Table 4). In Fig. 3, parts A, B, and C, the histograms of Fig. 2 have been adjusted vertically so that the shape of the histograms is more apparent visually. Note that with increasing experience (Level 3), the width of the distribution is narrowest, and the skew is least. The maximum bars of the histograms, however, are located approximately at the same values of the CRI rate for all three groups. Analysis of distributions for each group is presented in the normal probability plots of Fig. 3, parts D, E, and F. If the data are from a normal distribution, the plotted values should fall roughly around the diagonal lines in Fig. 3, parts D, E, and F. Points falling off the line indicate deviation from a normal distribution. Fig. 3, parts D and E, are similar in appearance and fall below the normality line for both low and high CRI values, with the deviation from normal being greatest for Level 1 (Fig. 3, part D). Fig. 3, part F, is distinctly different. Here the distribution approximates normality because the data points fall close to the normative line.

Table 2 Cranial Rhythmic Impulse (CRI) rate from all valid participants: Descriptive Statistics (Rates are reported as cycles per minute for data collection times of 3 min). Statistics (All participants) N Valid Missing Mean Std. Error of Mean Median Mode Std. Deviation Variance Skewness Std. Error of Skewness Kurtosis Std. Error of Kurtosis Range Minimum Maximum

727 7 6.882 .1649 6 3.33 4.446 19.766 2.510 .091 11.389 .181 38.33 1.00 39.33

The data in Fig. 3, parts D, E, and F, are scaled identically to facilitate comparisons. Note that the slope of the lines move to the vertical from Level 1 through Level 3, indicating a tighter grouping of the data, i.e., the data from experienced practitioners is less scattered, which also is reﬂected in the values of the standard deviations (Table 3). Further analysis of the three distributions is presented in the detrended normal probability plots of Fig. 3, parts G, H, and I. These detrended plots can also be used to detect patterns of how the histogram data depart from normality. In these displays, the differences between the usual z score for each case and its expected score under normality are plotted against the CRI values (the scale on the vertical axis remains in standardized units). Here, since the plot line is horizontal, the vertical plot scale enlarges, magnifying the view of the conﬁguration.21 (In a normal distribution, points will be scattered plus and minus about the horizontal line and will be clustered close to it.) Again, Fig. 3, parts G and H (Levels 1 and 2), show similar curved displays having large positive wings. These distributions lie far from the normal. In contrast, the distribution of Level 3 (Fig. 3, part I) lies close to the normal with only a single point being an outlier.

5. Discussion Why should we concern ourselves with the rate of the CRI? Cranial osteopathy, the PRM and the CRI are decidedly controversial, with a number of authors questioning their validity.1e4 Further, the fact that there were 22 years between the introduction of the cranial hypothesis7 and the initial use of the term cranial rhythmic impulse and the ﬁrst publication of an observed rate for the CRI8 could lead one to wonder if the rate was of any great relevance to early practitioners. We would contend that resolution of the controversy over cranial osteopathy could come only from an acceptable understanding of its underlying physiology. As stated earlier, the CRI is an observable (palpable) rhythmic ﬂuctuation believed to be synchronous with the PRM.6 As an observable phenomenon associated with the PRM, the central concept in cranial osteopathy, it offers access for the study of the cranial hypothesis. Yet measured rates for the CRI tend to vary sufﬁciently from one study to another (Table 1) as to call into question what is being measured. Since it is assumed to be a biological rhythm, the CRI should have a normative rate and range. Identifying these values will allow better understanding of the phenomenon and possibly provide access to further study of the underlying physiology and therapeutic impact of cranial osteopathy. Having normative values for the CRI also will aid in the teaching of cranial osteopathy. If a student has a clearly deﬁned idea as to the rate of the physiological rhythm they are trying to learn to palpate, the objective of their studies becomes easier to identify. Testing a student’s ability to palpate also will be facilitated. The use of a window of observation, similar to that employed in this protocol,

N. Sergueef et al. / International Journal of Osteopathic Medicine 14 (2011) 10e16

13

Fig. 2. Frequency histograms of cranial rhythmic impulse (CRI) rates partitioned by level of training. Level 1, 1 yr (N ¼ 463); Level 2, 2 yr (N ¼ 190); Level 3, 3e25 yr (N ¼ 74). Each bar represents a CRI range of 1.43 counts per minute (cpm); frequency is the number of the total 727 participants in a given range for each training level.

becomes a feasible testing tool if well-documented rates for the CRI are available. The establishment of normative values in the clinical sciences, however, ordinarily means the conduct of studies with large N numbers. This study provides a statistical N of 727 subjects (Tables 1 and 2). This number of cases (all different subjects) is 83% larger than the sum of all comparable studies identiﬁed in Table 1. Both the reported CRI rate means and standard deviations in this current study showed an inverse relationship with the level of examiner experience, i.e., as experience increased, means and standard deviations decreased. This is consistent with what one would expect: (1) beginning level students ought to show a greater range of palpatory results because of an increased possibility for error (increased SD), (2) the intermediate training level’s values would fall somewhere between beginners and experienced practitioners, and (3) the more experienced examiners should be capable of more precisely palpating the CRI, yielding a decreased variance. The data do show that these

variance expectations for the three levels are valid (Table 3, means; Table 4, multiple comparisons), with the experienced group demonstrating an SD that approximates half that of the two less experienced groups. During the implementation of the protocol the CRI counting period was reasonably short, 3 min, and it was the same in all instances, even though the participants did not know for how long they were counting. The data from the experienced practitioners presented in Table 3 and Fig. 3 demonstrates that the CRI values were reasonably closely clustered for the experienced group. This indicates that the experimental protocol was, therefore, reasonably well designed and that the spread in CRI values observed for the two less experienced groups was the result of practitioner inexperience and not the result of a poorly designed protocol. Further, and in support of the reliability of experienced examiners, are respective histograms of Levels 1, 2, and 3 CRI values and their analyses through normal probability and detrended normal probability plots (Fig. 3). These plots demonstrate that CRI values

Table 4 Statistical signiﬁcance of differences in results among the three educational levels. Levels Compared

Difference Between Mean Rates

(I)

(J)

(I e J)

1 1 2

2 3 3

.935 2.618 1.683

Std. Error

.377 .548 .600

All values except Level and P are cycles per minute. a The mean difference is signiﬁcant at the .05 level (Scheffé multiple comparisons).

95% Conﬁdence Interval For the Difference Between Means Lower bound

Upper bound

.0096 1.2737 .2122

1.8593 3.9615 3.1540

P

.047a <.001a .020a

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N. Sergueef et al. / International Journal of Osteopathic Medicine 14 (2011) 10e16

Frequencies A

B

C

LEVEL= 1 50

100

40

80

20

40 20 0

Frequency

30

60

Frequency

Frequency

LEVEL= 3

LEVEL= 2

120

20 10 0

38 33 29 24 20 15 11 6 2

29 24 20 15 11 6 2

Observed CRI Value

0

38 33

38 33 29 24 20 15 11 6 2

Observed CRI Value

10

Observed CRI Value

Normal Q-Q Plots E

D

F LEVEL= 2

LEVEL= 3

3

3

2

2

2

1 0 -1 -2 -3 -10

0

10

20

30

40

Expected Normal

3

Expected Normal

Expected Normal

LEVEL= 1

1 0 -1 -2 -3 -10

Observed CRI Value

0

10

20

30

40

1 0 -1 -2 -3

-10

Observed CRI Value

0

10

20

30

40

Observed CRI Value

Detrended Normal Q-Q Plots H

G

I LEVEL= 2

LEVEL= 3

5

5

4

4

4

3 2 1 0 -1 0

10

20

Observed CRI Value

30

40

Dev from Normal

5

Dev from Normal

Dev from Normal

LEVEL= 1

3 2 1 0 -1 0

10

20

Observed CRI Value

30

40

3 2 1 0 -1 0

10

20

30

40

Observed CRI Value

Fig. 3. Analysis of histogram distributions through Frequency, Normal QeQ, and Detrended Normal QeQ plots. (The histograms of Fig. 2 have been adjusted vertically for this ﬁgure so that the shape of the histograms is more apparent visually.) The duration of training/clinical experience of each group is indicated as Level 1 (1 year), Level 2 (2 years), and Level 3 (3e25 years). Parts AeC: Further analysis of the data of Fig. 2, presented as expanded histograms. The relative amplitude of these histograms has been adjusted vertically from Fig. 2 for visual comparison; each bar represents a CRI increment of 1.33 cycles/min. Parts DeF: Normal QeQ plots. The diagonal lines in each plot represent a computed normal distribution based upon the histogram immediately above it. The actual data points also are plotted. [Each observation in a normal probability plot is plotted against the corresponding quantile of a standard normal distribution (its expected z score or standard score)dthe observed data values are plotted on the horizontal axis and the “expected” values under normality on the vertical axis.21] Comparing the data points to the computed normal distribution line gives an indication of the degree and characteristics of deviation from normality. The slope of the line indicates the breath of the distribution, with narrow (compact) distributions approaching the vertical. Parts GeI: Detrended Normal QeQ plots. These plots amplify the spread in the data relative to the computed normal distribution represented by the horizontal line. Deviations from normality may fall above or below this line. Data from a distribution that is statistically normal will appear spread above and below the horizontal line in an apparent random fashion. KolmogoroveSmirnov and ShapiroeWilk tests for normality both show that all three plots deviate from normality (P < 0.001); however, Level 3 is much closer to normality than either Levels 1 or 2.

obtained from experienced practitioners (Level 3) reﬂect a normal statistical distribution, as would be expected from a healthy human subject population. The less experienced practitioner groups (Levels 1 and 2) contain higher frequency readings, with the least experienced group (Level 1) containing the greatest proportion of such readings. The tendency of novice practitioners to report higher CRI rates relative to experienced practitioners may represent an

inability of less experienced practitioners to ﬁlter out other rhythmic phenomena, such as respiration from the subject, or rhythms from their own bodies. Or it may reﬂect a tendency for certain beginners to apply manual force in anticipation of the CRI cycle, to lead the CRI cycle as opposed to merely following it. Also of note is the fact that it was only in the Level 1 group that examiners failed to palpate any rate for the CRI.

N. Sergueef et al. / International Journal of Osteopathic Medicine 14 (2011) 10e16

The data were gathered at several geographic locations as part of educational programs conducted by the same individual (NS). Training by one instructor raises the following question: Were the results due to the inﬂuence of that instructor? Published data suggest that this is not the case.18 The accuracy of the palpated CRI rates of examiners in this study, particularly that of Level 3, is supported by the comparable mean of the aforementioned study involving experienced practitioners (44 U.S. trained, osteopathic physicians, each with a different subject, see Table 1, Nelson et al.). The results of the current study for Level 3 examiners are 4.78 2.57 cycles/min: The comparable study reports 4.54 2.08 cycles/min.18 The limitations of this study are as follows: (1) Sample size among experience levels was not equal, potentially affecting computed P values; however, it is unlikely, given the magnitude of the differences among the means and deviations of the three groups that equalizing the group sizes will alter the principal ﬁndings. (2) The rate was silently counted in the examiner’s head and reported at the end of the designated time period. This leaves room for error in reporting, should the examiner lose count at some point during the measurement period, although the relatively short data acquisition period (3 min) greatly minimizes this risk. There is always the possibility that an examiner could misunderstand the instructions, perhaps counting half-cycles, i.e., ﬂexion-1, extension2, ﬂexion-3, etc. The fact that the means are relatively close for all groups appears to indicate that this did not happen to any great extent. (3) No repetitive measurement tests were performed. Consequently the data for each individual is limited to a single data point. [A kappa analysis for interexaminer reliability was not attempted for this study because other attempts to do so by our laboratory have shown that the extended (repeated) examination time demanded by such a repetitious protocol fatigues both the examiner and the subject, increasing the variance of measurement as time progresses and lowering the power of the statistical analysis to the point where the analysis becomes useless.19] (4) Examiner bias existed in this study. Students were, in the course of their studies, taught “accepted” values for the CRI. The values taught were consistent with those published previously in the original study by Woods and Woods8 and in recognized textbooks, 10e14 cpm.5,9,10 The results of this study are, however, decidedly lower, 2.43e11.33 cpm, and the values obtained by experienced examiners are even lower, 2.21e7.35 cpm, The fact that the examiners were unaware of the time they would be palpating, minimizes the issue of the examiner’s pre-expectations. The only way an individual could have manifested such a bias would have been to have looked at their watch during the protocol and manufacture what they thought was the “correct” rate. To the best of our knowledge, this did not happen. (5) The possibility of entrainment exists between the examiner and subject that could carry over when the individuals changed positions during the second part of the protocol, thereby inﬂuencing the second data set. Although this possibility exists we believe that the intervening positional changes that the participants experienced combined with the length of time between the termination of the ﬁrst rate recording period and the completion of the subsequent data gathering was sufﬁciently long to mitigate any such entrainment. That this study and the previous comparable study18 demonstrate a decidedly lower rate for the CRI than the generally accepted rate needs to be explained. In our past studies, where we have documented a relationship between the CRI and low frequency oscillations (Traube-Hering-Mayer) in bloodﬂow velocity, we have demonstrated that the .1e.15 Hz component of these complex wave forms is of a relatively constant frequency,18e20,22e24 although a 20% frequency modulation in the waveform has been noted.19 The fact that palpation of the CRI by experienced examiners tracks the .1e.15 Hz oscillation, but

15

consistently at one-half its frequency, is perplexing.18,19 It is of interest to note that we have identiﬁed a signal at .08 Hz that was resolved in ﬂowmetry data but not reported in earlier work with lower reported signal-to-noise resolution.20 That frequency, .08 Hz, is 4.80 cpm, a frequency that is strikingly close to the mean value (4.78 cpm) reported in this study and that (4.54 cpm) reported in our previous study.18 It appears that it is this .08 Hz signal that the examiners may be tracking. 6. Conclusions This study demonstrates that the distribution of the palpated rate for the CRI narrows as examiners become more experienced. Experienced examiners yield rates that fall upon a normative line of distribution that is more tightly grouped. Additionally, it is of interest to note that the rate of the CRI reported by experienced examiners in this study is essentially identical to the rate reported from our previous study.18 Experienced examiners appear to be tracking the CRI at a rate that is coincident with a .08 Hz (4.8 cpm) signal identiﬁed by laser-Doppler ﬂowmetry within cutaneous bloodﬂow velocities.20 The increased precision of CRI palpation with examiner experience indicates that the phenomenon that is being reported is, in fact, being perceived. Further, from the values reported, the accepted normative rate for the CRI should be lowered to 2e7 cpm. References 1. Ferre JC, Barbin JY. The osteopathic cranial concept: fact or ﬁction? Surg Rad Anat 1991;13:165e70. 2. Green C, Martin CW, Bassett K, Kazanjian A. A systematic review and critical appraisal of the scientiﬁc evidence on craniosacral therapy. Joint Health Technology Assessment Series. Vancouver, BC: British Columbia Ofﬁce of Health Technology Assessment (BCOHTA 99:1J); 1999. pp. 1e55. 3. Green C, Martin CW, Bassett K, Kazanjian A. A systematic review of craniosacral therapy: biological plausibility, assessment reliability and clinical effectiveness. Complement Ther Med 1999;7:201e7. 4. Hartman SE, Norton JM. Interexaminer reliability and cranial osteopathy. Sci Rev Alt Med 2002;6:23e34. 5. King HH, Lay EM. Osteopathy in the cranial ﬁeld. In: Ward RC, editor. Foundations for osteopathic medicine. 2nd ed. Baltimore, MD: Lippincott, Williams & Wilkins; 2003. p. 985e1001. 6. Educational Council on Osteopathic Principles (ECOP) of the American Association of Colleges of Osteopathic Medicine (AACOM). Glossary of osteopathic Terminology. Chevy Chase, MD: AACOM, www.aacom.org; 2009. See also. 7. Sutherland WG. The cranial bowl. Mankato, MN: Free Press Company; 1939. reprinted 1986. 8. Woods JM, Woods RH. A physical ﬁnding relating to psychiatric disorders. J Am Osteopath Assoc 1961;60:988e93. 9. Magoun HI. Osteopathy in the cranial ﬁeld. 2nd ed. Kirksville, MO: The Journal Printing Company; 1966. 10. Sergueef N. Le B.A.BA du crânien. Paris, France: SPEK; 1986. 11. Norton JM, Sibley G, Broder-Oldach R. Characterization of the cranial rhythmic impulse in healthy human adults. AAO J 1992;2:9e12. 26. 12. Wirth-Pattullo V, Hayes KW. Interrater reliability of craniosacral rate measurements and their relationship with subjects’ and examiners’ heart and respiratory rate measurements. Phys Ther 1994;74:908e16. 13. McAdoo J, Kuchera ML. Reliability of cranial rhythmic impulse palpation. J Am Osteopath Assoc 1995;95 (Abs):491eEOA. 14. Hanten WP, Dawson DD, Iwata M, Seiden M, Whitten FG, Zink T. Craniosacral rhythm: reliability and relationships with cardiac and respiratory rates. J Orthop Sports Phys Ther 1998;27:213e8. 15. Rogers JS, Witt PL, Gross MT, Hacke JD, Genova PA. Simultaneous palpation of the craniosacral rate at the head and feet: Intrarater and interrater reliability and rate comparisons. Phys Ther 1998;78:1175e85. 16. Sommerfeld P, Kaider A, Klein P. Inter-and intraexaminer reliability in the palpation of the “primary respiratory mechanism” within the “cranial concept”. Man Ther 2004;9:22e9. 17. Moran RW, Gibbons P. Intraexaminer and interexaminer reliability for palpation of the cranial rhythmic impulse at the head and the sacrum. J Manipulative Physiol Ther 2004;24:183e90. 18. Nelson KE, Sergueef N, Glonek T. Recording the rate of the cranial rhythmic impulse. J Am Osteopath Assoc 2006;106:337e41. 19. Nelson KE, Sergueef NS, Lipinski CM, Chapman AR, Glonek T. The cranial rhythmic impulse related to the Traube-Hering-Mayer oscillation: Comparing

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laser-Doppler ﬂowmetry and palpation. J Am Osteopath Assoc 2001;101: 163e73. 20. Nelson KE, Sergueef N, Glonek T. The effect of an alternative medical procedure upon low-frequency oscillations in cutaneous blood ﬂow velocity. J Manipulative Physiol Ther 2006;29:626e36. 21. SPSSÒ Base 8.0 Applications Guide. Chicago, IL: SPSS Inc.; Copyright Ó; 1998. 32,57e58.

22. Sergueef N, Nelson KE, Glonek T. The effect of cranial manipulation upon the Traube Hering Mayer oscillation. Alt Ther Health Med 2002;8:74e6. 23. Nelson KE, Sergueef N, Glonek T. Cranial manipulation induces sequential changes in blood ﬂow velocity on demand. AAO J 2004;14:15e7. 24. Sergueef N, Nelson KE, Glonek T. The effect of light exercise upon blood ﬂow velocity as measured by laser-Doppler ﬂowmetry. J Med Eng Tech 2004;28: 143e50.

International Journal of Osteopathic Medicine 14 (2011) 17e23

Contents lists available at ScienceDirect

International Journal of Osteopathic Medicine journal homepage: www.elsevier.com/ijos

Research report

An evaluation of osteopathic school programs designed to promote rural location by graduates Brian E. Whitacre a, *, Vicky Pace b, Jeffrey B. Hackler b, Matthew Janey b, Chad E. Landgraf b, William J. Pettit b a b

Department of Agricultural Economics, 504 Ag Hall, Oklahoma State University, Stillwater, OK 74074, USA Center for Rural Health, Oklahoma State University Center for Health Sciences, Tulsa, OK, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 28 September 2009 Received in revised form 24 November 2010 Accepted 25 November 2010

Background: Many osteopathic medical schools across the United States seek to produce physicians who will ultimately locate in rural areas. Most of these schools offer courses and programs designed to promote rural location. Objective: To explore how mandatory and optional programs offered by Oklahoma State University (OSU) College of Osteopathic Medicine (and student perception of them) impacted the location decisions of students graduating from the osteopathic program between 1997 and 2002. Methods: Data on student hometowns, medical school schedules and course evaluations, and current practice location were obtained for 190 OSU osteopathic graduates. Logistic regression was used to ﬁnd factors that were signiﬁcant in predicting the location decision. Results: Of the 190 students in the dataset who are now practicing physicians, approximately 30% chose to practice in a rural location. The regression results suggest that an optional summer program during a student’s ﬁrst year in which they spend 4 weeks in a rural primary care setting increases their probability of locating in a rural area by roughly 24%. There is also some evidence that a more positive overall experience in the ﬁrst one-month rotation in a rural community hospital improves the likelihood of rural location. Conclusions: The ﬁndings show that programs implemented by an osteopathic school can inﬂuence where graduates choose to practice. In particular, programs taking place in both the 1st and 4th year of training have an impact on rural practice location, implying that students can be inﬂuenced both early and late in their medical school careers. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Osteopathic school Curricula Location decision Rural

1. Introduction The shortage of physicians in rural areas is a well-documented problem in the United States. While 20% of Americans live in rural parts of the country, only 9% of physicians practice there.1 The result of this imbalance is that more than 1/3 of the rural U.S. population base of 60 million people live in a federally designated Health Professional Shortage Area (HPSA).2 This problem is exacerbated by the fact that rural Americans are generally older and have less income than their urban counterparts.3 The future of rural physicians is also in question, with fewer medical students entering the ﬁeld of primary care and the increasing level of medical student

* Corresponding author. Tel.: þ1 405 744 9825; fax: þ1 405 744 9835. E-mail address: [email protected] (B.E. Whitacre). 1746-0689/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ijosm.2010.11.007

debt e particularly since rural physicians already make lower unadjusted salaries than those practicing in urban areas.4e6 Several medical school programs across the country have attempted to address this problem by focusing their attention on producing rural physicians. Osteopathic schools, such as the Oklahoma State University College of Osteopathic Medicine (OSU COM), are known to produce physicians that are signiﬁcantly more likely than their allopathic counterparts to settle and remain in rural areas.7 The methods medical schools presume to be effective at producing rural doctors are varied, but include encouraging students to complete rotations in rural hospitals, allowing them to partake in internships with rural preceptors, and providing full courses dealing speciﬁcally with issues that rural doctors may face (such as setting up a practice on your own). However, few studies have focused explicitly on how well these tactics have performed in encouraging a soon-to-be graduate to ultimately locate in a rural area. One reason for this lack of empirical evidence is simply the

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time it takes to collect the relevant data e a medical student typically takes at least 4 years to graduate medical school and 3 or more years to complete a primary care residency before settling into practice. Thus, data on the courses a student took during medical school are only of use some six years later at the earliest, when a new doctor ﬁnally makes a practice location decision. Further, mandatory and optional courses provided by medical schools to promote rural physicians vary widely and documentation on how the courses are perceived by students is sometimes lagging. This paper uses a unique dataset to examine the courses (and evaluations of those courses) that osteopathic medical school students took over their careers, and whether or not they had an impact on the rural e urban location of their practice. Merging sources of data from the OSU COM, the ﬁnal dataset is composed of a list of 190 graduates between 1997 and 2002, their practice location as of 2008, other background information (including whether they were raised in a rural hometown), and information on the courses and evaluations performed throughout their medical school careers. 1.1. Existing research The majority of the literature on promoting rural physicians has focused on the impact of the medical student’s background e in particular, whether or not they were raised in a rural area. This relationship has been documented early and often, with Steinwald and Steinwald8 ﬁnding in 1975 that the two most signiﬁcant factors for physician placement were specialty type and place of rearing. A decade later, Leonardson, LaPierre, and Hollingsworth9 conﬁrmed that the size of the community where the physician grew up was a signiﬁcant factor for determining location. More recently, Easterbrook et al.10 found that physicians from hometowns of less than 10,000 were 2.3 times more likely to choose a rural practice for their ﬁrst practice than those coming from larger hometowns. A similar result was found for Australian doctors, with a summary of 12 studies conﬁrming that the likelihood of working in a rural practice is twice as high for doctors with a rural background.11 Further, a variable for self-identiﬁcation of having grown up in a rural area proved to be the only signiﬁcant predictor for eventual rural practice in a study of 599 Virginia medical school graduates.12 However, Chan et al.13 indicate that while students with rural upbringing were more likely to have some interest in rural practice, a large percentage of urban-born physicians claimed that rural medical training had a large inﬂuence on their decision to practice in a rural area. Additionally, Rosenthal, McGuigan, and Anderson14 ﬁnd that most graduates of “rural training tracks” (including a twoyear residency in a rural area) ultimately locate their practice in a rural community. Another important factor that mitigates the choice of a rural practice is the nature of the medical education that a physician receives as a medical student. Much of the current literature focuses on the allopathic (M.D.) approach to medical education; the osteopathic (D.O.) approach to medical education and its role in the selection of a rural practice setting garners minimal scholarly research.15 While many of the biomedical and clinical education components of osteopathic and allopathic medical education are nearly identical, osteopathic medical education is based on the basic philosophy that the musculoskeletal system, through the nervous and circulatory system, interacts with body organs and systems in health and disease.16 Further, osteopathic medical education emphasizes the primary care tradition and is grounded in service to the underserved (which includes rural). Many osteopathic medical schools actively recruit and select individuals who are likely to enter one of the primary care

specialties.17 Similarly, Bowen18 demonstrates that students drawn to osteopathic medicine are often predisposed to selecting a rural practice. Osteopathic medical students are generally older, have “birth origins” that are predominately rural or underserved, and come from lower- or middle-income upbringing. The interaction between gender and osteopathic medical education also appears to be an important determinant of rural primary care practice. Research from Texas indicates that female osteopathic physicians were 2.5 times more likely to select a rural primary care practice as compared to female physicians trained at allopathic medical schools.19 However, while most osteopathic studies on this subject document how sociodemographic characteristics inﬂuence rural location, research into the role of individual school programs is lacking. Thus, while the literature acknowledges that a rural upbringing is a signiﬁcant factor in determining physician location, the extent to which an osteopathic medical school may impact this decision by implementing various programs is still in question and solicits additional research. This paper investigates ﬁve types of rural programs implemented by the OSU COM, and examines how they have been rated by the students progressing through them. These programs and evaluations are then used in conjunction with hometown data and the ultimate location of the physician to determine whether they are having a statistical impact on rural location. The programs themselves are described in the following section. 1.2. OSU COM rural programs Oklahoma State University has several innovative programs that attempt to encourage rural location by physicians upon graduation and completion of residency. Several of these programs are optional, while others are mandatory. They include: (1) Summer Rural Externship e optional (2) Early Clinical Experience e optional (3) Community Clinic Clerkship e mandatory (4) Rural Clinic Clerkship e mandatory (5) Community Hospital rotations e mandatory. A brief summary of each program provides more information about them, such as when the programs are typically encountered by students and the responsibilities of the students enrolled. In these summaries, “rural setting” is deﬁned as a community with a population of less than 50,000 (following the current U.S. Census deﬁnition), although the majority of programs are based in significantly smaller towns. In comparison, “urban” settings are deﬁned as communities with populations larger than 50,000. 1.2.1. Summer Rural Externship (optional) The Summer Rural Externship (SRE) is a program that places a student in a community-based rural setting with a primary care physician. The student observes/works with the local physician between 30 and 35 h per week for four weeks. The course takes place during the summer following the ﬁrst year of medical school. Housing is provided for the student in the local community. This rotation is also geared towards community involvement through 6e8 h of community engagement each week, which provides the student with a better understanding of the resources available to them, the role of the physician in a rural community, and an opportunity to observe some of the beneﬁts and challenges of practicing in a rural area. The externship requires students to write a 6-10 page report at the end of the experience to describe what they learned and discuss their current opinions of rural medicine. While all SREs occurring between 1997 and 2002 were held in rural areas (based on the deﬁnition of 50,000 population), 55% took place in communities of less than 10,000 people.

B.E. Whitacre et al. / International Journal of Osteopathic Medicine 14 (2011) 17e23

19

Fig. 1. 2008 Practice Locations in Oklahoma by Rural/Urban Hometown Designation for OSU College of Medicine Graduating Classes 1997e2002.

1.2.2. Early Clinical Experience (optional) Early Clinical Experience (ECE) is a ﬁve-day tour of different physician ofﬁces across the state. Students listen to the physicians discuss career topics and how/why they made their own location decisions. This experience takes place during the summer following the ﬁrst year in medical school. 1.2.3. Community Clinic Clerkship (mandatory) This one-month rotation is performed during a student’s 3rd year in medical school. This clerkship introduces students to concepts and issues relevant to a rural practice that is close to urban resources. Weekly lectures are provided and allow for comparison of urban and rural practice. This clerkship is typically offered in the area surrounding the urban base of OSU COM (Tulsa, OK), so that weekly meetings can still be held to maintain consistency and drive home important points throughout the rotation. A case presentation is made by the student to OSU COM at the end of the month. 1.2.4. Rural Clinic Clerkship (mandatory) This one-month rotation is also performed during a student’s 3rd year in medical school after the student has completed the Community Clinic Clerkship. The general purpose is to give students direct involvement and experience in a functioning rural family practice that does not have access to large urban resources. During this rotation, housing is provided for students and may consist of a hospital room or a room with a local host family. Participation in community-based activities is expected, and a case presentation is once again required. 1.2.5. Community Hospital Rotations (mandatory) These two consecutive one-month rotations take place during the 4th year of medical school. The rotations are typically done in the same hospital and with the same supervising physician, but students work with different doctors throughout the hospital. The primary purpose behind the rotations is to give 4th year students direct involvement and experience in a small community hospital.

The responsibilities of the student are dictated by the on-site supervising physician, and can range from simple paperwork to assistance in complex medical procedures. Housing is typically provided either on-site (at the hospital) or with a local community member. While the ﬁrst two programs mentioned (SRE and ECE) are optional, the last three are mandatory for all OSU COM medical students. The three mandatory programs require all students to evaluate their rotation, allowing for variation among the students about how useful they felt each program was. The site evaluation questionnaire is based on a 4-point Likert scale, where students can either strongly agree, agree, disagree, or strongly disagree with a given statement. Site evaluations ask students questions such as whether their orientation was appropriate, whether they received effective personal instruction at the site, whether the formal education they received was useful, and whether the experience was a good one overall. Students were also asked whether they would recommend the program to future medical school classes. This large number of questions allows for a multitude of variables to be used to deﬁne an “effective” program in the regression analysis that follows. 2. Methods 2.1. Data sources Several datasets were merged in order to complete this analysis. The ﬁrst dataset used was a list of 289 practicing physicians in the state of Oklahoma that graduated from OSU COM between 1997 and 2002. This data came from a larger list of all practicing osteopathic physicians in the state as compiled by the Oklahoma Osteopathic Association. It was then reduced to only those physicians who graduated from OSU COM during this speciﬁc time period so that it could be combined with data from the school. One of the largest beneﬁts of this dataset is that it includes a physical address of the physician’s practice, thus allowing for easy identiﬁcation of

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B.E. Whitacre et al. / International Journal of Osteopathic Medicine 14 (2011) 17e23

Fig. 2. Physician Hometowns by Rural/Urban Designation for OSU College of Medicine Graduating Classes 1997e2002..

whether they are practicing in a rural area. As previously noted, this study uses the current U.S. Census’ deﬁnition of “rural,” which has a city threshold of 50,000 population. Thus, any practice located in a city with an ofﬁcial Census 2000 population of less than 50,000 was classiﬁed as being in a rural area. Approximately 34% of the 289 physicians in our initial dataset were working in a rural location (Fig. 1). This list of 289 practicing physicians was then matched to data regarding their curricula during their time at OSU COM. In

particular, whether or not they participated in the two optional programs (SRE and ECE) was noted. Further, their evaluations for each of the 3 mandatory programs (community clinic, rural clinic, and community hospital) were obtained by mapping their names or ID numbers to the appropriate year and evaluation. The ﬁnal dataset to complete the analysis was a listing of the hometowns of all OSU COM students, obtained from their 1st year records. Again, the Census deﬁnition of rural was used, with cities having population levels of 50,000 or more classiﬁed as urban (Fig. 2).

Table 1 Course Evaluations, Participation, and Hometown Status for OSU Osteopathic Graduates (1997e2002). Mandatory course evaluations

Community clinic Clerkship

Rural clinic clerkship

Community hospital I

Community hospital II

Appropriate orientationa Effective personal instructiona Demonstration of osteo. techniquesa Formal educationa Overalla Recommend # observations

3.64 3.66 3.38 3.42 3.64 0.94 47

3.66 3.75 3.42 3.41 3.80 0.96 167

3.53 3.64 3.20 3.37 3.58 0.94 149

3.58 3.68 3.13 3.35 3.60 0.96 159

Optional Course Participation Summer Rural Externship Early Clinical Experience Rural Hometown Rural Practice a

0.10 0.17 0.58 0.30

Course evaluations are scored on a 4-point Likert scale (strongly agree, agree, disagree, strongly disagree). where strongly agree ¼ 4. Recommend is a 0/1 variable.

B.E. Whitacre et al. / International Journal of Osteopathic Medicine 14 (2011) 17e23

21

Table 2 Logit Model Parameter Estimates for Likelihood of Rural Practice. (1) Rural Home Summer Rural Externship Early Clinical Experience CC - Overall RC - Orientation RC - Personal Instruction RC - Osteopathic Techniques RC - Formal Education RC - Overall CHI - Orientation CHI - Personal Instruction CHI - Osteopathic Techniques CHI - Formal Education CHI - Overall CHII - Orientation CHII - Personal Instruction CHII - Osteopathic Techniques CHII - Formal Education CHII - Overall Constant Pseudo R2 Percent Correctly Predicted Rural Practice Urban Practice Number of Observations

0.583*

(2)

(3)

(4)

0.239 1.839 0.850 0.541

0.633* 1.020* 0.103

0.849* 1.515** 0.214

(5) 3.430** 3.160** 1.311 0.255 0.743 0.531 0.437

1.155

0.374 1.142 0.457 1.198 0.986

2.809*

1.245* 0.046 3.360 0.445 0.688

1.197**

1.336**

1.071 14.191**

0.157 7.451**

0.014

0.031

0.200

0.107

0.00 1.00 163

0.08 0.96 163

0.55 0.92 36

0.12 0.99 106

17.918* 0.265 0.50 0.81 53

** and * indicates statistical signiﬁcance at the p ¼ 0.05 and p ¼ 0.10 levels, respectively. CC ¼ Community Clinic; RC ¼ Rural Clinic; CHI ¼ Community Hospital rotation I; CHII ¼ Community Hospital rotation II.

Combining all of these datasets left a high number of observations with missing information. Incomplete evaluations or missing hometown information rendered many data points unusable. From the initial list of 289 practicing physicians, only 190 (66%) were able to be matched to a relevant ID number for the school and at least 1 course evaluation. Summaries of course participation, course evaluations, and rural backgrounds for these 190 students are shown in Table 1. Ten percent of these students opted to participate in the Summer Rural Externship program, and 17% participated in the Early Clinical Experience program. Evaluations of the 3 mandatory programs (including two rotations in community hospitals) were generally positive, with all programs’ overall ranking higher than 3.5 on the 4-point Likert scale and between 94 and 96% recommending the rotation. However, some evaluation questions had signiﬁcantly lower scores, such as whether the student was asked to demonstrate osteopathic techniques during the rotation and whether the formal educational programs (rounds, lectures, etc.) were appropriate and useful. Additionally, as indicated by the number of observations for each group, there were wide variations in the number of completed evaluations for the 3 mandatory programs. The Rural Clinic Clerkship rotations had the most completed evaluations with 167, while the Community Clinic Clerkship had only 47 complete evaluations. The hometown was identiﬁed for 163 of the 190 students, with 58% coming from rural cities. Nearly 1 out of 3 (30%) maintains a practice in a rural community in Oklahoma. Given the similarity of this percentage to that for the full dataset of 289 physicians (34%) and a lack of any discernable pattern to those physicians omitted, there is little concern that using only a subset of the initial dataset will bias the results. 2.2. Methodology To determine what courses (or parts of courses) might impact the location decision of an osteopathic graduate, we use a standard logit framework for analyzing binary decision variables. The dependent variable in this case is whether the graduate ends up in a rural or urban area (¼1 if rural, ¼ 0 if urban). This variable is then

regressed against a series of independent variables such as participation in the optional courses, and the resulting parameter values and statistical signiﬁcance will indicate whether the variables positively or negatively inﬂuence the location decision e or if they do not inﬂuence the decision at all. The model is formally speciﬁed as:

y*i ¼ Xi b þ Zi1 a1 þ Zi2 a2 þ Ei1 s1 þ Ei2 s2 þ Ei3 s3 þ Ei4 s4 þ 3i (1) yi ¼ 1

if y*i 0

yi ¼ 0

if y*i < 0

where y*i is a latent measure of the beneﬁts and costs associated with practicing in a rural area for physician i. Although this variable is not observed, we do observe the actual location of the physician (yi), which equals 1 if the beneﬁts of practicing in a rural area outweighs the costs. On the right hand side of the equation is the hometown rural/urban status of physician i (Xi), his participation in SRE and ECE programs (Zi1,Zi2) his evaluations of the four mandatory programs (Ei1,Ei2,Ei3,Ei4) and the statistical model’s error term ð3i Þ. The associated parameter vectors of the model ðb; a1 ; a2 ; s1 ; s2 ; s3 ; s4 Þ will provide information about how each independent variable impacts the perceived value of practicing in a rural area when estimated. A simple adjustment to the model allows for the inclusion of multiple evaluations from a single mandatory program, such as the 5 categories displayed in Table 1. In a case with all 5 evaluations included for each program, there would be 20 separate Ei variables (5 evaluations 4 programs). To determine the impact of the individual programs, we ﬁrst run a model including the physician’s hometown status (Xi) as the only explanatory variable. We then add in the optional programs (Zi1,Zi2) and ﬁnally various mandatory evaluations (Ei1,Ei2,Ei3,Ei4) to see if the associated parameter values are signiﬁcant in helping to promote rural location. If the programs are having the desired

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impact, then we would expect to see a positive and statistically signiﬁcant coefﬁcient on the optional programs (indicating that participation positively impacted the likelihood of rural practice) and on the mandatory evaluations (indicating that a more positive evaluation resulted in a higher probability of rural practice). 3. Results The results of 5 separate models are shown in Table 2 below. The initial model (1) includes only a variable for whether or not the physician was raised in a rural area. As expected, this variable is positive and signiﬁcant at the 10% level, indicating that being raised in a rural area increases the likelihood of ultimately practicing in one. In logit models such as this one, the parameters themselves are ratios of logged odds and are not easily interpreted. Instead, we turn to marginal effects. These effects estimate the change in the dependent variable (in this case the probability of practicing in a rural area) based on a change in the independent variable. The marginal effect of being raised in a rural area is 0.119 (not shown in Table 2), suggesting that students raised in a rural area are 11.9% more likely to end up with a rural practice than those raised in an urban environment. Other summary statistics show that this model may not be the best ﬁt, however, with a pseudo R2 value of 0.014 e roughly implying that the lone independent variable explains only about 1.4% of the variation in the dependent variable. Further, while this model does a good job of predicting who will locate in an urban area (100% correctly predicted), it fails to correctly predict anyone who will locate in a rural area (0% correctly predicted). The second model adds in variables for participation in the optional Summer Rural Externship (SRE) and Early Clinical Experience (ECE) programs. The results from this model include a positive and statistically signiﬁcant impact of a rural home (similar to the ﬁrst model) and for participation in the SRE. The associated marginal effect for SRE implies that a student’s participation in this program raises the likelihood of practicing in a rural area by 23.9%. No statistically signiﬁcant result is found for the ECE program, indicating that participation does not impact the location of practice. Further, both the pseudo R2 and the percent correctly predicted increase for this model, suggesting the inclusion of the optional programs improved the overall ﬁt. The third model adds overall evaluation variables for all 4 mandatory programs. Unfortunately, the lack of completed Community Clinic evaluations leaves a much smaller dataset, with only 36 observations. Although the ﬁt of the model is much improved (pseudo R2 of 0.20, 55% of rural practices correctly predicted), the minimal number of observations renders both rural home and summer rural experience insigniﬁcant, suggesting that in this speciﬁcation they do not impact the likelihood of setting up a rural practice. Only the overall evaluation of Community Hospital I is signiﬁcant at the 10% level. However, the lack of signiﬁcance of SRE and rural upbringing combined with the small sample size leaves this speciﬁcation inferior. The fourth model excludes the problematic Community Clinic evaluation from the remaining evaluation variables for mandatory programs, thereby increasing the overall sample size to 106 observations. Results from this speciﬁcation again include an increased probability of rural practice for those raised in a rural area and for those participating in the SRE e this time signiﬁcant at the 5% level. Further, the evaluations of the ﬁrst Community Hospital rotation are signiﬁcant at the 10% level, implying that a more positive evaluation implies a higher likelihood of rural location. The overall ﬁt of this model is good, with a pseudo R2 of 0.107, and improvements to the percent correct predictions from model (2). The associated marginal effects (not shown in Table 2) show that in this speciﬁcation, participation in the SRE increases the probability

of rural practice by 32.4%, while a one point increase in the overall evaluation of the ﬁrst Community Hospital rotation leads to a 20% increase in the probability of rural practice. The ﬁfth and ﬁnal model uses lower-level evaluations from Rural Clinic and Community Hospital rotations 1 and 2 in hopes of identifying speciﬁc portions of these programs that may lead to a higher likelihood of rural location. Unfortunately, the sample size is again small due to a lack of complete evaluations (53 observations) and no individual evaluation portion is signiﬁcant in explaining rural location. However, both rural home and SRE are now signiﬁcant at the 5% level, and the model has a strikingly good ﬁt with a pseudo R2 of 0.265 and 50% of rural location correctly predicted. This result gives credence to the basic result that both a rural upbringing and participation in the SRE positively impact the probability of rural location. Multiple other models were estimated that are not shown in Table 2, such as including various types of course evaluations (e.g., only the orientation portion, or only the overall recommendation) with ﬁndings either consistent to those discussed above or with no signiﬁcant variables. Thus, in general, the models displayed in Table 2 represent the best array of speciﬁcations for looking at the impacts of various programs. 3.1. Limitations Several limitations of the study exist. Perhaps most importantly, the fact that the SRE and ECE programs are optional introduces the possibility of self-selection bias. In other words, students predisposed to practicing in a rural area may be more likely to choose these optional programs. This potentially biases the inﬂuence of the SRE or ECE coefﬁcients, since the variables are capturing more than simple program participation. Another limitation resides in the fact that the models displayed in Table 2 generally have different sample sizes due to the varying level of survey completion for the mandatory programs. Thus, we are not using the same sample of students to estimate each model. Comparing results across models using different sample sizes is not ideal; however, econometrically this is only a minor concern since the remaining data points are still randomly drawn from the overall student population. Finally, due to data availability, this study fails to account for other factors that could potentially inﬂuence the rural location decision; namely the location of residency training and specialty choice. 4. Discussion A multitude of options and courses are made available to osteopathic medical school students across the nation in the hopes that they may positively inﬂuence the likelihood of rural location after graduation. This paper has sought to explore how the programs employed by the Oklahoma State University College of Osteopathic Medicine ultimately impact the location decision of its physician graduates. The results suggest that participation in one optional program, the Summer Rural Externship, positively inﬂuenced the likelihood of a physician ending up in a rural location. This program takes place early in medical school (during the summer of the student’s 1st year). Given its consistent signiﬁcance in the results, other osteopathic schools may want to pursue similar programs to improve their rural location rates. Although the mandatory programs provided by the school generally lacked signiﬁcance in promoting rural location, there is some evidence to suggest that an increasingly positive overall experience in the ﬁrst Community Hospital rotation does improve the likelihood of graduates practicing in a rural community. This contribution is particularly intriguing given its placement in the 4th and ﬁnal year of training, indicating that students are still amenable to inﬂuence relatively late in their medical school career.

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A lack of signiﬁcance for other programs does not necessarily mean that they are not serving their purpose and should be removed. Rather, the consistently high evaluations imply that most experiences are viewed similarly by graduates regardless of where they choose to practice and this lack of variation may prevent meaningful insight into their impact. Future efforts to identify mandatory course components that might affect rural location should focus on discussing the importance of these evaluations with students, and different methods of ranking should be considered. Further, when each of the ﬁve programs discussed in the analysis were initially implemented, little consideration was given to speciﬁc characteristics of the individuals offering their services. For example, the SRE took place in locations where the preceptors were willing to participate, not necessarily because they practiced in a small town. Given this lack of formal criteria for participation in the programs, evaluating the location of future programs in advance may focus them more effectively on producing future rural physicians. One ﬁnal potential course of research for future studies is to incorporate varying deﬁnitions of rural, including how the analysis deﬁnes where students grew up, where the medical school programs occur, and where graduates ultimately practice. Using ruraleurban commuting area (RUCA) codes or other measures of rurality as opposed to the 50,000 population threshold applied here could result in different and interesting results. This type of analysis might be particularly useful if speciﬁc deﬁnitions (such as RUCA codes) are used to identify future rural preceptors or hospitals in hopes of inﬂuencing physician location within a precise rural category, as suggested above. Author contribution statement VP, JH, CL, and WP conceived the idea for the study. BW, VP, JH, and CL designed the study. All authors compiled data for the study. BW and VP analyzed the data and provided statistical analysis. BW wrote the ﬁrst draft of the manuscript. All authors edited and approved the ﬁnal version of the manuscript. Acknowledgements This research was partially supported by a technical assistance grant from the Health Resources and Services Administration; its content is the responsibility of the authors and does not necessarily

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represent the ofﬁcial views of the Health Resources and Services Administration.

References 1. Gazewood J, Rollins L, Galaska S. Beyond the horizon: the role of academic health centers in improving the health of rural communities. Acad Med 2006;81:793e7. 2. Federal Ofﬁce of Rural Health Policy. Facts about.rural physicians. Available at: http://www.shepscenter.unc.edu/research_programs/rural_program/phy.html; 2008 [accessed 09.09.08]. 3. Rabinowitz H, Diamond J, Markham F, Wortman J. Medical school rograms to increase the rural physician supply: a systematic review and projected impact of widespread replication. Phys Supply 2008;83:235e43. 4. Whitcomb M. The challenge of providing doctors for rural America. Acad Med 2005;80:715e6. 5. Association of American Medical Colleges. Association of American medical colleges matriculation questionnaire 2005: all schools. Available at: http://www. aamc.org/data/msq/allschoolsreports/msq2005.pdf; 2008 [accessed 09.09.08]. 6. Reschovsky J, Staiti A. Physician incomes in rural and urban America. Cent for Studying Health Syst Change (Issue Brief) 2005;92:1e4. 7. Hart L, Salsberg E, Phillips D, Lishner D. Rural health care providers in the United States. J Rural Health 2002;18:211e32. 8. Steinwald B, Steinwald C. The effect of preceptorship and rural training programs on physicians’ practice location decisions. Med Care 1975;13: 219e29. 9. Leonardson G, LaPierre R, Hollingsworth D. Factors predictive of physician location. J Med Educ 1985;60:37e43. 10. Easterbrook M, Godwin M, Wilson R, Hodgetts G, Brown G, Pong R, et al. Rural background and clinical rural rotations during medical training: effect on practice location. Can Med Assoc J 1999;160:1159e63. 11. Laven G, Wilkinson D. Rural doctors and rural backgrounds: how strong is the evidence? a systematic review. Aust J Rural Health 2003;11:277e84. 12. Owen J, Conaway M, Bailey B, Hayden G. Predicting rural practice using different deﬁnitions to classify medical school applicants as having a rural upbringing. J Rural Health 2007;23:133e40. 13. Chan B, Degani N, Crichton T, Pong R, Rourke J, Goertzen J, et al. Factors inﬂuencing family physicians to enter rural practice. Does rural or urban background make a difference? Can Fam Physician 2005;51:1247. 14. Rosenthal T, McGuigan M, Anderson G. Rural residency tracks in family practice: graduate outcomes. Fam Med 2000;32:174e7. 15. Chen F, Fordyce M, Andes S, Hart L. U.S. Rural Physician Workforce: analysis of medical school graduates from 1988e1997. Final report #113. Seattle, WA: WWAMI Rural Health Research Center, University of Washington; 2008. 16. Osborne R. A History of the Oklahoma State University College of osteopathic medicine. Stillwater, OK: Oklahoma State University; 1998. 17. Shannon S. Osteopathic medical education in 2009: sails set for improved healthcare? J Am Osteopath Assoc 2009;109:125e7. 18. Bowen R. They really do go. Rural and Remote Health:1035. Available at: http:// www.rrh.org.au, 2008;8 [accessed 03.06.09] (online). 19. Miller T, Hooker R, Mains D. Characteristics of osteopathic physicians choosing to practice in rural primary care. J Am Osteopath Assoc 2006;106:274e8.

International Journal of Osteopathic Medicine 14 (2011) 24e32

Contents lists available at ScienceDirect

International Journal of Osteopathic Medicine journal homepage: www.elsevier.com/ijos

Critical Review

Helical tensegrity as a structural mechanism in human anatomy Graham Scarr* 60 Edward Street, Stapleford, Nottingham, NG9 8FJ, United Kingdom

a r t i c l e i n f o

a b s t r a c t

Article history: Received 31 May 2009 Received in revised form 4 November 2009 Accepted 8 October 2010

Tensegrity is a structural system popularly recognised for its distinct compression elements that appear to ﬂoat within a tensioned network. It is an attractive proposition in living organisms because such structures maintain their energy-efﬁcient conﬁguration even during changes in shape. Previous research has detailed the cellular cytoskeleton in terms of tensegrity, being a semi-autonomous system amenable to such analysis because of its size. It has also been described at higher levels in the extra-cellular/fascial matrix and musculo-skeletal system, but there are fewer syntheses of this. At a fundamental level, the helix and tensegrity share common origins in the geometries of the platonic solids, with inherent hierarchical potential that is typical of biological structures. The helix provides an energy-efﬁcient solution to close-packing in molecular biology, a common motif in protein construction, and a readily observable pattern at many size levels throughout the body. The helix and tensegrity are described in a variety of anatomical structures, suggesting their importance to structural biology and manual therapy. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Filament Geodesic Helix Icosahedron Platonic solid Spiral Structural hierarchy Tensegrity Tetrahedron Tetrahelix

1. Introduction The world of biology is full of weird and wonderful shapes, some with no obvious purpose, and others that suggest some hidden meaning. Even human anatomy has its fair share of the bizarre in the shapes of bones and limbs. How and why does each one develop its characteristic form, and how does that relate to function? Is there more to shape than genetics and Wolffs’ Law? Three thousand years ago, the Greeks believed that just ﬁve archetypal forms could describe everything in the universe, because they were pure and perfect, and part of natural law. Recent research reinstates these physical laws as a major determinant of biological complexity in the sub-cellular realms, and signiﬁcant to structures at higher scales.1e4 Tensegrity (tension-integrity) is a structural mechanism that potentially integrates anatomy from the molecular level to the entire body, and is popularly recognised for its distinct compression elements that appear to ﬂoat within a tensioned network. It is a most attractive proposition in living systems, because such structures automatically assume a position of stable equilibrium, with a conﬁguration that minimizes their stored elastic energy.

* Tel.: þ44 115 9491753. E-mail address: [email protected]. 1746-0689/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ijosm.2010.10.002

Tensegrity structures allow movement, with the minimum of energy expenditure, without losing stiffness or stability.1,5e7 This contrasts with the orthodox view that explains the musculo-skeletal system through classical Newtonian mechanics, using pillars, arches and ﬁxed-fulcrum levers to counteract the force of gravity. In this approach, bones stack on top of one another like a pile of bricks, restrained by soft tissues that permit movement in a local piece-meal like way.8 Comparisons of tensegrity and biological structures show them both to have non-linear visco-elastic properties, with ﬂuid-like movements that result from integration of all components in the system.1,5,6,9 The molecular helix provides an energy-efﬁcient solution to close-packing in biology and also displays tensegrity properties. It is a common motif in protein construction, and a readily observable pattern at many size levels throughout the body. It is proposed that helical tensegrity is a key mechanism in structural biology and consequently has signiﬁcance for manual therapies. 2. The helix The helix is like a coiled spring, or put mathematically, “A spiral curve lying on a cone or cylinder, and cutting the generators at a constant angle” (Walker, 1991).10,11 In biology, it can be appreciated as a regular stacking of discrete components, such as the nucleotides and bases in DNA, or the steps in a spiral staircase.

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Globular proteins, often containing multiple helical domains, can themselves polymerize into helixes (Fig. 1a and b).12 Similar helixes can wind around each other to form coiled-coils (Fig. 1c),13 and assemble into mechanically rigid rods or ﬁlaments, or further combine into more complex structures with specialized functions (Fig. 2). In collagen type I, repeating sequences of amino acids spontaneously form a left-handed helix of procollagen, with three of these helixes combining to form a right-handed helix of tropocollagen. Five tropocollagen molecules then coil in a staggered helical array,14 which lengthens longitudinally by the addition of more tropocollagen to form a microﬁbril, with higher arrangements forming ﬁbrils, ﬁbres and fascicles.15 Collagen appears at several different hierarchical levels within bones, tendons, ligaments and fascia (Fig. 2). 2.1. Structural hierarchies Hierarchies link structures at multiple levels and are widespread in living organisms. They provide an efﬁcient mechanism for packing in 3-D16 by using components that are made from smaller components, with each made from smaller still, often repeating in a fractal-like manner (Fig. 2).1,5,17 Hierarchies enable mechanical forces to be transferred down to a smaller scale with the dissipation of potentially damaging stresses.18e21 At atomic and molecular levels, the basic forces of attraction and repulsion automatically balance those stresses in the most energetically efﬁcient conﬁguration.12,22e24 2.2. Helical tubes The tubular nature of the helix scales up into blood vessels,25 the urinary system and intestinal tract.26,27 Carey (1920) observed left and right-handed helical patterns in the epithelium during formation of the oesophagus and trachea, respectively, in the early embryo.28 In the walls of elastic arteries, such as the aorta, helical collagen reinforcement resists high loads from the pressure of blood. The middle layer organizes into lamellar units, with the orientation of collagen ﬁbres and smooth muscle cells forming a continuous helix. Collagen is more dispersed in the outer adventitia, but still forms two helical groups of ﬁbres.25

Fig. 2. Hierarchical structure of collagen within tendon. Figure 2 reproduced with permission of Elsevier from: Scarr GM. Simple geometry in complex organisms. J Bodyw Mov Ther 2010;14:424e44.

Within the spine, the intervertebral disc contains collagen arranged in concentric lamellae, with opposing orientations in alternate helical layers of 65 (axial).29 The inner lamellae of the annulus ﬁbrosus consist of collagen type II ﬁbres, cross-linked to type IX on the ﬁbre surface, within a highly hydrated proteoglycan matrix; gradually changing to collagen type I ﬁbres in the outer lamellae.30,31 The higher proteoglycan/water content in the inner lamellae acts as a thick-walled pressure vessel containing the nucleus pulposus, while the higher concentration of collagen type I in the outer lamellae provides tensile reinforcement during bending and torsion.29,32 Pressurized tubes cause circumferential and longitudinal stresses in the tube wall that are typically contained by collagen under tension within a helix. Clarke and Cowey (1958) showed that an optimum ﬁbre angle of ∼55 (axial) balances both these stresses, with a reduced angle resisting tube elongation, and a higher angle resisting circumferential and volume increases.33,34 Such helical ﬁbre arrays allow pressurized tubes to bend smoothly without kinking, and resist torsional deformation;32 collagen has itself been described as a tube.35 Cardiac muscle ﬁbre orientation varies linearly between inner and outer walls, from 55 (axial) in one direction to 55 in the

Fig. 1. a) F-actin microﬁlament; b) tubulin microtubule; c) Spectrin tetramer e each strand of alpha and beta spectrin consists of a series of double and triple coiled-coils (supercoils). Figure reproduced with permission of Elsevier from: Scarr GM. Simple geometry in complex organisms. J Bodyw Mov Ther 2010;14:424e44.

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opposite, with tangential spiralling in a transverse plane.36 The entire heart has also been described as a helical coil of muscle with contractions that cause clockwise and anti-clockwise twisting motions.37 This typically produces a left ventricular ejection fraction of 60%, for a muscular contraction of just 15%,38 conﬁrming the mechanical efﬁciency of a helix.

2.3. Tubes within tubes Traditionally considered as mere packing tissue, fascia has been shown to exert considerable inﬂuence over muscle generated force transmission.39e42 It naturally develops into compartments, or ‘tubes within tubes’, particularly noticeable in cross-sections of the limbs. Within muscle, a delicate network of endomysium surrounds individual muscle ﬁbres and is continuous with the perimysium ensheathing groups of ﬁbres in parallel bundles, or fasciculi. Perimysial septa are themselves inward extensions of the epimysium that covers the muscle and is continuous with the fascia investing whole muscle groups. All these sheaths (tubes) coalesce and transmit the force generated within muscle ﬁbres through tendons and inter/extra-muscular fascial attachments.39,42 These fascial tissues are all reinforced by two helical crossed-ply

sets of collagen,36 with the ‘ideal’ resting ﬁbre orientation of 55 (axial)33 that varies with changing muscle length. Tubular organs that maintain constant volume throughout changes in shape, due to crossed-helical arrangements of muscle and fascial tissue, have been described in the tongues of mammals and lizards, the arms and tentacles of cephalopods, and the trunks of elephants.43 Helical winding and its functional signiﬁcance have also been described in the body walls of worms33; squid44; amphibians45; eels46; ﬁsh and dolphins47; suggesting that a similar helical arrangement is likely to occur throughout the human. However, although the thoraco-lumbar and abdominal muscle/ fasciae appear to be partial spirals, information on the ﬁbre orientation of other fascial compartments is incomplete. Stecco (2004) described helical fascial sheaths that transfer tensional forces within and between themselves, and control movement in a way that the nervous system is incapable of.48 Anecdotally, palpatory phenomena with a helical component are observed within the soft tissues of the extremities.49 A normal pattern exhibits right-handed helical motion in the limbs on the left side, and left-handed helical motion on the right, although current anatomical knowledge is unable to explain this. The helix has long been recognised in joint motion,8 and its widespread appearance at multiple size-scales throughout the

Fig. 3. Close-packing of spheres to form: (a) triangles and hexagons in 2-D; (b) tetrahedron (dark/blue), octahedron (light/yellow) and (c) cube in 3-D; and (d) icosahedron. (The magnetic sticks connecting each sphere represent the geodesic connection between their centres of mass). (For interpretation of the references to colour in this ﬁgure legend, the reader is referred to the web version of this article). Figure 3c reproduced with permission of Elsevier from: Scarr GM. Simple geometry in complex organisms. J Bodyw Mov Ther 2010;14:424e44.

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body suggests that it has some special signiﬁcance. At a fundamental level, the helix and tensegrity are linked through a common origin in the geometries of the platonic solids.1,4,50 3. Simple geometry 3.1. The platonic solids, geodesic geometry and close-packing The platonic solids are regular polyhedra distinguished by having faces that are all the same shape, and naturally form through the efﬁciencies of geodesic geometry (the connection of points over the shortest path) and principles of symmetry.1,4,50 In two-dimensions, objects of similar size close-pack and form stable triangular conﬁgurations (Fig. 3a). Adding another sphere to each triangle creates a tetrahedron, and the addition of more spheres allows the octahedron and cube to emerge (Fig. 3b and c), because of the same packing arrangement. These platonic shapes are generally only found as ﬁxed inorganic crystals, but there are many consequences of close-packing. The icosahedron differs from the other platonic shapes by packing spheres around a nuclear space to form the geodesic dome (Fig. 3d).50 It is also triangulated and has multiple symmetries, which allow it to stack in a column or helix and form more complex patterns and shapes.1,2 Some naturally occurring structures based on the icosahedron are carbon fullerenes; pollen grains and ‘spherical’ viruses.22e24 Both the tetrahedron and icosahedron spontaneously form through the interactions of natural physical forces, and are the basis for appreciating complex shapes in human anatomy.2,4,51 3.2. Chirality and equivalence The property of chirality is intrinsic to the helix, and the platonic solids demonstrate this as they polymerize into left and righthanded helixes (Fig. 4).51e54 At a basic level, four spheres close-pack to form a tetrahedron, the shape that occupies the smallest proportion of unit space; minimum volume within maximum surface area.50 The addition of more spheres as in the lattice packing of Fig. 3b and c alters that proportion because of the squares within the octahedron, but a tetrahelix comes closer to the optimum, making it a more suitable model for molecular packing because of this margin of energy-efﬁciency (Fig. 4a).51,53,54 A tetrahelix also displays inherent hierarchy within its sub-helixes of different pitch (Fig. 5).

Fig. 5. Right-handed tetrahelix (dark/blue) showing: a). 3 long right-handed helixes (light/yellow); b). 2 medium left-handed helixes; c). 1 short right-handed helix. (For interpretation of the references to colour in this ﬁgure legend, the reader is referred to the web version of this article).

Mapping a tetrahelix onto a plane surface, by ‘unzipping’ one of its long helical edges, displays the packing efﬁciency of a triangular pattern (Fig. 3a). Rolling that map into a cylinder demonstrates equivalence, where each component is in the same relative position to all the others.53,54 Equivalence implies that components are arranged symmetrically, and the only shapes that can accommodate it have surfaces based on the platonic solids and cylinders.22e24,55,56 Because molecules in a peptide sequence are unlikely to match the points on a geometric lattice precisely, evolution has evaded this constraint through the device of ‘quasiequivalence’, where component proteins contort slightly but still relate to the geometric template.1,23,24,53 Tropocollagen (Fig. 2) has been described as three stretched quasi-tetrahelixes surrounding a central core.53,54 Each glycine residue, from the three procollagen peptides, contributes a hydrogen atom that forms the corner of a regular tetrahedron, and together they form the right-handed tetrahelical core of the tropocollagen molecule. The left-handed procollagens are the sub-helixes shown in Fig. 5b; and this conﬁguration also gives rise to a stack of slightly contorted icosahedra.53,54 Most (if not all) molecular helixes are geometrically related to the tetrahelix and icosahedron,12,22,53,54,56

Fig. 4. Chiral helical polymers of the a) tetrahedron and b) icosahedron.

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Fig. 6. a) Geodesic dome icosahedron; b) tensegrity icosahedron; c) ‘tension triangles’ connecting groups of struts with opposite chirality. Fig. 6a and b reproduced with permission of Elsevier from: Scarr GM. A model of the cranialvault as a tensegrity structure, and its signiﬁcance to normal and abnormal cranial development. Int J Osteo Med 2008;11:80e9.

including the alpha-helix of DNA, which has been described as a triplet of tetrahelixes with one strand missing.53 Molecules automatically assume a state of minimal-energy as they balance the attraction and repulsion of their constituent atoms. As the helix is a more efﬁcient close-packing conﬁguration it is understandable that it should be such a common structural shape. At a larger scale, the bacterial cell wall contains actin homologues arranged as a structural helix determining cell shape and elongation.57,58 Plants display similar conﬁgurations in their cell walls59 and geometric patterns at a higher level.

to move with the minimum of energy expenditure without losing stiffness or stability.6,7,51 Because tension and compressional forces are separated, the material properties of components can be optimized, and in biological systems this typically occurs through hierarchies. Tensegrity hierarchies achieve a signiﬁcant reduction in mass,6,7 and provide a functional connection at every level, from the simplest to the most complex, with the entire system acting as a unit.5,51,76

3.3. Fibonacci and the golden mean

The icosahedron is a fundamental geometric shape because it encloses a greater volume, within minimum surface area, than any regular structure apart from a sphere (Fig. 6a). It is developed into a tensegrity structure by using six compression struts to traverse the inside (Fig. 6b). These connect and hold opposite vertices apart with the outer edges of the icosahedron now replaced by cables under tension. The resultant pull of the cables is balanced by the struts, which remain distinct from each other and do not touch. They provide structural integrity so that the compression elements ﬂoat within the tension network.50,79 Considering the six struts in different groups of three, joined on the surface by ‘tension triangles’ (Fig. 6c), shows that each strut within the group is oriented at 90 to the others, and together they create a chiral twist. On the other side of the structure is a similar group with a twist in the opposite direction, which means that a tensegrity icosahedron already contains helical precursors of both chiralities. When three struts are modelled on their own (Fig. 7), they form a shape called a tensegrity prism.6,7 Increasing the number of struts causes their centres to position more towards the outside of the structure, enlarging the central space and eventually forming a cylindrical ‘wall’ due to the changing orientation (Fig. 7bed). The struts are equivalent, and all form part of an inﬁnite series of left or right-handed helixes; the model in Fig. 8 demonstrates their tubular nature. Each strut could be made from a smaller helix, or the whole structure become part of a strut within a larger helix ie it has hierarchical capability. Helical molecules are at the ‘lower’ end of structural hierarchies that ﬁll the entire body, but have physical properties that continue into those higher levels. Helical tensegrity is a structural mechanism with many properties useful to organic life.

The parastichies of ﬂower heads are parallel spirals that run in opposite directions, a result of the most efﬁcient close-packing arrangement of objects in their growing tips.60 The number of elements within each opposing spiral is nearly always two consecutive numbers of the Fibonacci sequence, where each new term is the sum of the two preceding ones (1,1,2,3,5,8,13,21,34.). The ratio of any two consecutive numbers approximates to the Golden Mean (1.61804), and becomes closer as the sequence gets higher. The helical pattern on the side of a pineapple, arrangement of branches on a plant stem61 and position of coronary artery lesions62 relate to the same sequence. The Golden Mean often appears in the proportions of biological structures and platonic solids,63 including the icosahedron, which is the model that takes us into the tensegrity of macro-anatomy.50 4. Tensegrity Descriptions of tensegrity in biology have appeared in the literature since the early 1980’s,64,65 and include the cellular cytoskeleton;5 developing neurites66 and cerebral cortex67; spider silk6,68 and wasp arcus69; mammalian70e72 and avian lung73; fascial matrix;74e76 shoulder75; spine;51 pelvis77 and cranium.78 Fuller (1975) described a tensegrity structure as a set of struts under compression, and an arrangement of cables under isometric tension, that always balances in the most energetically efﬁcient conﬁguration.50 It is geodesic by its very nature, because tension always acts in straight lines, and automatically reduces itself to a minimum. Tensegrity structures make possible an inﬁnite variety of stable shapes through changes in the lengths of their compression members, and changes in those shapes that require very little control energy. As each component inﬂuences all the others, stresses distribute throughout the system, creating a structure that can react to external forces from any direction without collapsing.6,7,51 An organism utilizing such a system would be able

4.1. The tensegrity helix

5. The helical tensegrity body Helical molecules behave as tensegrity structures in their own right, as they stabilize through a balance between the forces of

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Fig. 7. Tensegrity prisms (right-handed) with increasing numbers of equivalent struts.

Fig. 8. A helical tensegrity polymer derived from Fig. 7.

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attraction (tension) and repulsion (compression).79,80 They readily combine into more complex structures that retain some of the same properties.2,12 The cellular cytoskeleton is described as a multi-functional tensegrity structure that inﬂuences cell shape, and activates multiple intra-cellular signalling pathways.5 Helical microﬁlaments of actin and microtubules of tubulin are the tension and compression elements, respectively (Fig. 1a and b); while spectrin ﬁbres and actin bundles may have similar roles within the cell cortex (Fig. 1c).81,82 Tensioned intermediate ﬁlaments link everything together, from the nucleus to the cell membrane.83 Tension is generated through the action of actomyosin motors and polymerization of microtubules, and any change in force at one part of the structure causes the cytoskeleton to alter overall cell shape.5 Many enzymes and substrates are situated on the cytoskeletal lattice, and changes in its conﬁguration alter their activity, leading to a switch between different functional states such as growth, differentiation or apoptosis.5 The cytoskeleton connects to the matrix and other cells through transmembrane proteins, such as integrins and cadherins, respectively. These create a mechanical coupling that transfers tension, generated within the cytoskeleton, to the matrix and adjacent cells. A pre-stressed state of isometric tension thus exists between them, so that a change in matrix tension causes a realignment of structures within the cytoplasm, and a change in cell function. This reciprocal transfer of mechanical forces is likely to orchestrate cellular growth and expansion, allowing the emergence of complex multi-cellular tissue patterns, based on the same principles.5,84,85 5.1. Helical tubes The formation of capillaries results from tension-dependent interactions between endothelial cells and an extra-cellular scaffold of their own construction, and is described through tensegrity.86 The growing matrix causes changes in the conﬁguration of cytoskeletal components,5 and initiates chemical signalling cascades that inﬂuence further development of the capillary network.87 The capacity for ﬂuid ﬂow through a tube depends, in part, on the porosity of the tube wall. The helical tensegrity ‘wall’ in Fig. 8 has many gaps, but if the struts were expanded into plates that just touched each other, they could be made to ‘seal’ the internal space. This compares with the selective barrier of endothelial cells that allows vascular contents to pass out between capillary walls. The internal cellular cytoskeleton determines cell shape and orientation, through tensegrity;5 is affected by signalling mechanisms and variations in ﬂuid ﬂow; and alters the tension between cells through adherens junctions,88 ultimately affecting tube permeability.89,90 In tensegrity terms, there is no speciﬁc need for a compressional element within the tube wall if this is provided by outward pushing radial pressure, although arterial walls are pre-stressed even when load free. It is likely that wall components under tension are linked to other structures under compression at different hierarchical levels; Fuller (1975) emphasized that tension and compression must always coexist.50 Collagen type I ﬁbrils are the predominant tensors, and are virtually inextensible under tension (<5%)30; but the mechanical properties of more than twenty other types are poorly understood. Proteoglycans and glycosaminoglycans tend to increase in tissues under compression. Combining these and other components into tissue speciﬁc matrices contributes to huge histological variation. Conﬁrmation that they are tensegrity conﬁgurations, however, will depend on analysis of their physical interactions. A fundamental principle of tensegrity is that the forces of tension and compression are separated into different components,

and always act in straight lines; which means that there are no shear stresses or bending moments. The model in Fig. 8 shows curved struts that seem contrary to this, but they can be understood in terms of hierarchies. Curved struts only remain stable if their crystal/molecular structures are strong enough to resist the potentially damaging shear stresses that lead to buckling; or they are part of a tensegrity hierarchy that eliminates those stresses by its very nature. Curves may appear at one level within a hierarchy, but when looked at in more detail, have structural components that handle tension and compression in straight lines.21 Undoubtedly, the ﬁbre angle within any particular tissue depends on the functional context. The model in Fig. 8 shows struts arranged in a self-similar array and tension cables with differing orientations. Previous descriptions of “random” collagen orientations may have misinterpreted what were actually functionally ordered tensegrity alignments,91 and the sensitivity of newer imaging techniques and their analysis may resolve this.92,93 5.2. Helixes within helixes Axial compression of a tensegrity helix initiates rotation in a direction dependent on the helical angle and strut orientation (chirality), with a corresponding decrease in the central diameter. Axial extension causes it to expand demonstrating a negative Poisson ratio; most man-made materials reduce their width when stretched,9,16 but this unusual response is common in biological structures.1,51 Surrounding a helix, with another one of opposite chirality, increases resistance to axial compression, as each helical layer counteracts the rotation of the other; crossed helixes have been shown to alter tubular properties.33,34 The intervertebral disc contains collagen arranged in concentric lamellae, with opposing orientations in alternate helical layers that provide tensile reinforcement.29 Whether this is a tensegrity conﬁguration is yet to be assessed; but the widespread view that discs provide resistance to spinal compression as a prime function is probably too simplistic, and the whole spine has been looked at from a tensegrity perspective.51 Although disc failure usually occurs in tension,94 this is usually due to abnormal loading. The negative Poisson ratio may also have relevance to the helical dynamics of the heart and has been described with the tensegrity ‘jitterbug’ mechanism. When any two tension triangles of a tensegrity ‘icosahedron’ are pushed together or pulled apart (Fig. 6c), the entire structure contracts and expands, respectively.1,50,51,95 5.3. Putting this all together The helix is an energy-efﬁcient solution to molecular closepacking and spontaneous assembly, with the inherent ability to form hierarchies. Collagen, the most widespread of structural proteins, consists of several helical levels and is a major component of the extra-cellular matrix that surrounds virtually every cell in the body (Fig. 2). The extra-cellular matrix is a structural framework continuous with the fascia and has been described through tensegrity.51,74,76 Helical ‘tubes within tubes’ mean that fascial compartments of the trunk and limbs can be considered in the same way. Objections that fascia is too ﬂexible to contain compression struts can be overcome by considering the diameter of muscle, and its increase during contraction, as such struts. This would undoubtedly alter the tension pattern of surrounding fascia, which has itself been shown to inﬂuence the force appearing at tendons.39,40 In a tensegrity sense, fascia is the bodies main component of tension suspended between bones under compression, with smaller compartments taking origin from larger ones. Muscle ﬁbres can then be considered as mere motors.

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Helical and tensegrity structural systems complement each other, and are based on the fundamental properties of the tetrahedron and icosahedron. A chain of tensegrity icosahedra simply contains the crossed-helical ﬁbres of a tube. Putting all this together from a helical tensegrity perspective necessitates a reappraisal of structural biology and manual therapeutic techniques in terms of fundamental geometry. 6. Conclusion The observation of a geometric pattern doesn’t necessarily imply anything meaningful, as Johannes Kepler (1571e1630) found out with his early description of a platonic solar system. However, the simple tetrahedron, octahedron, cube and hexagon are recognised in the structures of inorganic crystals, a result of atomic closepacking and principles of symmetry. (Fig. 3b and c).1,4,50 Carbon fullerenes and viruses appear as icosahedra and are related to the geodesic geometry of a sphere(Fig. 3d).1,2,23 The hexagonal packing of muscle ﬁbrils and cells occurs because of the same physical laws.4,5,65 There are many possible consequences of close-packing, and the tetrahelix as one of them provides a more energy-efﬁcient solution in molecular biology (Fig. 5).53,54 Molecules assemble spontaneously and automatically balance the attraction and repulsion of their constituent atoms in a state of minimal-energy.24,79 The helix forms because of the same ‘platonic’ rules, those of organic chemistry and the dynamic nature of biological systems. The tetrahelix and its geometry then describe the helical hierarchies of protein structures and DNA (Figs. 1,2 and 5).53,54 Concurrent with the molecular helix is the principle of tensegrity. Tension and compression (attraction and repulsion); geodesic geometry and minimal-energy; and the inherent ability to form hierarchies are characteristics of both these structures. At the cellular level, the tensegrity principle describes the mechanical behaviour of the cytoskeleton, being a semi-autonomous system amenable to such analysis because of its size.5 As a structural mechanism, tensegrity depends on the integration of every part, and it has been proposed that this includes the whole body, from molecules, cells, extra-cellular and fascial matrix to the entire musculo-skeletal system.1,4,5,74e76 Although it has been described at higher levels of anatomy, detailed multi-scale syntheses of its components are few. The helix, however, is a readily observable pattern at many different levels and may be inseparable from tensegrity, but there is a caveat. If the structure of the human body is considered as a vast hierarchy of interacting sub-tensegrities, structurally and functionally, the examination of any part in isolation can be misleading, as it is inevitably incomplete.39e41 The possibilities for enquiry become virtually endless and make it unlikely that ‘bio-tensegrity’51 could ever be proved. However, if it describes biological systems more thoroughly, it is only a matter of time before this becomes the standard approach to biomechanics. Human anatomy and physiology have been described in terms of tensegrity, and the volume of supporting evidence is steadily increasing. The helix is a well-known structural motif in biology. The fundamental links between tensegrity, the helix and platonic solids support a comprehensive view of human anatomy that is best appreciated as a complex interaction of natural physical forces. References 1. Levin SM. The icosahedron as the three-dimensional ﬁnite element in biomechanical support. Proceedings of the Society of General System Research Symposium on Mental Images, Values and Reality 1986;Philadelphia. pp. G14eG26.

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International Journal of Osteopathic Medicine 14 (2011) 33e37

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RESEARCH AND TREATMENT BULLETIN Section Co-ordinator: Paul D. Blanchard The British School of Osteopathy, Research Centre, 275 Borough High Street, SE1 1JE London, UK Shoulder pain: The relationship with lifestyle and metabolic factors Stuart Walker, The British School of Osteopathy, London, UK Shoulder pain is a common presenting symptom in osteopathic practice. It is estimated that, in a general population, the prevalence of shoulder pain during the preceding 30 days is between 18% and 31%.1 There are many causes of shoulder pain including traumatic and degenerative conditions that may be caused or aggravated by wideranging environmental and individual factors. Interestingly a number of studies have noted a link between shoulder disorders and metabolic factors such as obesity and diabetes.2 The authors of this study have set out to explore this relationship further by hypothesising that lifestyle factors, metabolic factors and carotid artery intima-media thickness (carotid IMT) are associated with shoulder pain and rotator cuff tendonitis. The measurement of carotid IMT has been shown to be a risk indicator for atherosclerotic vascular diseases.3 The study investigated the hypothesis by carrying out a cross-sectional health survey in the general adult Finnish population using a large sample size of 8,028 subjects. This study was evidently part of a group of studies that were investigating musculoskeletal issues and relating them to lifestyle factors. A detailed survey protocol was followed for each participant including symptom interview, musculoskeletal physical examination, lifestyle/physical factor/sociodemographic interviews, general physical examination, blood tests for glucose and C-reactive protein and triglycerides and, finally, an ultrasound measurement of carotid IMT. This wide-ranging data on the individuals was then used to perform regression type statistical analysis in order to determine which factors were most linked to shoulder pain and tendonitis. The results were able to show that metabolic factors, particularly abdominal obesity, and carotid IMT were associated with shoulder pain. In addition Type I diabetes and abdominal obesity were

associated with chronic rotator cuff tendonitis in men. It is thought that atherosclerosis and disturbed glucose metabolism may affect the nutrition of the shoulder structures leaving them prone to injury and slow to repair. Heavy smoking or long smoking duration was also found to be associated with unilateral shoulder pain in men and bilateral shoulder pain in women. Smoking, whilst contributing to cardiovascular complications also increases the expression of proinflammatory cytokines thereby promoting inflammatory conditions. As osteopaths in general practice we all encounter shoulder pain patients on a weekly, if not daily, basis. Being aware that obesity, smoking and disturbed glucose metabolism can both predispose and maintain patients to shoulder pain and rotator cuff tendonitis enables osteopaths to consider their patients in a wider health context and allow them to dispense useful advice as to how lifestyle behaviours may be contributing to their problem. As clinicians, however, we will also be aware just how resistant to change these predisposing factors can be. References 1. Luime JJ, Koes BW, Hendriksen IJ, Burdorf A, Verhagen AP, Miedema HS, et al. Prevalence and incidence of shoulder pain in the general population; a systematic review. Scand J Rheumatol 2004;33:73e81. 2. Viikari-Juntura E, Shiri R, Solovieva S, Karppinen J, Leino-Arjas P, Varonen H, et al. Risk factors of atherosclerosis and shoulder pain is there an association? A systematic review. Eur J Pain 2008;12:412e26. 3. Rechardt M, Shiri R, Karppinen J, Jula A, Heliovaara M, ViikariJuntura E. Lifestyle and metabolic factors in relation to shoulder pain and rotator cuff tendonitis: a population-based study. BMC Musculoskelet Disord 2010; 11:165.

Doctors, physiotherapists and chiropractors communicate less well with patients with chronic low back pain Mark Waters, The British School of Osteopathy, London, UK Many osteopaths are very familiar with Waddell’s1 work on low back pain and once again, almost a decade on, we see it cited here as justification for a new study into how health care providers interact with patients. Here the team of researchers in Scandinavia have focused on the quality of communication between practitioners and patients with low back pain with emphasis on information given in a back pain clinic.2 The research was conducted in an interdisciplinary back pain clinic employing doctors, physiotherapists and chiropractors with patients who had been referred to the clinic. Twenty one practitioners participated in the research and 79 patients (3 doctors carrying out 7 consultations, 9 chiropractors with 34 consultations and 9 physiotherapists with 38 consultations). Fifty three patients were female and the mean age was 45. Consultations were video recorded and evaluated using the Four Habits Coding Scheme (4HCS). This scheme was from a clinical communication training program originating in the USA. Under the scheme all elements of communication are amalgamated into four habits; how the patient is met and the case International Journal of Osteopathic Medicine

history taken, the elicitation of the patient’s perspective, demonstration of empathy and finally patient understanding of the information conveyed is checked and adherence to therapy encouraged. Following the consultation the patients completed questionnaires about their experiences of the interaction and data about age, gender, education level and duration of pain. Age was the only variable that was considered to be normally distributed. The results showed “strongly significant negative correlations” between the 4HCS score and patient age and pain duration with the difference pertaining mostly to interest in the patients understanding and psychosocial status, encouraging expression of emotions, tests for comprehension and involvement in decisions. The researchers concluded that the communication quality of the doctors, the physiotherapists and the chiropractors was lower when dealing with patients who have long standing back pain compared to those with pain of a shorter duration. The research team was not able to provide a strong theoretical basis to explain their findings but speculated that it may be due to the way duration of pain influences the mind set of all people involved. They suggest that patient’s pessimism may lead to them just wanting treatment to help manage the pain rather than a full investigation of the circumstances surrounding their condition. Health care providers, in turn are reticent in forcing this on patients and feel that the effort involved in motivating a discouraged person is too much. Patients with chronic pain may have suffered psychological trauma and providers may be subconsciously reluctant to explore this. Poorer communication was also found with older patients and once again the researchers speculated that perhaps providers may think older patients have a reduced chance of improvement. Presumably the healthcare providers scrutinised no doubt believed they were treating all patients equally. More work will be required to explain the discrepancy in quality of communication that exists but the research certainly identifies the problem. Clearly the study was specific to the clinic in which it was conducted but as the UK NICE guidelines3 regarding back pain potentially bring more patients into osteopathic clinics this study does highlight the need for practitioners in this discipline to question the way they communicate with certain patients. References 1. Waddell G, The back pain revolution. London: Churchill Livingstone; 2004. 2. Gulbrandsen P, Madsen HB, Benth JS, Laerum E. Health care providers communicate less well with patients with chronic low back pain - a study of encounters at a back pain clinic in Denmark. Pain 2010;150:458e61. 3. Savigny P, Watson P, Underwood M. Early management of persistent non-specific low back pain: summary of NICE guidance. BMJ 2009;338:b1805. Full guidelines available from: http://guidance.nice.org.uk/CG88/Guidance/pdf/English.

Trial comparing manipulation with mobilisation for recent onset neck pain shows no difference of effect for either treatment Brett Vaughan, School of Biomedical & Health Sciences, Victoria University, Australia This paper by Leaver et al.1 generated quite a lot of media interest in Australia with some media reports suggesting that cervical spine manipulation (i.e. ‘thrust manipulation’) may not be appropriate given the increased risk of stroke, when compared to mobilisation of the cervical spine.2 Neck pain is a common presentation in osteopathic practice and this study sought to compare the effectiveness of mobilisation and manipulation for the management of cervical spine pain. Both techniques are commonly utilised by osteopaths and have been shown to be effective for cervical spine pain, however, there is reported to be a higher risk of stroke and similar events with manipulation. Participants for this study were recruited from chiropractic, physiotherapy and osteopathic practices in Sydney, Australia. All participants had neck pain of less than three months duration, with no neck pain in the month preceding the onset of the neck pain. Participants (n ¼ 182) were randomly allocated into a manipulation (n ¼ 91) or mobilisation group (n ¼ 91) and received four treatments over a two-week period. The particular mobilisation or manipulation International Journal of Osteopathic Medicine

technique utilised was based on the treating practitioner’s personal preference. The primary outcome measure was ‘days to recovery’ which was defined as the first of seven days where the participant rated the pain 1 out of 10. Other outcome measures used included the Neck Disability Index (NDI), Patient Specific Functional Scale (PSFS), global perceived effect and healthrelated quality of life (12-Item Short-Form Health Survey Physical and Mental Component Summaries). All outcomes were assessed at baseline with pain and global perceived effect measured at the end of treatment (two weeks) and at 12 weeks post-randomisation. NDI, PSFS and healthrelated quality of life were measured at four weeks and 12 weeks post-randomisation. Overall, five participants withdrew from the study, including one participant who withdrew following an adverse event (development of severe arm pain and weakness). At baseline the mean pain score was six, with the vast majority of participants also experiencing upper extremity pain, headaches or upper thoracic pain. The mean NDI score at baseline was 15.5. The median number of days to recovery was 47 for the manipulation group and 43 days for the mobilisation group. With regard to median time to return to normal activity, participants in the manipulation group took 22 days compared to 24 days for the mobilisation

group. Pain intensity decreased from a mean of 6/11 pre-treatment to 2.5/11 after two weeks of treatment. There were no statistically significant differences between the two groups on all other outcome measures. The study concluded that manipulation was not superior to mobilisation for cervical spine pain in terms of pain, function, disability, global perceived effect and health-related quality of life. Interestingly, over half of the participants did not fully recover from their cervical spine pain. Adverse effects were noted in both groups with no statistically significant difference between groups, with neck pain and headaches being the most common adverse effects. No serious adverse effects were noted during the study. Based on the findings of this study, the authors have suggested “.there is reason for practitioners and their patients to re-evaluate the use of manipulation for recent onset neck pain”. References 1. Leaver AM, Maher CG, Herbert RD, Latimer J, McAuley JH, Jull G, et al. A randomized controlled trial comparing manipulation with mobilization for recent onset neck pain Arch Phys Med Rehabil. 2010;91:1313e8. 2. Leaver AM. Controversial study suggests neck manipulation not worth the risk. http://www.usyd.edu.au/news/84.html? newsstoryid¼5582 (accessed 2.11.10).

Staying at work with back pain: Patients’ experiences of work related help received from GP’s and other clinicians Elisabeth Bird, Private practice, Falmouth, UK Back pain is one of the most common and difficult occupational health problems.1 Given that there are few studies on patient perception of occupational health care; the authors focused their study2 on exploring individual experiences of patients suffering from back pain, conveying their work concerns to their GP’s and clinicians. This was a qualitative study of 25 employed patients. The interviews were digitally recorded and conducted individually. Questions were based around pre-chosen topical areas which included the effect of back pain on their work ability, assistance received from the patients’ clinician or GP about their work ability and the subsequent expectations of rehabilitation on their work performance. The scripts were then analysed by discussion and review by the research team. The results identified five themes of patient perception: ‘Doubts as to what GP’s have to offer those working with back pain’ and ‘GP’s are more inclined to write sickness certificates than help patients’ manage work problems’. Participants expected that the usual outcome for back pain treatment from their GP would be a medication prescription and/or handing out sick notes. The general consensus was not dissatisfaction with their GP but a general lack of confidence in their GP or clinician’s ability to confidently help with their work difficulties. ‘Little evidence of effective advice about work from the GP’ and ‘GP and clinician management may increase concerns about working with back pain’. The participants’ lack of confidence in their GP’s or clinicians capacity to help was supported by the lack of evidence of any effective advice given out. Several interviews revealed that GP’s, chiropractors and physiotherapists often prescribed a complete abstinence from work or from work tasks, instead of suggesting modifications to help with their recovery. ‘Lack of dialogue between GP’s, clinicians and employers’. Only one of the participants’ GPs contacted the employer regarding the patients back pain management with no positive outcome. The perception of patient expectation and outcome in occupational health care is important to consider because patient expectations are probably strong determinants of outcome. The research demonstrated

a lack of practitioner confidence in effective occupational health care; and this was mirrored by patient opinion. However with this in mind, it should also be noted that patients often attribute work demands as the sole cause of their back pain, and this is probably not the case,1,3 nonoccupational interventions and psychosocial issues also require careful consideration. Emphasis on occupational management for patients from a primary care position is often ineffective, despite its poor conveyance exposed in this investigation; supported by evidence that abstinence from work with patients suffering from lower back pain does little to improve their symptoms and that work is in fact a vital part of rehabilitation.4 This study demonstrated that (misguided) self management of work difficulties seems to be the most usual course for the study participants. This is disappointing when there are helpful options available in primary health care and well documented studies to support more effective resolution in the prevention and treatment of back care,5 which are still not being made readily available to patients. More defined treatment options for back pain and better communication and support between GP’s and clinicians about the reality of occupational intervention are vital. This type of communiqué can surely assist patients’ work concerns more efficiently, instead of the present ‘headless chicken’ type management. This might encourage reducing the need for work abstinence and most importantly help dissolve the ambiguity of patients; a tactic which should harmonize with, primarily, employers providing better work-related health care.

References 1. Waddell G, Burton A. Occupational health guidelines for the management of low back pain at work: evidence review. Occup Med 2001;51:124. 2. Coole C, Watson P, Drummond A. Staying at work with back pain: patients’ experiences of work-related help received from GPs and other clinicians. A qualitative study. BMC Musculoskelet Disor 2010; 11:190. 3. Waddell G, Burton A. Concepts of rehabilitation for the management of common health problems. The Stationery Office; 2004. 4. Waddell G, Burton AK. Clinical management of common health problems. In: Concepts of rehabilitation for the management of common health problems. The Stationery Office; 2004. 5. Savigny P, Watson P, Underwood M. Early management of persistent non-specific low back pain: summary of NICE guidance. BMJ 2009;338:b1805. Full guidelines available at: http://guidance.nice. org.uk/CG88/Guidance/pdf/English (Retrieved 15 November 2010).

Men with left-sided spinal pain may be more likely to suffer affective disturbances and may benefit from additional psychiatric or psychological care Rafael Zegarra-Parodi, CEESO Paris and Lyon, France There is a brain asymmetry in the control of the autonomic nervous system. The sympathetic nervous system is controlled in the right hemisphere for contralateral peripheral nervous system activity and, conversely, the parasympathetic nervous system is left lateralized centrally and right lateralized peripherally. The right cerebral hemisphere is also more involved than the left hemisphere in the processing of pain and negative emotions. This lateralization might be relevant for practitioners involved in chronic musculoskeletal pain management as lateralized pain activating the contra lateral hemispheres could theoretically have different effects on pain perception and psychopathology. Wasan et al.1 designed a prospective cohort study aimed at determining pain levels, function and psychological symptoms in relation to predominant sidedness of pain and gender in patients with chronic spinal pain. Subjects (n ¼ 519) had an evaluation by their treating physician which concluded that there was an anatomical or structural basis explaining at least a portion of their pain complaints (facet arthropathy, degenerative disc disease or herniated disc) following new MRI or CT imaging. Subjects included in this study were those who were proposed

International Journal of Osteopathic Medicine

these treatments: facet joint injection, radiofrequency lesioning of the facet joints, or transforaminal epidural steroid injections. Subjects had to complete the Hospital Anxiety and Depression Scale and the Brief Pain Inventory just prior to the procedure. Despite the ratings of pain being similar between groups, the left-sided pain patients had significantly greater depression syndromes and reported significantly greater interference of pain with their mood. Men accounted for the majority of differences in psychological symptoms between the left- and right-sided groups (P < 0.01) while none of these comparisons among women were significant. The authors concluded that men with left-sided spinal pain may be more likely to suffer affective disturbances and may benefit from additional psychiatric or psychological care. Osteopathic practitioners might be interested with these findings firstly by the repercussions of musculoskeletal system pathologies that are not just locally limited to pain and movement restriction. The current association of spinal pain with psychological symptoms as described in the Wasan et al study could indeed illustrate the interrelation between structure and function, one of the four key osteopathic principles.2 Such descriptive study could provide more data to justify the emphasis on the musculoskeletal system’s influence on health outcomes, an aspect of osteopathic principles which is often controversial in the literature. Biomechanical changes following spinal manipulation are hypothesized to affect neural input, subsequently altering central processing and affecting reflex somatomotor or somatovisceral output at different spinal cord levels.3 Manual practitioners might ask themselves if brain control of the autonomic nervous system would be influenced by manipulation too. However subjects included in this study were suffering from degenerative or pathological conditions that are contra-indicated for many manual techniques or even treatments. No data is available on the theoretical impact of functional disturbances such as somatic dysfunctions on pain perception and psychopathology. Osteopathic researchers could evaluate this hypothesis with preliminary data coming from osteopathic practitioners using data collection tools such as the “Outpatient Osteopathic SOAP Note Form”.4e6 The relevance of pain lateralization in manual therapies could also be discussed in a descriptive study among men with left-sided chronic spinal pain. References 1. Wasan A, Anderson N, Giddon D. Differences in pain, psychological symptoms, and gender distribution among patients with left vs right sided chronic spinal pain. Pain Med 2010;11:1373e80. 2. Rogers F, D’Alonzo Jr G, Glover J, Korr I, Osborn G, Patterson M, et al. Proposed tenets of osteopathic medicine and principles for patient care. J Am Osteopath Assoc 2002;102:63. 3. Pickar J. Neurophysiological effects of spinal manipulation. Spine J 2002;2:357e71. 4. Sleszynski SL, Glonek T. Outpatient osteopathic SOAP note form: preliminary results in osteopathic outcomes-based research. J Am Osteopath Assoc 2005;105:181e205. 5. Licciardone JC, Nelson KE, Glonek T, Sleszynski SL, Cruser dA. Osteopathic manipulative treatment of somatic dysfunction among patients in the family practice clinic setting: A retrospective analysis. J Am Osteopath Assoc 2005;105:537e44. 6. Davis MF, Worden K, Clawson D, Meaney FJ, Duncan B. Confirmatory factor analysis in osteopathic medicine: fascial and spinal motion restrictions as correlates of muscle spasticity in children with cerebral palsy. J Am Osteopath Assoc 2007;107:226e32.

Physiological effects and efficiency of manual therapy in the treatment of chronic tension-type headache Jerôme Wagner1, Jerry Draper-Rodi1,2 1

Private practice, Paris, France

2

The British School of Osteopathy, London, UK

Tension-type headache is common in the general population with a reported one-year prevalence rate of 38.3% for the episodic form and 2.2% for the chronic form. Tension-type headache may cause substantial levels of disability. Toro-Velasco et al1 investigated the effects of manual therapy on heart rate variability parameters (Holter electrocardiogram recordings), psychological disorders (Profile of Mood States questionnaire), pressure pain sensitivity (pressure pain thresholds), and pain intensity in patients with Chronic Tension-Type Headache (CTTH). Eleven patients (eight female), between 20 and 68 years old with CTTH participated in this crossover study. Patients received either an experimental treatment (pressure release,

International Journal of Osteopathic Medicine

muscle energy or soft tissue techniques) or a placebo intervention. Data was obtained before intervention, immediately after intervention, and then 24 h after intervention. Self-reported head pain was also noted before intervention and 24 h post-intervention. The application of a session of manual therapy produced an immediate increase of the heart rate variability index, and an immediate decrease in tension, anger status, and perceived pain, though these effects were transient (lasting under 24 h). A second trial, by Castien et al2 set out to evaluate the effectiveness of manual therapy on frequency of headache, use of pain medication, impact of headache, and cervical physical function in patients with CTTH, compared to usual GP care. 80 participants, between 18 and 65 years old fulfilling the criteria for CTTH, were randomly given either manual therapy (mobilisation of the cervical and thoracic spine, exercises and postural correction) or usual care. Assessments were performed at the baseline, directly after the 8-week treatment period and

after 26 weeks. The results of this trial showed that manual therapy is effective in the treatment of CTTH, reducing headache frequency, intensity and impact, both short-term (at 8 weeks) and long-term (at 26 weeks). These two studies are complementary. The first study shows the physiological effects of manual treatment on CTTH patients and that this treatment is effective in the short-term only. The second study demonstrates that manual treatment on CTTH patients is effective in the short-term and the long-term. The difference in the duration of the effects in these studies may be explained by the fact that different treatment is given in each. Treatment was limited to certain manual techniques, and these were not the same in both studies pressure release, muscle energy techniques and soft tissue techniques were used in the first study, and thrust manipulation, thoracic and cervical spine mobilisation in the second. Another difference is that in the second study, the manual practitioners gave advice on exercises and postural corrections. It has already been demonstrated that exercises

given to patients improve efficacy of treatment.3,4 In certain cases, this may be enough to decrease symptoms.5 References 1. Toro-Velasco C, Arroyo-Morales M, Fernández-de-las-Peñas C, Cleland J, Barrero-Hernández F. Short-term effects of manual therapy on heart rate variability, mood state, and pressure pain sensitivity

International Journal of Osteopathic Medicine

in patients with chronic tension-type headache: a pilot study. J Manipulative Physiol Ther 2009;32:527e35. 2. Castien R, van der Windt D, Grooten A, Dekker J. Effectiveness of manual therapy for chronic tension-type headache: a pragmatic, randomised, clinical trial. Cephalalgia, in press. 3. Gilardeau C, Daubinet G. Pathologie non inflammatoire et non infectieuse de la sacro-iliaqueJoint pathologies infection or

inflammatory excluded of the sacro-iliac. J de traumatologie du sport 2010;27:31e44. 4. DonTigny R. Mechanics and treatment of the sacroiliac joint. J Man Manipulative Ther 1993;1:3e12. 5. Sokunbi O, Cross V, Watt P. Moore A. Experiences of individuals with chronic low back pain during and after their participation in a spinal stabilisation exercise programme - a pilot qualitative study. Man Ther 2010;15:179e184.

International Journal of Osteopathic Medicine 14 (2011) 38

Contents lists available at ScienceDirect

International Journal of Osteopathic Medicine journal homepage: www.elsevier.com/ijos

Book and media review The Resilient Clinician, R.J. Wicks. Oxford University Press, New York. 255 pp., Hardback, US$29.95, ISBN 13: 9780195316971; ISBN 10: 0195316975 Although The Resilient Clinician is written by a psychologist for other mental health clinicians, it has an equal resonance for other healthcare clinicians including osteopaths. This is a fairly short book, and can be read in one sitting. It does, however, contain many powerful messages and is notable for its very positive and constructive tone. The text is divided into four chapters dealing explicitly with identifying the dangers associated with stress, and being aware of the ongoing challenges of dealing with our own and our patients’ stress. Further chapters cover the development of resilience by recommending the creation of our own self-care protocols which could be employed on a regular basis. Strategies for replenishing ourselves through solitude, silence, and mindfulness, for example, are discussed; and the practice of mindfulness is also advocated as a method to facilitate self-reﬂection. Although such strategies are increasing in their popularity, they are far from universally known or advocated at present.

doi:10.1016/j.ijosm.2010.12.005

In addition to the initial four chapters, the text includes appendices clearly summarising the signs and symptoms of burnout, strategies for basic stress management, and dealing with daily burnout. Included questionnaires allow also individual clinicians to measure their own stress. The ﬁnal chapter includes a variety of questions on which to reﬂect to consider whether insidious stress is becoming a destructive force in our personal and/or professional life. This is an enjoyable book to read. It is well researched and has an overarching positive tone directing clinicians to some very positive steps to increase their strengths and resources rather than to eliminate their weaknesses. Increasingly individuals are surrounded by a culture of “busyness” in their personal and professional lives, while practising also in very challenging times. The Resilient Clinician is an inspiring book to provide guidance and support during such times, hopefully encouraging us not just to survive but to thrive. Carol Fawkes Coventry, United Kingdom E-mail address: [email protected].

International Journal of Osteopathic Medicine 14 (2011) 39

Contents lists available at ScienceDirect

International Journal of Osteopathic Medicine journal homepage: www.elsevier.com/ijos

Erratum

Erratum to “Thoracic outlet syndrome part 1: Clinical manifestations, differentiation and treatment pathways” [International Journal of Osteopathic Medicine 13 (2010) 133e142] L.A. Watson a, Tania Pizzari b, *, Simon Balster a a b

LifeCare Prahran Sports Medicine Centre, 316 Malvern Road, Prahran, VIC 3181, Australia La Trobe University, Musculoskeletal Research Center, Bundoora, Victoria 3086, Australia

The details of the third author were not included in the author group. The correct author group is mentioned above. The publisher sincerely apologises for this error.

DOI of original article: 10.1016/j.ijosm.2010.11.001. * Tel.: þ61 3 94795872. 1746-0689/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.ijosm.2010.12.001