Manual Therapy Journal - Volume 11, Issue 3, Pages 167-240 (August 2006)

VOLUME 11 NUMBER 3 PAGES 167– 240 AUGUST 2006

Editors

International Advisory Board

Ann Moore PhD, GradDipPhys, FCSP, CertEd, FMACP Clinical Research Centre for Health Professions University of Brighton Aldro Building, 49 Darley Road Eastbourne BN20 7UR, UK

K. Bennell (Victoria, Australia) K. Burton (Hudders¢eld, UK) B. Carstensen (Frederiksberg, Denmark) E. Cruz (Setubal Portugal) L. Danneels (Mar|¤ akerke, Belgium) S. Durrell (London, UK) S. Edmondston (Perth, Australia) J. Endresen (Flaktvei, Norway) L. Exelby (Biggleswade, UK) J. Greening (London, UK) C. J. Groen (Utrecht,The Netherlands) A. Gross (Hamilton, Canada) T. Hall (West Leederville, Australia) W. Hing (Auckland, New Zealand) M. Jones (Adelaide, Australia) S. King (Glamorgan, UK) B.W. Koes (Amsterdam,The Netherlands) J. Langendoen (Kempten, Germany) D. Lawrence (Davenport, IA, USA) D. Lee (Delta, Canada) R. Lee (Hung Hom, Hong Kong) C. Liebenson (Los Angeles, CA, USA) L. Ma¡ey-Ward (Calgary, Canada) C. McCarthy (Coventry, UK) J. McConnell (Northbridge, Australia) S. Mercer (Queensland, Australia) E. Maheu (Quebec, Canada) D. Newham (London, UK) J. Ng (Hung Hom, Hong Kong) L. Ombregt (Kanegem-Tielt, Belgium) N. Osbourne (Bournemouth, UK) M. Paatelma (Jyvaskyla, Finland) N. Petty (Eastbourne, UK) A. Pool-Goudzwaard (The Netherlands) M. Pope (Aberdeen, UK) G. Rankin (London, UK) D. Reid (Auckland, New Zealand) M. Rocabado (Santiago, Chile) C. Shacklady (Manchester, UK) M. Shacklock (Adelaide, Australia) D. Shirley (Lidcombe, Australia) V. Smedmark (Stenhamra, Sweden) W. Smeets (Tongeren, Belgium) C. Snijders (Rotterdam,The Netherlands) M. Sterling (St Lucia, Australia) R. Soames (Leeds, UK) P. Spencer (Barnstaple, UK) P. Tehan (Victoria, Australia) M. Testa (Alassio, Italy) M. Uys (Tygerberg, South Africa) P. van Roy (Brussels, Belgium) B.Vicenzino (St Lucia, Australia) H.J.M.Von Piekartz (Wierden,The Netherlands) M.Wallin (Spanga, Sweden) M.Wessely(Paris, France) A.Wright (Perth, Australia) M. Zusman (Mount Lawley, Australia)

Gwendolen Jull PhD, MPhty, Grad Dip ManTher, FACP Department of Physiotherapy University of Queensland Brisbane QLD 4072, Australia Editorial Committee Karen Beeton MPhty, BSc(Hons), MCSP Masterclass Editor MACP ex o⁄cio member Department of Allied Health Professions—Physiotherapy University of Hertfordshire College Lane Hat¢eld AL10 9AB, UK Je¡rey D. Boyling MSc, BPhty, GradDipAdvManTher, MAPA, MCSP, MErgS Case reports & Professional Issues Editor Je¡rey Boyling Associates Broadway Chambers Hammersmith Broadway LondonW6 7AF, UK Tim McClune D.O. Spinal Research Unit. University of Hudders¢eld 30 Queen Street Hudders¢eld HD12SP, UK Darren A. Rivett PhD, MAppSc, MPhty, GradDip ManTher, BAppSc (Phty) Case reports & Professional Issues Editor Discipline of Physiotherapy Faculty of Health The University of Newcastle Callaghan, NSW 2308, Australia Raymond Swinkels MSc, PT, MT Book Review Editor Ulenpas 80 5655 JD Eindoven The Netherlands

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Editorial

Editorial for Special Issue of Manual Therapy Journal based on the Second International Conference on Movement Dysfunction Pain and performance, evidence and effect The Second International Conference on Movement Dysfunction was held in Edinburgh, Scotland in September 2005. It was a great pleasure to welcome delegates from all over the world to Edinburgh, the home of the Scottish Parliament, ancient architecture, history and tradition, a tourist haven which is picturesque, vibrant and cosmopolitan. The First International Conference on Movement Dysfunction was held in 2001 and this second conference built on the successes of the 2001 event in focusing on pain, performance, evidence and effect. Within the theme of movement dysfunction, this second conference had several aims which revolved around presenting a greater understanding of movement analysis and management and highlighting current research and clinical development in this field. It further aimed to provide increased support for evidence-based practice and to provide further evidence for multi-factorial and multidisciplinary therapeutic management of musculoskeletal disorders. There was also an emphasis on the clinical applications derived from current research findings. These aims were reflected in the exciting programme that was offered. The programme included 9 keynote speakers, 17 guest speakers and incorporated 7 workshops from international leaders in the field. In all, 43 scientific papers were presented, 50 poster presentations were given. Cumulative research would indicate that the successful management of movement dysfunction requires a multi-modal approach. This multi-modal approach was reflected in many of the presentations given at the conference. The breadth of this approach is illustrated in Fig. 1. It depicts the basic sciences underpinning our approaches to movement dysfunction which are linked with general management and treatment strategies through a process of complex clinical reasoning, examination and assessment procedures. It also illustrates the essential knowledge, theory, science and skills which underpin the management of movement dysfunction. 1356-689X/$ - see front matter r 2006 Published by Elsevier Ltd. doi:10.1016/j.math.2006.03.004

Anatomy Biomechanics Physiology Joint movement Neural physiology Blood supply Muscle activity

Pathogenesis Pathology Orthopaedics Rheumatology Medical disorders Neurology Radiology Dentistry

Examination Assessment Differential diagnosis Clinical reasoning

General management Evidence in practice Treatment Pain modulation Restoration of mobility Soft tissue Passive mobilisations Manipulation Control of movement Stabilisation

Functional reablement Exercise – strength, endurance, co-ordination Ergonomic advice General advice re self management Education

Behavioural Sciences Communication Interactive skills Biopsycho/social factors

Fig. 1.

There are additional factors that are important issues in the successful management of persons with movement dysfunction and these include the patient/therapist relationship, together with factors which influence patients’ recovery and clinical presentation. Management is also affected by patients’ and therapists’ attitudes, beliefs, needs, expectations, preferences and, from the therapists’ point of view, their expertise and there will also be a number of factors which influence clinical performance and abilities. Despite the rapid and substantial growth in research in the field of movement disorders, there are still challenges ahead and more knowledge to attain. It has become evident that the current gold standard of proving treatment effectiveness has potential flaws without careful design. For example, many past clinical trials have treated regional musculoskeletal disorders as relatively homogenous disorders. We now know from the latest research that, for example, back and neck pain are heterogeneous groups in both the acute and chronic states. Trials in the past that have treated such populations as homogenous have possibly been too generalised to serve a useful purpose in contemporary

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practice. Future clinical trials depend on valid subclassifications being developed for musculoskeletal disorders. There has been an explosion in the development of quantifiable measures of movement disorders in the research setting. For future translation of knowledge to the clinical setting, it is also important to ensure that measurement technology is available and affordable for use in clinical practice. This is an ongoing challenge for practitioners in health service environments and equally challenging is the capacity to embed evidence into practice. The Second International Conference on Movement Dysfunction had a very strong focus on muscle dysfunction and was very quantitatively biased. The vision for the Third International Conference on Movement Dysfunction is that there will be greater concentration in the programme on qualitative approaches, patient profiling, systematic data collection, and increasing the range of research approaches used in the underpinning research activities into movement disorders. It is hoped that more randomised control trials will be presented which are based on sound evidence from other research methodological ap-

proaches. There appears to be a need for greater consideration of the physiological effects underpinning pain relief with altered motor control and changes in muscle activation patterns. It was suggested that perhaps some investigations of the effects of functional re-ablement and factors which affect functional reablement also take place within the next few years. In addition, patient empowerment and self-efficacy need to be considered as important entities as well as the important issues surrounding the patient/therapist relationship and the impact that this may have on patient outcome. The next 4 years will present exciting challenges for clinicians and researchers alike in meeting the challenge for further enhancement of knowledge and clinical practice.

Editors Ann P. Moore Gwendolen Jull University of Brighton, Aldro Building, 49 Darley Road, Eastbourne, East Sussex, BN20 7UR, UK E-mail address: [email protected] (A.P. Moore)

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Keynote address

Classification of lumbopelvic pain disorders—Why is it essential for management Peter O’Sullivan Curtin University of Technology, School of Physiotherapy, GPO Box U1987, Perth WA 6845, Australia

The majority of lumbopelvic pain disorders have no diagnosis leaving a management vacuum. The classification of lumbopelvic pain disorders into subgroups is considered one of the greatest challenges, so as to enable the application of specific and effective interventions. It is well acknowledged that chronic lumbopelvic pain disorders are complex and multi-dimensional in nature. These disorders are commonly associated with changes in neurophysiology, altered motor control, psychological factors such as fear and anxiety, faulty coping strategies, social impact and in some cases pathoanatomical factors (Waddell, 2004). There is considerable debate as to the significance of these different factors and what is cause and effect. There is a growing focus within physiotherapy to treat motor control impairments associated with these disorders. Altered motor control in CLBP disorders is complex, highly variable and individual in nature. Trunk motor control is influenced by: spinal–pelvic posture, movement, stability demand, respiration and continence demand as well as neurophysiological factors, pathology and various psychological factors. Altered motor control may be adaptive (protective) or mal-adaptive (provocative). It can result in excessive spinal stability and increased spinal loading (due to muscle guarding and splinting) or reduced spinal stability (inhibition of spinal stabilizing muscles) leading to pain (O’Sullivan, 2005). It is proposed that there are three main groups that present with chronic disabling lumbopelvic pain with regard to motor control impairments (O’Sullivan, 2005). 1. The first group appears to be represented by subjects where the movement impairment and motor dysfunction is secondary and adaptive to an underlying pathological process such as inflammatory pain disorders, neurogenic pain, neuropathic or centrally mediated pain disorders, severe structural disorders. 1356-689X/$ - see front matter doi:10.1016/j.math.2006.01.002

2. A second group exists where a dominance of psychological and/or social (non-organic) factors are the underlying drive behind the disorder. This results in altered central processing, amplification of pain, and resultant disordered movement and motor dysfunction. In these two groups, attempts to simply normalize the motor dysfunction and movement impairment does not result in resolution of the disorder and is likely to fail. 3. It is proposed that a third group exists where maladaptive movement and motor patterns result in chronic abnormal tissue loading and ongoing pain and distress. This group appears to present in two manners: (a) Pain disorders associated with ‘movement impairment’ classification are characterized by avoidant pain behaviour and are associated with a loss of normal physiological lumbopevic mobility in the direction of pain. These disorders present with abnormally high levels of muscle guarding and co-contraction of lumbopelvic muscles. This results in abnormally high levels of compressive loading across articulations, excessive stability and hence movement restriction as well as muscle strain and fatique. This is usually accompanied by fear of moving into the painful impairment, as well as faulty cognitive coping strategies and beliefs regarding the pain disorder. This represents a mal-adaptive response to a pain disorder and a mechanism for ongoing pain and disability. Management of this group is based on a cognitive behavioural model. The aim is to reduce fear of movement and reduce muscle tone by education and facilitating graduated movement exposure into the painful range in a relaxed and normal manner.

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(b) Pain disorders associated with ‘control impairment’ classification are associated with no impairment to the mobility of the symptomatic spinal segment in the direction of pain provocation. Rather they present with impairments in the control of the symptomatic spinal segment in the direction of pain. This is associated with deficits in motor control with the inability to effectively control the neutral zone of the motion segment or fix the spinal segment at an end range provocative positions. This appears to result in pain secondary to recurrent end range strain and non-physiological spinal segment movement and loading. These patients adopt postures and movement patterns that are maladaptive, provocative (not avoidant) and represents a mechanism for ongoing pain and disability. A motor learning intervention based on a cognitive behavioural treatment model with the aim of changing faulty movement behaviour that is linked to the pain disorder is advocated for these disorders. There is growing evidence to support the presence of these sub-groups of patients leading to effective targeted interventions (O’Sullivan, 2000, 2004, 2005; O’Sullivan et al., 2002, 2003, 2006; Burnett et al., 2004; Elvey and O’Sullivan, 2004; Dankaerts et al., 2006a, b).

References Burnett A, Cornelius A, Dankaerts W, O’Sullivan P. Spinal kinematics and trunk muscle activity in cyclists: a comparison between healthy controls and non-specific chronic low back pain subjects. Manual Therapy 2004;9:211–9. Dankaerts W, O’Sullivan PB, Straker LM, Burnett AF, Skouen JS. The inter-examiner reliability of a classification method for nonspecific chronic low back pain patients with motor control impairment. Manual Therapy 2006a;11:28–39. Dankaerts W, O’Sullivan PB, Burnett AF, Straker LM. Differences in sitting postures are associated with non-specific chronic low back pain disorders when sub-classified. Spine 2006b; in press. Elvey R, O’Sullivan P. A contemporary approach to manual therapy. Modern Manual Therapy. Boyling and Jull, 3rd ed. Amsterdam: Elsevier; 2004. O’Sullivan P. Lumbar segmental instability: clinical presentation and specific exercise management. Manual Therapy 2000;5(1):2–12. O’Sullivan P. Clinical instability of the lumbar spine. Modern Manual Therapy. Boyling and Jull, 3rd ed. Amsterdam: Elsevier; 2004. O’Sullivan P. Diagnosis and classification of chronic low back pain disorders: maladaptive movement and motor control impairments as underlying mechanism. Manual Therapy 2005;10:242–255. O’Sullivan P, Beales D, Beetham J, Cripps J, Graf F, Lin I, et al. Altered motor control in subjects with sacro-iliac joint pain during the active straight leg raise test. Spine 2002;27(1):E1–8. O’Sullivan P, Burnett A, et al. Lumbar repositioning deficit in a specific low back pain population. Spine 2003;28(10):1074–9. O’Sullivan PB, Mitchell T, Bulich P, Waller R, Holte J. The relationship between posture, lumbar muscle endurance and low back pain in industrial workers. Manual Therapy 2006; in press. Waddell G. The back pain revolution. Edinburgh: Churchill Livingstone; 2004.

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Keynote address

Workshop: Clinical implications for clinicians treating patients with non-specific arm pain, whiplash and carpal tunnel syndrome Jane Greeninga,b, a

Department of Physiology, University College London, Gower Street, London WC1E 6BT, UK b R.L. Physiotherapy Clinics, London EC1A 2EJ, UK

Received 24 October 2005; received in revised form 17 February 2006; accepted 2 March 2006

Abstract Nerve sheath inflammation without significant axonal degeneration can result in c fibres (both axons in continuity and the nervi nervorum) becoming spontaneously active and mechanically sensitive. This may help explain the painful responses when examining neural dynamics in patients with non specific arm pain, carpal tunnel syndrome and arm pain following whiplash injury, when longitudinal nerve excursion (measured using ultrasound imaging), appears to be within normal ranges. These findings have implications for the clinical examination and treatment of these patients groups. r 2006 Elsevier Ltd. All rights reserved. Keywords: Non-specific arm pain; Whiplash; Carpal tunnel syndrome; Ultrasound imaging; Nerve mechanosensitivity; Nerve movement

1. Introduction Traditionally, standard examination of the peripheral nervous system has relied on a clinical examination of nerve function (tests of reflex, muscle power and sensation), with the gold standard for indication of nerve injury being abnormal findings on nerve conduction studies. Physiotherapists in particular have added to the range of clinical tests by applying movement tests to major nerve plexuses and peripheral nerves. Positive tests being interpreted as an indication of change in neural dynamics. The utility of nerve conduction tests is in demonstrating conduction loss following frank nerve injury and in indicating the site of nerve damage. However, sensory conduction velocities tell us little with regard to the function of C and Ad fibres. Further, as clinicians, we see many patients who present with symptoms suggesCorresponding author. Department of Physiology, University College London, Gower Street, London WC1E 6BT, UK. Tel.: +44 020 7679 7334; fax: +44 020 7383 7005. E-mail address: [email protected].

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tive of neuropathy but without obvious signs of nerve damage and in who nerve conduction studies are normal. Examples are patients with chronic whiplash disorders and patients with non-specific arm pain (NSAP) (previously referred to as repetitive strain injury). Subtle changes to the function of large myelinated sensory nerve fibres, small dorsal root fibres and sympathetic fibres have been found in NSAP patients consistent with a minor neuropathy (Greening et al., 2003). Clinically, both patients with NSAP and upper limb pain following whiplash injury demonstrate similar painful responses to movement tests of the brachial plexus and upper limb peripheral nerves and have hyperalgesic responses to digital mechanical pressure applied over the plexus and peripheral nerve trunks (Quintner, 1989; Ide et al., 2001; Greening et al., 2001, 2005). Studies, using high frequency ultrasound imaging, of median nerve movement in patients with NSAP and those with arm symptoms following whiplash injury indicate change to nerve movement during deep breathing, an interesting finding that may indicate alteration to the environment around the cords of the brachial plexus

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at the thoracic outlet (Greening et al., 2005). In addition, patients with NSAP have a reduction in transverse median nerve movement at the proximal carpal tunnel but importantly do not have significant change to longitudinal nerve movement with wrist or finger extension (Greening et al., 2001; Lynn et al., 2002). Similarly, while patients with carpal tunnel syndrome (CTS) have reduced transverse movement of the median nerve at the wrist, there is no reduction in longitudinal median nerve sliding through the carpal tunnel in response to finger extension (Erel et al., 2003). A surprising result since CTS is considered to be a common nerve entrapment syndrome. Recent physiological work has shown that nerves that have sustained minor injury, or inflammation, are capable of producing neuropathic symptoms. Results from animal studies of neural mechanosensitivity following nerve inflammation demonstrate C-fibre firing in response to nerve pressure, as well as C-fibre firing in responses to nerve stretch (within the physiological range) (Bove et al., 2003; Dilley et al., 2005). These are important findings that may help explain nerve trunk hyperalgesia and suggest that neuro-mechanosensitivity rather than frank nerve entrapment may result in ‘‘positive findings’’ when tests of nerve movement are applied clinically.

2. Clinical significance Neuropathic symptoms following minor nerve injury may be more common than previously suspected. The presence of minor nerve injury in patients with NSAP and whiplash has implications not just for assessment but also for the treatment of this and other similar conditions. Findings of C-fibre mechanosensitivity to nerve stretch following nerve sheath inflammation and

no reduction in longitudinal nerve movement in CTS have implications for our understanding of the cause of painful responses when applying clinical tests of nerve movement. For many patients with minor nerve injuries, the only indication of nerve injury, apart from symptom characteristics, would be changed sensory thresholds and positive neural provocation tests.

References Bove GM, Ransil BJ, Lin HC, Leem JG. Inflammation induces ectopic mechanical sensitivity in axons of nociceptors innervating deep tissues. Journal of Neurophysiology 2003;90:1949–55. Dilley A, Lynn B, Pang SJ. Pressure and stretch mechanosensitivity of peripheral nerve fibres following local inflammation of the nerve trunk. Pain 2005;117:412–62. Erel E, Dilley A, Greening J, Morris V, Lynn B. Longitudinal sliding of the median nerve in the forearm during finger movements in normal subjects and in patients with carpal tunnel syndrome. Journal of Hand Surgery (Br) 2003;5:439–43. Greening J, Lynn B, Leary R, Warren L, O’Higgins P, Hall-Craggs M. The use of ultrasound imaging to demonstrate reduced movement of the median nerve during wrist flexion in patients with nonspecific arm pain. Journal of Hand Surgery 2001;26B(5):401–6. Greening J, Lynn B, Leary R. Sensory and autonomic function and ultrasound nerve imaging in RSI patients and keyboard workers. Pain 2003;104:275–81. Greening J, Dilley A, Lynn B. In vivo study of nerve movement and mechanosensitivity of the median nerve in whiplash and nonspecific arm pain patients. Pain 2005;115:248–53. Ide M, Ide J, Yamagam M, Takagik K. Symptoms and signs of irritation of the brachial plexus in whiplash injuries. Journal of Bone and Joint Surgery (Br) 2001;83:226–9. Lynn B, Greening J, Leary R. Sensory and autonomic function and ultrasound nerve imaging in RSI patients and keyboard workers. HSE Contract Report 417/2002, 2002. Quintner J. A study of upper limb pain and paraesthesia following neck injury in motor vehicle accidents: assessment of brachial plexus tension test of Elvey. British Journal of Rheumatology 1989;28:528–33.

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Keynote Address

Tissue pathophysiology, neuroplasticity and motor behavioural changes in painful repetitive motion injuries Ann E. Barr Temple University, Philadelphia, PA, USA Received 28 October 2005; accepted 30 March 2006

Keywords: Repetitive motion injury; Inflammation; Carpal tunnel syndrome; Motor behaviour

1. Introduction Therapeutic interventions in repetitive motion disorder have focused primarily on the musculoskeletal tissues of the ‘‘exposed’’ body parts. Yet, many patients experience persistent symptoms and chronic disability in spite of treatment of localized tissue injury. Work with an in vivo model in the rat to determine both the nature of tissue pathophysiology and the dose–response relationship between repetition-force and tissue pathophysiology has provided insight into such systemic and nervous system effects.

2. Methods Rats are trained to reach and grasp a small food pellet or a force handle, in which case they pull at a target force threshold to obtain a food pellet reward, for 2 h/ day, 3 days/week. Four repetition-force protocols have been used: high repetition-high force (HRHF; 8–12 reaches/min, 60% maximum grip strength), high-repetition-low force (HRLF; 8–12 reaches/min, o15% maximum grip strength), low repetition-high force (LRHF; 4–6 reaches/min, 60% maximum grip strength) and LRLF (4–6 reaches/min, o15% maximum grip strength). Reach rate, task duration (the amount of time per day the animals are willing to participate in the task), grip strength, paw sensation, and grooming skill are monE-mail address: [email protected]. 1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.03.007

itored. Nerve conduction velocity (NCV) is determined for the median nerve. Tissues and serum are examined for evidence of injury, inflammation and fibrosis. Spinal cord and somatosensory cortex have also been examined for evidence of neuroplasticity.

3. Review of results Evidence of tissue injury includes decreased median nerve NCV in the HRLF, HRHF, and LRHF groups by 12 weeks, which is accompanied by decreased grip strength and paw sensation. These findings are indicative of carpal tunnel syndrome (Clark et al., 2003, 2004). Myotendinous fibrillation is evident as early as 6 weeks of HRLF task performance, and is accompanied by infiltrating macrophages (Barbe et al., 2003). Cortical bone at sites of tendon or ligament attachments undergoes degradation by osteoclasts and formation of woven bone (Barr et al., 2003), a pathological finding in the mature skeleton. Macrophage infiltration is evident in many tissues, including tendon, connective tissue, muscle, and peripheral nerve, and is found in the distal as well as the proximal forelimb (Barbe et al., 2003; Barr et al., 2003; Barr and Barbe, 2004). The macrophage response is dose-dependent (HRHF4HRLF4LRLF) with respect to number of infiltrating cells and time to resolution of the response. The macrophage response extends to the contralateral, nonreach limb and the hindlimb (Barr et al., 2004). The production of pro-inflammatory cytokines by several cell types also accompanies the

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macrophage response. In addition, IL-1 alpha is upregulated in the serum of HRLF animals by 8 weeks, suggesting a systemic inflammatory response. Fibrosis is evident in and around the median nerve after 12 weeks of the HRLF and HRHF tasks (Clark et al., 2003, 2004). Changes to the spinal cord are bilateral, with upregulation of substance P and its receptors in the superficial laminae of the bilateral dorsal horns by 5 weeks. Reach rate is maintained throughout the first 6 weeks in the LRLF group, it declines in week 6 in the HRLF and LRHF groups, and declines in weeks 3 and 6 in the HRHF group. Grip strength also declines in the HRLF and HRHF groups (Clark et al., 2003, 2004). Animals develop an uncoordinated, raking movement pattern regardless of task level, but the LRLF group exhibits this behaviour to a lesser degree. This movement pattern is associated with prolonged reach time and difficulty manipulating and eating small food pellets (Barbe et al., 2003; Barr et al., 2002). Finally, there are several behavioural outcomes that indicate a sickness response in our model (Dantzer, 2004). Task duration is accompanied by somnolence and decreases in a dosedependent manner. Decreased grooming skill is accompanied by an increased frequency of non-responses rather than a degradation of forelimb function. This type of behavioural withdrawal is similar to the types of behaviours noted in other animal models of acute infection or cytokine-mediated illness (Watkins and Maier, 1999; Dantzer, 2004).

4. Conclusions This model shows the effects of repetitive and/or forceful movements of the upper limb on tissues and on behaviour. Findings show that cumulative exposure to this task causes tissue and behavioural responses consistent with repetitive strain injury. The primary tissue response is inflammatory and appears to be mediated by inflammatory cells and proinflammatory molecules within the first 3–8 weeks, although the inflammatory response is dependent on tissue type and task exposure, declining with lower task demands. There is a resolution of the cytokine response in the HRLF and LRLF groups despite continued task performance (although macrophages continue to increase in some tissue types through week 12 in the HRLF group).

Progressive degradation of motor performance is evident among animals at high exposure levels. In addition to loss of motor performance ability, animals performing the HR and/or HF tasks exhibit sickness behaviours. These findings show a complex bio-psychosocial response to the performance of highly repetitive and/or forceful tasks that may be mediated by the immune system through a widespread inflammatory mechanism (Barr et al., 2004). These findings provide evidence for a highly complex response to the performance of highly repetitive motions that involves not only the exposed peripheral tissues, but also somatosensory and affective as well as regulatory structures of the central nervous system. Clinicians should refocus treatment to encompass all of the tissues and systems affected by repetitive motion disorders.

References Barbe MF, Barr AE, Amin A, Gorzelany I, Gaughan JP, Safadi F. Repetitive reaching and grasping causes motor decrements and systemic inflammation. Journal of Orthopaedic Research 2003;21:7–16. Barr AE, Barbe MF. Inflammation reduces physiological tissue tolerance in the development of work related musculoskeletal disorders. Journal of Electromyography and Kinesiology 2004;14:77–85. Barr AE, Amin M, Barbe MF. Dose–response relationship between reach repetition and indicators of inflammation and movement dysfunction in a rat model of work-related musculoskeletal disorder. Proceedings of the HFES 46th Annual Meeting, 2002. p. 1486–90. Barr AE, Safadi FF, Gorzelany I, Amin A, Popoff SN, Barbe MB. Highly repetitive, negligible force reaching in rats causes pathological overloading of upper extremity bones. Journal of Bone and Mineral Research 2003;18:2023–32. Barr AE, Barbe MF, Clark BD. Systemic inflammatory mediators contribute to widespread effects in work-related musculoskeletal disorders. Exercise and Sport Sciences Reviews 2004;32(4):135–42. Clark BD, Barr AE, Safadi F, Beitman L, Al-Shatti TA, Barbe MF. Median nerve microtrauma in a model of work-related musculoskeletal disorder. Journal of Neurotrauma 2003;20:681–95. Clark BD, Al-Shatti TA, Barr AE, Amin M, Barbe MF. Performance of a High-repetition, high-force task induces carpal tunnel syndrome in rats. Journal of Orthopaedic and Sports Physical Therapy 2004;34:244–53. Dantzer R. Cytokine-induced sickness behavior: a neuroimmune response to activation of innate immunity. European Journal of Pharmacology 2004;500:399–411. Watkins LR, Maier SF. Implications of immune-to-brain communication for sickness and pain. Proceedings of the National Academy of Sciences, USA 1999;96:7710–3.

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Measuring and managing pain and performance Maureen J. Simmonds Faculty of Medicine, School of Physical Therapy and Occupational Therapy, Centre de recherche interdisciplinaire en readaptation, McGill Centre for Research on Pain, McGill University, 3654 Promenade Sir William Osier, Montreal, Que., Canada H3G 1Y5 Received 4 July 2005; accepted 2 March 2006

Abstract Pain and movement dysfunction are invariant sensory and motor expressions of health disorders. They are also complex, interrelated problems and may be accompanied by fatigue and depressed mood. Optimum management is predicated on the appropriate selection, application and interpretation of assessment measures. Research on pain and physical function using physical performance tests has shown that regardless of whether pain and impairment is a consequence of musculo-skeletal injury or systemic disease such as cancers, pain-free individuals outperform those with pain in terms of movement speed and endurance ability across a variety of performance tests (e.g. walk and reach tests, and repeated sit-to-stand and trunk flexion tests). Slow movements are characterized by fractionated and extraneous movement patterns. They are also associated with a relatively high level of muscle activity (amplitude and duration) throughout the task compared to fast movements. Slow movements are also relatively inefficient in terms of physiological energy and time burden. For a similar level of effort, individuals with pain are able to perform significantly less work. Our research has shown that individuals with pain move slower across a range of self-selected movement speeds i.e. slow, preferred and fast speeds. It is also apparent that patients systematically over estimate expected pain during task performance at faster speeds. Preliminary work using speed targeted treatment shows promise in terms of improving physical performance and reducing the burden of illness and physical dysfunction. r 2006 Elsevier Ltd. All rights reserved. Keywords: Pain; Physical performance; Assessment

1. Introduction Pain and movement dysfunction are the most common signs and symptoms of health problems. These key problems predominate, regardless of whether the problem is one of injury or illness; regardless of the type of injury or illness (e.g. osteoarthritis, stroke, or cancers); regardless of which bodily system is primarily affected (e.g. neurological, musculoskeletal, cardiovascular or visceral); and regardless of the age or gender of the affected individual. Despite this high prevalence of pain, a preponderance of evidence indicates that it is frequently poorly managed within the health care environment. Inappropriate and inadequate assessment, advice and management of pain add to the health Tel.: +514 398 8864; fax: +514 398 5439.

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burden, distress and dysfunction for the individual and for society. A variety of national and international initiatives have aimed to increase awareness of pain and improve the knowledge of health care practitioners, patients and others about pain, thereby anticipating improvement in pain management. For example, a recent mandate in the United States required that medical schools examine their curricula for pain content. Also, the primary accreditation agency for health related care in the United States; Joint Commission on Accreditation of Healthcare Organizations (http://www.icaho.org) now requires hospitals and clinics to meet specific criteria on pain management in order to gain or maintain accreditation status. For instance, hospitals and clinics are required to:




recognize the right of patients to appropriate assessment and management of their pain

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assess pain in all patients record the results of the assessment in a way that facilitates regular reassessment and follow-up educate relevant providers in pain assessment and management determine competency in pain assessment and management during the orientation of all new clinical staff establish policies and procedures that support appropriate prescription or ordering of pain medications ensure that pain does not interfere with participation in rehabilitation educate patients and their families about the importance of effective pain management include patients’ needs for symptom management in the discharge planning process collect data to monitor the appropriateness and effectiveness of pain management

These standards explicitly acknowledge that pain is a co-existing condition with a number of diseases and injuries, and that it requires explicit attention (http:// www.jcrinc.com/). Movement difficulty or dysfunction is the other common reason for health care referral. Movement dysfunction can be a co-morbid problem, a cause or a consequence of pain. The relationship between pain and movement dysfunction is not as simple or ‘obvious’ as often believed. Rather, pain and movement are both complex and multidimensional. Moreover, both pain and movement are part of an integrated system that is mediated by myriad cognitive, emotional, and social factors. Recognition of the complexity of the problem, and the limitations of biomedical and/biomechanical factors as explanatory models of pain and movement dysfunction have led to an expanded conceptual (biopsycho-social) model of health and disability (e.g. Simmonds et al., 2000). This expanded conceptual model of management clearly requires an expanded assessment approach i.e. assessment and management at a functional rather than impairment level. Assessment at a functional level tests the ability of an individual to put together a series of movements (rather than a single movement of a single joint in a single plane) to safely and efficiently complete a task i.e. it assesses function of the person rather than function of the part of the person. It follows that this ‘person’ level approach helps focus treatment at the level of the person (mind, body and social domain i.e. bio-psycho-social approach).

2. Assessment Assessment of function at the level of the person can be carried out using standardized, psychometrically sound self report measures complemented by standar-

dized, psychometrically sound physical performance task batteries (Lee et al., 2000). Self-report measures required for assessment of function may be condition specific e.g. Roland and Morris Disability Questionnaire for back problems (Roland and Morris, 1983), or generic e.g. SF-12 (Ware et al., 1996). Self-report measures are valuable but they do not always differentiate between whether or why a specific task is not done or can’t be done. More importantly, self-report measures do not accurately characterize or quantify the impact of the health condition nor a change in that impact. For example, a common self-report item addresses walking ability; e.g. ‘‘I walk more slowly because of my back pain’’ or ‘‘I have difficulty walking’’. These items may be appropriately endorsed by an individual but they do not provide an objective or quantifiable measure of ‘‘walking more slowly’’ or ‘‘with difficulty’’ either at baseline or following an intervention. It is plausible that performance may change, in either direction, with an intervention or over time. However, because this change is not quantified it cannot be used to guide or refine treatment. Standardized, simple physical performance task batteries have been developed and tested for a variety of different conditions (see Table 1). These task batteries measure the time taken to complete a specific task once (e.g. fast 50 foot walk) or several times (e.g. repeated sitto-stand), or the distance reached or walked in a given time (e.g. 5 or 6 min). The measurement of simple everyday tasks has clinical utility and is meaningful to patient and practitioner. These measures can be used to characterize and quantify the impact of specific conditions. They can also be used to guide and refine treatment and to systematically examine the effect of specific modifiable (e.g. pain) or non-modifiable factors (e.g. gender) on movement and function. We have tested the psychometric properties of physical performance batteries in patients with back pain (Simmonds et al., 1998), various types of cancers (Simmonds, 2002) and in patients with HIV/AIDS (Simmonds et al., 2005). The performance test batteries have strong test–retest, intra- inter-rater and day-to-day reliabilities (rp:7). They also have strong discriminative, concurrent, construct, and predictive validity (Novy et al., 2002), and are responsive to change. Two constructs underlie physical performance and these are speed/coordination and endurance (Novy et al., 2002; Simmonds, 2002). The Physical Performance task battery has now become part of the standard clinical assessment in a number of centres worldwide and has been used as an assessment and outcome measure in many research studies. This systematic evaluation of physical performance across patient groups and compared to norms, has allowed us to characterize and quantify the impact of specific conditions, and the effect of mediating factors

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Table 1 Description of physical performance tests and protocol for standardized task batteries physical performance batteries Task

Repeated sit-to-stand Repeated trunk flexion Loaded reach

Fifty-foot walk Five-minute walk 3601 rollover

Coin test Belt tie Sock test Repeated sit-to-stand Repeated reach-up

Forward reach

Fifty-foot walk Six-minute walk

Pen pick-up All tasks in cancer Battery

Procedure

Measure

Back pain Subjects rise to standing and return to sitting as quickly as possible, five times. After a brief pause the task is repeated. Subjects are timed as they bend forward to the limit of their range and return to the upright position as quickly as tolerated, five times. After a brief pause the task is repeated. Subjects stand next to a wall on which a meter rule is mounted horizontally at shoulder height. They hold a weight that is 5% of their body weight (up to maximum of 5 kg) at shoulder height and close to the body and then reach forward. Subjects walk 25 feet, turn around, and walk back to the start as fast as they can. Subjects walk as far and as fast as they can for 5 min. Subjects lie supine on a treatment bed. They roll over 3601 as quickly as they can. After a brief pause, they roll 3601 in the opposite direction. Cancer physical performance Subjects sit at a table. They are timed as they pick up four coins and place them in a cup. (They are required to pick up each coin individually.) Subjects sit in a standard chair. They are timed as they wrap a bandage (approximately 4 feet long) around their waists and tie it in front of them. Subjects sit in a standard chair. They are timed as they put on one loose-fitting sock. Subjects rise to standing and return to sitting as quickly as possible twice. After a brief pause the task is repeated. Subjects stand facing a wall and reach up as high as they can with both hands. A mark is placed on the wall at the reach distance. Subjects then reach up and return their hands to their sides three times, as quickly as they can. After a brief pause the task is repeated. Subjects stand sideways next to a wall on which a meter rule is mounted horizontally at shoulder height. They then reach forward as far as they can. Subjects walk 25 feet, turn around, and walk back to the start as fast as they can. Subjects walk as far and as fast as they can for 6 min. (They are allowed to sit and rest if and as necessary during the 6-min period.) HIV/AIDS Subjects stand and a pen is placed on the floor directly in front of their feet. They then bend down and pick up the pen as quickly as they can. As in cancer battery

such as gender, age, pain distribution, and fatigue on psychomotor performance (Novy et al., 1999; Lee et al., 2002; Simmonds et al., 2005). It has also allowed for the identification of fundamental and common effects of injury and disease (psychomotor slowing) on physical performance. This has led us to test specific speed targeted intervention approaches. Preliminary results from these pilot trials suggest that this approach holds promise in terms of ameliorating the impact of illness, injury, and aging on psychomotor performance (see later). Individuals with low back pain are outperformed by age and gender matched pain free norms across physical performance tasks. However the magnitude of compromise is task specific. For example, individuals with LBP have about a 20% compromise in walking (i.e. they walk about 80% of the distance of healthy norms in 5 min) but approximately 40% compromise in sit-to-stand

Average time of the two tasks Average time of the two tasks Maximum distance reached in centimetres Total time Distance walked is recorded. The time to complete a rollover in both directions is totalled Total time Time taken is recorded Time taken is recorded Average time of two tasks Average time of two tasks Maximum distance reached (in centimetres) is recorded Time taken is recorded Distance walked is recorded Time taken is recorded

(Simmonds et al., 1998). Individuals with HIV/AIDS also have a 25% compromise in walking but a 75% compromise in the sit-to-stand test (Simmonds et al., 2005). This is important information because it provides an indication of the burden of the compromise—it is not only time consuming to move slowly, it is also physiologically inefficient. Many individuals with pain, illness, and physical dysfunction often have fatigue as part of their symptom burden. Although the mechanisms have not been fully elucidated it is feasible that movement and performance inefficiencies are contributors to the problem. It is also possible that slow movements are not a consequence of the disorder but rather are a motor expression of the disorder. It is interesting that despite significant performance differences between patient groups and age and gender matched norms, the (perceived) effort required to perform the task is actually very similar

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(Simmonds, 2002), i.e. 100% effort is required to perform at 80% (or less) capacity. Central fatigue and local muscle fatigue is often a problem for individuals with systemic illness as well as those with musculoskeletal problems (e.g. back pain) and it also compromises physical performance. For example, in a group of individuals with HIV/AIDS, 98% of patients had complaints of fatigue (mean 5.472.3 on a 10) that was associated with compromised physical performance. Fatigue in patients with AIDS, like those with cancer may be related to anaemia. Improvements in haemoglobin level by transfusion or medication (e.g. Procrit) results in improved physical performance (Simmonds, 2002). For patients with back pain, the problem of muscle vs. general fatigue/weakness is less clear. For example, the Sorensen test of trunk extension was purported to be a test of muscle fatigue/ endurance of the spinal extensor muscles (BieringSorensen, 1984). However, this assertion was based on a study which tested healthy pain free subjects. When this test of ‘‘muscle endurance’’ is used in healthy pain free individuals, indeed muscle fatigue is the limiting performance factor. In contrast, when individuals with back problems are tested, the limiting factor is one of pain; i.e. the test is one of pain tolerance rather than muscle weakness (Lee et al., 2002). This is a very important distinction because it changes the conceptual understanding and interpretation of the problem and thus the therapeutic management of the problem. Clearly this is a problem of pain rather than muscle weakness. It is also a problem of over-interpretation of the results of studies. The problem of over-interpretation of studies and misinterpretation of studies findings due to a biased or incomplete conceptualization of the problem is replete in the literature. The difficulty of framing the right question should not be underestimated. Moreover, if the question is based on inadequate or flawed conceptual framework, the answer is not only moot it may lead to erroneous and potentially ineffective or harmful interventions. This can be a source of frustration for patient and practitioner. Treatment failures contribute to distress and disability and may also lead to learned helplessness—a significant consequence of an incomplete conceptual framework. Individuals with pain and illness move more slowly than age and gender matched cohorts across a variety of performance tests which use ‘‘time’’ as the performance indicator. Individuals not only move more slowly when they are attempting to move ‘as fast as they can’, they also move more slowly (walk and sit-to-stand tasks) across a continuum of speeds (i.e. slow, preferred and fast) compared to an age and gender matched cohort. The reason for this shift in speed has not been completely investigated. It is plausible that the relatively slow ‘preferred’ speed is simply used as the ‘conceptual speed anchor’ and the individual calibrates against this

Fig. 1. Pre-post difference scores for subjects with back pain and a control performing the repeated sit-to-stand task (n ¼ 30). Topical heat increased performance speed but only in the back pain group and only in the preferred speed condition. NB: topical heat decreased pain in the back pain group (t ¼ 3:2, p ¼ :006).

preferred speed in order to move relatively slower or faster. We have explored movement speed in patients with back pain. Factors that influence speed of movement include the presence of referred leg pain. For example, at preferred speed of walking, there are significant differences in walking speed between each of three subject groups (individuals with referred leg pain, individuals with back pain only, and an age and gender matched control group). However when challenged to walk faster, individuals with back pain only, can achieve speeds close to those of a control group however this is not possible for those with referred leg pain (Lee et al., 2000). Using a sit-to-stand task we examined the effect of actual and anticipated pain on movement as well as the effect of pain relief (Simmonds and Rebelo, 2003). We found that patients systematically and significantly overestimated expected pain at preferred and fastest speeds of movement. There was also a trend towards underestimating expected pain at slow speeds but this was not significant. Topical heat significantly reduced pain and led to an increase in movement speed but only at preferred speed (Fig. 1). The fact that topical heat did not change movement speeds in the control group suggests that the change in performance was pain related and not related to physiological warm up of the tissues or non-specific (i.e. placebo) effects.

3. Treatment approaches The use of standardized physical performance tests as assessment and outcome measures has led to a better understanding of the impact of illness, injury and symptoms (pain and fatigue). It has also led to more

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holistic functionally driven and activity based treatment approaches. Given that psychomotor slowing is a universal expression of illness, injury and indeed aging, some investigators have begun to test speed targeted interventions (Lamontagne and Fung, 2004). We have begun to test simple walking protocol, based on a Wingate protocol. This protocol involves repetitions of three minutes of walking at preferred speed interspersed with 30 s of walking at fastest speed. The number of repetitions of this protocol are increased over a 4 or 8 week period in order to improve the training effect. The feasibility of this simple protocol has been tested and preliminary results show promise in terms of improving physical and cognitive performance across a range of tasks. References Biering-Sorensen F. Physical measurements as risk indicators for lowback trouble over a one-year period. Spine 1984;9(2):106–19. Lamontagne A, Fung J. Faster is better: Implications for speedintensive gait training after stroke. Stroke 2004;35:2543. Lee CE, Simmonds MJ, Novy DM, Jones SC. A comparison of selfreport and clinician measured physical function among patients with low back pain. Archives of Physical Medicine and Rehabilitation 2000;82:227–31. Lee CE, Simmonds MJ, Etnyre BR, Morris GS, Jones SC. Ground reaction forces pattern of walking in individuals with and without low back pain. Cleveland: International Society for the Study of the Lumbar Spine; 2002. Novy DM, Simmonds MJ, Olson S, Lee CE. Gender differences in physical performance in individuals with and without low back pain. Archives of Physical Medicine and Rehabilitation 1999;80:195–8.

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Novy DM, Simmonds MJ, Lee CE. Physical performance tasks: what are the underlying constructs? Archives of Physical Medicine and Rehabilitation 2002;83(l):44–7. Roland M, Morris R. A study of the natural history of back pain. Part I: Development of a reliable and sensitive measure of disability in low back pain. Spine 1983;8:141–4. Simmonds MJ. Physical function in patients with cancer. Psychometric characteristics and clinical usefulness of a physical performance test battery. Journal of Pain and Symptom Management 2002;24: 404–14. Simmonds MJ. The effect of pain and illness on movement: assessment methods and their meanings. In: Giamberadino M, editor. Pain clinical update. Seattle: IASP Press; 2002. p. 179–87. Simmonds MJ, Rebelo V. Self-selected speed of movement during a repeated sit-to-stand task in individuals with and without LBP. Fourth congress of european federation of the international association for the study of pain chapters, Prague, Czech republic, September 2–6, 2003. Simmonds MJ, Olson S, Novy D, Jones S, Hussein T, Lee CE, et al. Physical performance tests: are they psyehometrically sound and clinically useful for patients with low back pain? Spine 1998;22(23):2412–21. Simmonds MJ, Novy DM, Sandoval R. The influence of pain and fatigue on physical performance and health status in ambulatory patients with HIV. Clinical Journal of Pain 2005;3(21):200–6. Simmonds MJ, Harding V, Watson P, Claveau Y. Physical therapy assessment: expanding the model. In: Proceedings of the ninth world congress on pain. Progress in Pain Research and Management, August 22–27, 1999, Vienna, Austria, vol. 16, 2000. p. 1013–30. Ware JE, Kosinski M, Keller SD. A 12-iten short form health survey: construction of scales and preliminary tests of reliability and validity. Med care 1996;34:220–33.

Online Resources http://www.icaho.org/news+room/health+care+issues/painmonojc.pdf www.icrinc.com/

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Keynote address

Balancing the ‘bio’ with the psychosocial in whiplash associated disorders$ Michele Sterling Division of Physiotherapy, The University of Queensland, St Lucia 4072, Australia Received 28 October 2005; received in revised form 23 December 2005; accepted 3 February 2006

The biopsychosocial model of pain and disability (Main et al., 2000) has provided a framework to explain (persistent) musculoskeletal pain by illustrating the influences of mainly psychosocial factors. Whilst some physiological factors are referred to, these are limited to non-specific factors such as reduced physical activity, guarded movement, and physical deconditioning (Main et al., 2000). The separation of physical and psychological aspects of pain may not be possible but focusing primarily on psychological factors will provide a limited view of the patient’s pain condition. As Merskey (2005) points out all potential contributions from relevant physiological (biomedical), psychological and social factors underlying the pain should be explored. With respect to the enigmatic condition of whiplash associated disorder (WAD) numerous factors including psychosocial aspects, accident-related features, pathoanatomical structures and compensation/litigation factors have been investigated in the attempt to understand the cause/s of transition to chronicity that occurs in some. Despite these investigations, two recent systematic reviews could agree on only high initial pain intensity as showing consistent evidence for delayed functional recovery (Cote et al., 2001; Scholten-Peeters et al., 2003). However, since the time of these reviews, recent longitudinal data have provided important information of both physical and psychological influences on recovery from whiplash. In a cohort of 80 acutely (o1 month) injured whiplash people, those with poor recovery at both 6 months and 2 years post injury $ Work is attributed to Division of Physiotherapy, The University of Qld. E-mail address: [email protected].

1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.02.001

demonstrated a more complex presentation when compared to recovered participants and those with less severe symptoms. This consisted of motor dysfunction, widespread mechanical and thermal hyperalgesia and posttraumatic stress symptoms, these features being present very soon after injury and persisting throughout the study periods. In contrast the only deficits that persisted in those people with full or reasonable recovery were cervical muscle dysfunction with both local cervical hyperalgesia and psychological distress resolving by 2–3 months. The strongest predictors of poor recovery were a combination of high initial levels of pain and disability, cervical movement loss, cold hyperalgesia and moderate levels of posttraumatic stress (Sterling et al., 2005, 2006). The predictive capacity of this combination of factors was superior to pain and disability levels alone where the factor combination categorized 70% of those who developed moderate/ severe symptoms compared to only 37% using only pain and disability scores (Sterling et al., 2005, 2006) emphasizing the importance of considering these additional factors in the early assessment of the whiplash injured. Sensory hypersensitivity of WAD has been shown to occur independently of psychological distress (Sterling et al., 2003) and whilst demonstrating a relationship with posttraumatic stress, this relationship is mediated by pain and disability levels (Sterling and Kenardy, 2006) suggesting that psychological factors alone cannot explain the sensory disturbance. A more likely explanation is that it reflects biological phenomena involving augmented central pain processing. It has been shown that widespread sensory hypersensitivity does not occur in idiopathic (non-traumatic) neck pain indicating

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different underlying mechanisms to these two conditions (Scott et al., 2005). Further investigation of this phenomena in our laboratories have shown that chronic WAD participants with sensory hypersensitivity also demonstrate lowered detection thresholds in the hands for vibration, electrical and heat stimuli–that is hypoaesthesia to these stimuli occurring concurrently with lowered pain thresholds or hypersensitivity. A lowering of vibration and electrical detection thresholds suggest Abeta fibre dysfunction with lowered heat detection threshold suggestive of C fibre dysfunction. When taken together these findings may indicate that a minor peripheral nerve injury is a possible contributor to whiplash pain (Chien et al., 2005). Such a proposal is not totally without basis with animal, cadaver and clinical studies providing circumstantial evidence that nerve damage is possible with whiplash injury (Ortengren et al., 1996; Taylor and Taylor, 1996; Ide et al., 2001). Although such injuries are yet to be verified with diagnostic imaging. The influence of widespread sensory hypersensitivity on physiotherapy interventions has been explored in a preliminary randomized controlled trial of a multimodal physiotherapy program for chronic whiplash. Whilst the multimodal approach consisting of education, advice, manual therapy and specific exercise was superior to education and advice alone, it was much less effective in subjects with both mechanical and cold hyperalgesia compared to those without these sensory features (Jull et al., 2005). It is not yet known what is the most efficacious treatment for the whiplash group with these features but it will likely involve a multiprofessional approach including the physiotherapist, psychologist and general medical practitioner. The accumulation of recent research clearly demonstrates acute and chronic whiplash injury to be a heterogeneous condition involving both physical or biological (motor dysfunction, sensory disturbance) and psychological factors to varying degrees. This heterogeneity implies that assessment of the whiplash patient will need to consider all possible aspects of this

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condition, both physical and psychosocial. A specific treatment approach targeting deficits identified in individual patients may offer hope in the quest to prevent the transition to chronicity associated with this condition.

References Chien A, Eliav E, Sterling M. Sensory function in chronic whiplash associated disorders, 11th World Congress on Pain, Sydney, 2005. Cote P, Cassidy D, Carroll L, Frank J, Bombardier C. A systematic review of the prognosis of acute whiplash and a new conceptual framework to synthesize the literature Spine 2001;26:E445–58. Jull G, Sterling M, Kenardy J, Beller E. A randomised controlled trial for chronic whiplash, 2005 submitted for publication. Main C, Spanswick C, Watson P. The nature of disability. In: Main C, Spanswick C, editors. Pain management: an interdisciplinary approach. Churchill Livingstone: Edinburgh; 2000. p. 89. Merskey H. Distortion of the biopsychosocial approach. Pain 2005;113:240–2. Ortengren T, Hanssen H, Lovsund P, Svenssen M, Suneson A, Saljo A. Membrane leakage in spinal ganglion nerve cells induced by experimental whiplash extension motion: a study in pigs. Journal of Neurotrauma 1996;13:171–80. Scholten-Peeters G, Verhagen A, Bekkering G, van der Windt D, Barnsley L, Oostendorp R, et al. Prognostic factors of whiplash associated disorders: a systematic review of prospective cohort studies. Pain 2003;104:303–22. Scott D, Jull G, Sterling M. Sensory hypersensitivity is a feature of chronic whiplash associated disorders but not chronic idiopathic neck pain. Clinical Journal of Pain 2005;21:175–81. Sterling M, Jull G, Vicenzino B, Kenardy J. Sensory hypersensitivity occurs soon after whiplash injury and is associated with poor recovery. Pain 2003;104:509–17. Sterling M, Jull G, Vicenzino B, Kenardy J, Darnell R. Physical and psychological factors predict outcome following whiplash injury. Pain 2005;114:141–8. Sterling, M., Jull, G., Kenardy, J. Physical and psychological predictors of outcome following whiplash injury maintain predictive capacity at long term follow-up. Pain. 2006, in press. Sterling, M., Kenardy, J. The relationship between sensory and sympathetic nervous system changes and acute posttraumatic stress following whiplash injury–a prospective study, Journal of Psychosomatic Research, 2006, in press. Taylor J, Taylor M. Cervical spinal injuries: an autopsy study of 109 blunt injuries. Journal of Musculoskeletal Pain 1996;4:61–79.

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Original article

The relationship between patella position and length of the iliotibial band as assessed using Ober’s test Lee Herringtona,b,, Natalie Rivetta, Samantha Munroa a

Allerton Annexe, University of Salford, Manchester M6 6PU, UK Centre for Rehabilitation and Human Performance Research, University of Salford, Manchester, UK

b

Received 28 September 2005; received in revised form 7 February 2006; accepted 1 June 2006

Abstract The purpose of the study was to investigate the relationship between length of the iliotibial band (ITB) and the medio-lateral position patella. Eighty subjects (37 male, 43 female) were examined for patella position and ITB length. All subjects were physically active, asymptomatic and aged between 18 and 34 years (mean 21.5 years). ITB length was assessed using the Ober’s test and modified Ober’s test, with hip adduction angle being measured using a fluid goniometer. Patella position was assessed using the method first described by McConnell [The management of chondromalacia patellae: a long term solution. Australian Journal of Physiotherapy 1986;32:215–22]. Patella position had a weak correlation (r ¼ 0:28) with modified Ober’s (extended knee) test and a poor correlation with Ober’s (knee flexed) test (r ¼ 0:1). In the group of 47 subjects with laterally displaced patellae, patella position had a moderate statistically significant correlation to ITB length measured by modified Ober’s test (r ¼ 0:34, P ¼ 0:012). Only a poor relationship existed between Ober’s test and patella position in the laterally displaced group. The results of this study only partially support the hypothesis that there is a relationship between ITB length and lateral patella displacement. The relationship was not strong enough to confirm ITB length as the only cause of lateral patella displacement. r 2006 Elsevier Ltd. All rights reserved. Keywords: Patella position; ITB; Ober’s test

1. Introduction Patellofemoral pain syndrome (PFPS) is the most common overuse injury occurring at the knee. In a retrospective analysis of running-related injuries conducted by Taunton et al. (2002), 17% of the injuries reported were due to PFPS, making it one of most common injuries that occurred in the 2002 cases examined. A lack of flexibility in the iliotibial band (ITB) is a factor that has been previously documented as a major contributor to the aetiology of PFPS, through its retinacular connection to the patella creating lateral displacement of the patella (Puniello, 1993).

Corresponding author. Allerton Annexe, University of Salford, Manchester M6 6PU, UK. Tel.: +44 1612 95 2326. E-mail address: [email protected] (L. Herrington).

1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.06.008

Many authors have hypothesized about the possible effect the ITB could have on patella position and tracking (Puniello, 1993; Kwak et al., 2000). Others have cited ITB tightness as a factor leading to PFPS (Puniello, 1993; Larsen et al., 1995), even though the direct evidence for such a connection is limited and is largely based on cadaveric and biomechanical modelling studies. The anatomy of the distal end of the ITB provides an indication of how the ITB might influence patella position and movement. The ITB separates into two distinct bands distally at the knee, one is the continuation of the ITB; iliotibial tract attaching into Gerdy’s tubercle of the tibia, the other is the iliopatellar band which forms an integral part of the lateral retinaculum of the knee attaching into the lateral border of the patella (Terry et al., 1986). The specific effects of ITB forces on the PFJ were studied by Kwak et al. (2000),

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who found that loading of the ITB translated the patella laterally and caused a concurrent lateral displacement of PFJ contact point at all angles of knee flexion. This was in contrast to the work of Shellock et al. (1989), who found using kinematic (dynamic) MRI that the patella displaced laterally during the first 301 of knee flexion but the lateral retinaculum remained redundant. This suggests that the potential force created by stretching of the lateral retinaculum does not cause the lateral displacement of the patella, in early knee flexion. The discrepancy between these findings might be due to the dual band nature of the ITB. Kwak et al. (2000) found that ITB loading also caused tibial external and valgus rotation (via the ITB), this would have the effect of displacing the tibial tubercle laterally, because of the fixed length of the patella tendon. This would in turn have the effect of pulling the patella laterally, without a change in lateral retinaculum length occurring and may impart explain the findings of Shellock et al. (1989). Frequently, patients suffering from PFPS are assessed for inflexibility of the ITB using Ober’s test (and its modifications), which provides an indirect measure of ITB flexibility. Ober’s test measures the amount hip adduction as a representation of ITB flexibility (Gajdosik et al., 2003). A number of studies have aimed to quantify Ober’s test as an indirect method of measuring ITB length and also assess the reliability of the measurements obtained. Melchione and Sullivan (1993) showed good intratester and intertester reliability (ICC 0.94 and 0.73, respectively). Gajdosik et al. (2003) investigated the effect of varying knee positions (901 flexion and full extension) and gender on Ober’s test, they showed that adduction angles were significantly less when the knee was flexed (Ober’s position) than extended (Modified Ober’s position). Reese and Bandy (2003) further investigated the influence of knee position on Ober’s test, they found intratester reliability to be good (Ober’s test ICC ¼ 0.90 and modified Ober’s test ICC ¼ 0.91) and a significant difference in the range of adduction obtained between Ober’s test and the modified Ober’s test (Po0:05). Despite this test being shown to be reliable and used for a number of years now, it is yet to be established if this measure of ITB length is related to the actual position of the patella. Clinically, frontal plane patella position has been assessed using the method described by McConnell (1986) for a number of years. The reliability and validity of the method has been questioned (Fitzgerald and McClure, 1995; Tomisch et al., 1996; Powers et al., 1999; Watson et al., 1999), with only the studies of Herrington (2002), Herrington and Nester (2004) and McEwan et al. (2006) supporting the reliability and validity of the technique. The major reasons for the discrepancies between these studies has been related to the level of training of the examining therapist and the use of

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interval scale measurements rather than arbitrary nominal ones (Herrington, 2002). Despite the regularly presented assertion within the literature that ITB length and patella position are related, no study to date has assessed the relationship of ITB length as assessed by Ober’s test and the frontal plane patella position. The aim of this study was therefore to establish the relationship between Ober’s test (flexed knee) and modified Ober’s test (extended knee) and frontal plane medio-lateral position of the patella using the method described by McConnell (1986).

2. Method 2.1. Subjects Eighty subjects (37 male, 43 female) were examined for patella position of their right knee and had their ITB length of the right leg examined. All subjects were physically active asymptomatic individuals aged 18–34 years (mean 21.5 years). The tests were performed in agreement with the Declaration of Helsinki and all subjects gave informed written consent to participate prior to commencing study. The study was approved by the institutional research ethics committee. 2.2. Ober’s test The subject was positioned on the side lying with the right leg upper most. A pressure biofeedback unit was placed under the pelvis to assist in detection of the onset of pelvic motion. The left leg was placed at 901 of hip and knee flexion. The shoulders and pelvis were aligned along the straight edge of the plinth. The examiner stood behind the subject and stabilized the pelvis by pushing downward with their left hand. Modified Ober’s (straight leg) and Ober’s (bent leg) tests were then performed in random order. In modified straight leg Ober’s the right leg was kept extended (Fig. 1A), while in the bent leg (standard Ober’s) the knee was flexed to 901 (Fig. 1B). The leg was held at the knee throughout the tests with the horizontal position defined as 01 before passive adduction occurred; this was measured using a fluid-filled goniometer (CE0120, MIE medical research Ltd., Leeds), as was the final position. The hip was then flexed, abducted and extended to pass the ITB over the greater trochanter before being passively adducted. A reading was taken at the onset of lateral pelvic tilt detected by the change in pressure from the baseline of 40 mmHg in the pressure biofeedback unit (Stabiliser Pressure Biofeedback, Chattanooga, Australia) of greater than 5 mmHg and palpation. Each measure was repeated three times and an average was recorded as a degree of adduction from the horizontal.

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Fig. 1. (A) Test position for the modified Ober’s test. (B) Test position for Ober’s test.

2.3. Measurement of medio-lateral patella position The method used was that described by Herrington (2002) and McConnell (1986). The medial and lateral epicondyles of the femur and mid-point of the patella were palpated on the subject’s knee, which was positioned and supported in 201 of knee flexion (in order to place the patella within the trochlea groove). The distance from the palpated position of the medial and lateral epicondyles of the femur to the mid-point of the patella was then marked on a piece of folded zinc oxide tape (Fig. 2). The medial and lateral measurements were each repeated three times on separate pieces of tape, with re-palpation of the landmarks on each occasion. 2.4. Statistical analysis Descriptive statistics were obtained for all variables. A Kolmogorov–Smirov test for normality was used to

determine if the data for all three variables were normally distributed. A Pearson correlation was used to determine the strength of relationship between patella position and Ober’s (bent leg) and modified Ober’s (straight leg) test. Intratester reliability was analysed using intraclass correlation coefficients. Data were analysed using the statistical software package SPSS (version 12).

3. Results 3.1. Intratester reliability Intratester reliability of the tests was established by repeating the measurements on five subjects on two separate occasions. Patella position measurements showed an intraclass correlation coefficient of r ¼ 0:99 (Po0:01) with a standard error of measurement of

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Fig. 2. Technique for assessing patella position.

6 mm. The measurements for Ober’s tests were r ¼ 0:96 (Po0:01) standard error of measurement 1.31 and modified Ober’s test r ¼ 0:97 (Po0:01) standard error of measurement 1.11. 3.2. Patella position On Kolmogorov–Smirov test, the data were shown to be normally distributed. Of the 80 subjects, 7 had centrally placed patellae, 26 medially and 47 laterally displaced, the mean value was
3 mm (76 mm), the minus value indicating laterally displaced position with the range varying between 23 mm laterally and 10 mm medial displacement. There was no significant difference between male and female subjects (P ¼ 0:15). 3.3. Ober’s test On Kolmogorov–Smirov test, the data were shown to be normally distributed for both tests. There were no significant differences between male and female subjects for either the Ober’s (P ¼ 0:78) or modified Ober’s test (P ¼ 0:13). The mean value for modified Ober’s test was 16.21 (75.41) of hip adduction, whilst Ober’s test had a mean value of 9.91 (74.81) of hip adduction. 3.4. Relationship between tests Patella position had a weak correlation (r ¼ 0:28) with modified Ober’s (extended knee) test and a poor correlation with Ober’s (knee flexed) test (r ¼ 0:1). In the group of 47 subjects with laterally displaced patellae, patella position had a moderate statistically significant correlation to ITB length measured by modified Ober’s test (r ¼ 0:34, P ¼ 0:012). Only a poor relationship existed between Ober’s test and patella position in the laterally displaced group (r ¼ 0:2).

4. Discussion The aim of the study was to establish if a relationship existed between an indirect measurement of ITB length, namely Ober’s test and the frontal plane position of the patella. If the relationship exists, it would lend support to the hypothesis that the ITB through its deep retinacular attached to the patella (iliopatellar band) influences position of the patella and therefore patella tracking. The findings of this study provide partial support to this hypothesis with hip adduction angle during modified Ober’s (extended knee) test having a moderate statistically significant relationship with lateral patella displacement. The findings of this study though highlighting a relationship showed it not to be an overly strong one, indicating that ITB might not be the only cause of lateral patella displacement. This in part might be due to the inability to directly measure the length of the ITB, though Ober’s test is regarded as the best available indirect measure (Melchione and Sullivan, 1993). The findings of this study reflect those of previous studies investigating ITB length (Melchione and Sullivan, 1993; Gajdosik et al., 2003; Reese and Bandy, 2003) and the differences they found between the modified and original Ober’s test are also mirrored in the findings of the present study. Reese and Bandy (2003) stated that the inability to control pelvic movement brought about the greatest variability in the results seen in the literature in relation to the range of findings when undertaking Ober’s test. This study used a previously untried method to control the pelvis, which though far less complex than the fixation rig used by Reese and Bandy (2003) produced very similar results. The measurement of the patella position could have proved a potential source of measurement error as it is essentially based on palpation and its reliability and

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validity have been questioned (Powers et al., 1999), although in two subsequent studies (Herrington, 2002; Herrington et al., 2005), good validity and reliability has been demonstrated. The intratester reliability in this study was also shown to be excellent (r ¼ 0:99), supporting these studies. Shellock et al. (1989) found the lateral retinaculum to be redundant during the first 301 of knee flexion despite the patella being translated laterally, indicating that the tension from the ITB on its iliopatellar band is not significant in positioning or drawing the patella laterally. Interestingly, Kwak et al. (2000) showed that it might not be the iliopatellar band of the ITB which causes lateral patella displacement, but the tibial external and valgus rotation caused by the ITB through its attachment to Gerdy’s tubercle. The tibial external and valgus rotation would have the effect of displacing the tibial tubercle laterally and because of the fixed length of the patella tendon, it would pull the patella laterally, without a change in lateral retinaculum length occurring. With reference to the findings of this study, this would indicate that those subjects, who had laterally displaced patellae and short ITB, might have their relatively laterally placed patella, not because of short lateral retinaculum, but because of the lateral transposition of the tibial tubercle. This would have implications for manual therapists who might have to direct their attention to mobilizing the tibia medially, rather than the patella medially.

5. Conclusion In the clinical literature, the assertion that patella position and ITB length are interrelated is regularly presented; despite this, no study to date has presented research to support this contention. The results of this study only partially support the hypothesis that there is a relationship between ITB length and lateral patella displacement. The relationship was not strong enough to confirm ITB length as the only cause of lateral patella displacement. References Fitzgerald K, McClure P. Reliability of measurements obtained with four tests for patellofemoral alignment. Physical Therapy 1995;75:84–92.

Gajdosik R, Sandler M, Marr H. Influence of knee positions and gender on the Ober test for length of the iliotibial band. Clinical Biomechanics 2003;18:77–9. Herrington L. The inter-tester reliability of a clinical measurement used to determine the medial lateral orientation of the patella. Manual Therapy 2002;7:163–7. Herrington L, Nester C. Q-angle undervalued? The relationship between Q angle and medio-lateral position of the patella. Clinical Biomechanics 2004;19:1070–3. McEwan I, Herrington L, Thom J. The validity of a clinical measure of patella position. Manual Therapy 2006 6, in press, doi:10.1016/ j.math.2006.06.013. Kwak S, Ahmad C, Gardner T, Grelsamer R, Henry J, Blankevoort L, et al. Hamstring and iliotibial band forces affect knee kinematics and contact pattern. Journal of Orthopaedic Research 2000;18:101–8. Larsen B, Andersen E, Urter A, Mickelson M, Newhouse K. Patellar taping: a radiological examination of medial glide taping. American Journal of Sports Medicine 1995;23:465–71. McConnell J. The management of chondromalacia patellae: a long term solution. Australian Journal of Physiotherapy 1986;32: 215–22. Melchione W, Sullivan M. The reliability of measurements obtained by use of an instrument designed to indirectly measure iliotibial band length. Journal of Orthopaedic and Sports Physical Therapy 1993;18:511–5. Powers C, Mortenson S, Nishimoto D, Simon D. Criterion-related validity of a clinical measurement to determine the medial/lateral component of patellar orientation. Journal of Orthopaedic and Sports Physical Therapy 1999;29:372–7. Puniello M. Iliotibial band tightness and medial patella glide in patients with patellofemoral dysfunction. Journal of Orthopaedic and Sports Physical Therapy 1993;17:144–8. Reese N, Bandy W. Use of an inclinometer to measure flexibility of the iliotibial band using the Ober test and the modified Ober test: differences in magnitude and reliability of measurements. Journal of Orthopaedic and Sports Physical Therapy 2003;33: 326–30. Shellock F, Mink J, Deutsch A, Fox J. Patellar tracking abnormalities: clinical experience with kinematic MR imaging in 130 patients. Radiology 1989;172:799–804. Taunton J, Ryan M, Clement D, Mckenzie D, Llyod-Smith D, Zumbo B. A retrospective case-control analysis of 2002 running injuries. British Journal of Sports Medicine 2002;36:95–101. Terry G, Hughston C, Norwood L. The anatomy of the iliopatellar band and iliotibial tract. American Journal of Sports Medicine 1986;14:39–45. Tomisch D, Nitz A, Threlkeld J, Shapiro R. Patellofemoral alignment: reliability. Journal of Orthopaedic and Sports Physical Therapy 1996;23:200–8. Watson C, Propps M, Galt W, Redding A, Dobbs D. Reliability of McConnell’s classification of patellar orientation in symptomatic and asymptomatic subjects. Journal of Orthopaedic and Sports Physical Therapy 1999;29:378–85.

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Manual Therapy 11 (2006) 187–191 www.elsevier.com/locate/math

Original article

Chronic musculoskeletal pain in chronic fatigue syndrome: Recent developments and therapeutic implications Jo Nijsa,b,, Mira Meeusa,b,1, Kenny De Meirleira a

Department of Human Physiology, Faculty of Physical Education and Physiotherapy, Vrije Universiteit Brussel, Belgium Department of Health Sciences, Division of Musculoskeletal Physiotherapy, Higher Institute of Physiotherapy, Hogeschool Antwerpen, Belgium

b

Received 10 October 2005; received in revised form 8 March 2006; accepted 30 March 2006

Abstract Patients with chronic fatigue syndrome (CFS) experience chronic musculoskeletal pain which is even more debilitating than fatigue. Scientific research data gathered around the world enables clinicians to understand, at least in part, chronic musculoskeletal pain in CFS patients. Generalized joint hypermobility and benign joint hypermobility syndrome appear to be highly prevalent among CFS sufferers, but they do not seem to be of any clinical importance. On the other hand, pain catastrophizing accounts for a substantial portion of musculoskeletal pain and is a predictor of exercise performance in CFS patients. The evidence concerning pain catastrophizing is supportive of the indirect evidence of a dysfunctional pain processing system in CFS patients with musculoskeletal pain. CFS sufferers respond to incremental exercise with a lengthened and accentuated oxidative stress response, explaining muscle pain, postexertional malaise, and the decrease in pain threshold following graded exercise in CFS patients. Applying the scientific evidence to the manual physiotherapy profession, pacing self-management techniques and pain neurophysiology education are indicated for the treatment of musculoskeletal pain in CFS patients. Studies examining the effectiveness of these strategies for CFS patients are warranted. r 2006 Elsevier Ltd. All rights reserved.

1. Introduction The main feature of chronic fatigue syndrome (CFS) diagnosis is the exclusion of all conditions other than CFS (e.g. diabetes, cancer, and obesity), together with the presence of a debilitating fatigue lasting for at least 6 months (Holmes et al., 1988; Fukuda et al., 1994). Worsening of symptoms (pain, fatigue) is typically seen after previously well-tolerated levels of exercise/physical activity. Chronic fatigue has been arbitrarily put forward as the primary symptom of CFS. Between 54% and 75% Corresponding author. Vrije Universiteit Brussel, MFYS/SPORT, KRO-gebouw –1, Laarbeeklaan 101, B-1090 Brussels, Belgium. Tel.: +32 2 4774604; fax: +32 2 4774607. E-mail address: [email protected] (J. Nijs). 1 Mira Meeus is financially supported by a Ph.D. grant (‘‘Chronic pain in chronic fatigue syndrome: a biopsychosocial approach’’) supplied by the Higher Institute of Physiotherapy, Department of Health Care Sciences, Hogeschool Antwerpen, Antwerp, Belgium.

1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.03.008

of CFS patients experience chronic widespread pain (Nishikai et al., 2001). Chronic fatigue with widespread muscle and joint pain has been suggested as an important subclass of CFS (Tan et al., 2002), and the observed associations between musculoskeletal pain severity and disability (r between 0.51 and 0.58) was similar to the association between fatigue severity and disability (r ¼ 0:50) (Nijs et al., 2003a, 2004a). The latter suggests musculoskeletal pain to be as important as fatigue to CFS patients. A few years ago, little was known about the nature of chronic musculoskeletal pain in CFS. To date, scientific research data gathered around the world enables clinicians to understand, at least in part, chronic musculoskeletal pain in CFS patients. The present manuscript provides the reader with our current understanding of chronic musculoskeletal pain in CFS patients. In the US, patients with CFS are often seen in chiropractic practise. Studying the health-care use of 402

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patients from a university-based chronic fatigue clinic, it was found that 27% of CFS patients visited chiropractors, and 12% visited osteopaths (Bombardier and Buchwald, 1996). Nearly 56% of the studied patients fulfilling the diagnostic criteria for both CFS and Fibromyalgia visited chiropractors, and 15.3% visited osteopaths. Although studies examining the effectiveness of interventions aiming at reducing musculoskeletal pain in CFS are scarce, the knowledge addressing chronic musculoskeletal pain in CFS enables clinicians to provide a plausible treatment strategy. Therefore, this manuscript provides suggestions for manual physiotherapists to treat chronic musculoskeletal pain in CFS patients.

2. Musculoskeletal pain in CFS: is generalized joint hypermobility an issue? If generalized joint hypermobility appears to be an issue in CFS, then physiotherapists should include joint hypermobility in the assessment and management of CFS. Generalized joint hypermobility (assessed using the Beighton et al., 1973 criteria) was more prevalent in patients with CFS than in matched healthy controls (21% versus 4%; P ¼ 0:004) (Nijs et al., 2006). The majority of CFS patients (58.8%) fulfilled the criteria for benign joint hypermobility syndrome (BJHS) (as described by Grahame et al., 2000). Knee proprioception was similar in both groups (P ¼ 0:81), and no associations were found between generalized joint hypermobility and self-reported pain severity, disability, or knee proprioception. There appears to be no association between musculoskeletal pain and joint hypermobility in CFS patients (Nijs et al., 2004b). A review of the evidence on generalized joint hypermobility in Fibromyalgia and CFS, together with an overview on assessment and treatment strategies, is presented elsewhere (Nijs, 2005). If generalized joint hypermobility is not of clinical importance to CFS patients, then other factors must explain chronic musculoskeletal pain in CFS.

3. Musculoskeletal pain in CFS: a biopsychosocial explanation The study showing decreased pain threshold following graded exercise in CFS patients (Whiteside et al., 2004) suggested a link between impaired exercise performance and pain experience in CFS patients (in healthy subjects, a substantial increase in pain threshold in response to exercise is typically observed). A recent study (Nijs et al., under review) provided evidence supportive of this assumption: pain catastrophizing was identified as a major predictor of exercise performance in female CFS

patients experiencing chronic widespread pain. In addition, pain catastrophizing was found to predict bodily pain, even after controlling for depression. From previous studies, it is concluded that fear of movement (‘kinesiophobia’) is not related to exercise performance in CFS patients (Nijs et al., 2004c, d). In addition, kinesiophobia in general (fear of an exercise-triggered increase in general symptom severity), rather than painrelated fear of movement, was related to self-reported disability in CFS patients (Nijs et al., 2004c). There is a body of literature providing evidence for somatization (Johnson et al., 1996; Fischler et al., 1997) and activity-avoidance (Nijs et al., 2004c) in CFS patients. These cognitive styles and personality traits, together with pain catastrophizing, may result in sensitization of dorsal horn spinal cord neurons (through inhibition of descending tracks in the central nervous system), or are the result of central sensitization (Zusman, 2002). Central sensitization is defined as ‘‘an augmentation of responsiveness of central pain-signalling neurons to input from low-threshold mechanoreceptors’’ (Meyer et al., 1995). Direct evidence supporting the central sensitization hypothesis in CFS patients is currently lacking. Still, the observed decreased pain threshold following graded exercise in CFS patients is indicative of a dysfunctional central antinociceptive mechanism in CFS (Whiteside et al., 2004), and evidence of a deregulated serotonergic neurotransmission in the brain of CFS patients, consistent with altered pain processing, has been provided (Yamamoto et al., 2004). Strong evidence supportive of altered central sensory processing (i.e. central sensitization) among patients with Fibromyalgia has been published (Staud et al., 2001, 2003; Price et al., 2002; Banic et al., 2004). Studies examining whether these data apply to CFS patients with chronic widespread pain are underway. The central sensitization hypothesis fits our current understanding of CFS psychopathology and pathophysiology. The link with CFS psychopathology has been outlined in the preceding paragraph. From a pathophysiologic perspective, the evidence of a high prevalence of opportunistic infections (e.g. Vojdani et al., 1998; Nijs et al., 2002) is consistent with the numerous reports of deregulated and suppressed immune functioning in CFS patients (e.g. Suhadolnik et al., 1997; Levine et al., 1998; Nijs et al., 2003b). Deregulation of intracellular immune function was even found to be a predictor of physiological exercise parameters (Nijs et al., 2005). Infection triggers the release of the pro-inflammatory cytokine interleukin-1b, which is known to play a major role in inducing cyclooxygenase-2 (COX-2) and prostaglandin E2 expression in the central nervous system (Bazan, 2001; Samad et al., 2001). Upregulation of COX-2 and prostaglandin E2 sensitizes peripheral nerve terminals. Indeed, even peripheral infections activate spinal cord

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glia (both microglia and astrocytes), which in turn enhance the pain response by releasing nitric oxide (NO) and proinflammatory cytokines (for a detailed description of these complex pathophysiological interactions, the interested readers are referred to Maier and Watkins, 1998; Watkins and Maier, 1999). These dynamic immune-to-brain communication pathways can explain a wide variety of psychological and physiological symptoms (the ‘sickness response’) seen in patients with CFS. In addition, Vikman et al. (2003) demonstrated that long-term treatment of cultured spinal dorsal horn neurons with interferon-gamma triggers NO-dependent reduction of GluR1 clustering on dendrites (GluR1 together with GluR2 are the two most prominent AMPA receptors in the superficial dorsal horn), accompanied by an enhanced spontaneous activity in the neuronal network. Since GluR1 is mainly associated with inhibitory neurons, these observations underscore the role of a NO-dependent reduction in inhibitory activity of the central nervous system in central sensitization. Since elevated NO levels have been documented in CFS patients (Kurup and Kurup, 2003), and oxidative stress was found to be associated with symptom expression (including musculoskeletal pain) in CFS patients (Richards et al., 2000; Vecchiet et al., 2003; Kennedy et al., 2005), the observations by Vikman et al. (2003) may explain part of the chronic pain experience in patients with CFS. Moreover, experimental evidence has shown that CFS patients respond to incremental exercise with a lengthened and accentuated oxidative stress response, explaining muscle pain and postexertional malaise as typically seen in CFS subjects (Jammes et al., 2005). On the other hand, substance P levels do not seem to be upregulated in CFS patients (Evengard et al., 1998). Substance P, a peptide involved in the neurotransmission of pain from the periphery to the central nervous system, is typically elevated in patients with Fibromyalgia. Still, from the available evidence it is concluded that chronic widespread musculoskeletal pain in CFS patients fits our current understanding of the complex biopsychosocial interactions in CFS.

4. Manual physiotherapy as a treatment for chronic musculoskeletal pain in CFS patients? What can the manual physiotherapy profession offer to patients with CFS experiencing chronic widespread musculoskeletal pain? From our current understanding of chronic musculoskeletal pain in CFS, as presented above, it is clear that hands-on manual therapy techniques are not indicated for treating chronic musculoskeletal pain in all CFS cases. Still, local musculoskeletal problems like thoracic outlet compres-

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sion syndrome, low back pain, and neck pain are often seen in CFS patients. In selected cases, the local musculoskeletal problems may be more than epiphenomena: from our own clinic we recall patients reporting the onset of CFS symptoms after a Whiplash trauma, or after a rupture of the symphysis pubis during delivery and consequent lumbopelvic instability. In these patients, appropriate manual physiotherapy did not cure the disease, but was able to resolve the localized musculoskeletal pain problem and associated disability. Trained manual physiotherapists are able to differentiate between a localized and a central pain problem, even in a complex disorder like CFS. In case of the former, local manual therapy techniques are indicated, but should be adopted in respect to the reduced pain threshold and pathophysiology of the patient. In case of the latter, behavioural treatment strategies and pain neurophysiology education are indicated. This will be explained in the next paragraphs. What kind of behavioural treatment can diminish musculoskeletal pain in CFS patients? The effectiveness of graded exercise therapy and cognitive behavioural therapy for CFS patients has frequently been examined. In many of the published studies, graded exercise therapy has been adopted as a component of the cognitive behavioural programme (i.e. graded exercise was used as a way to diminish avoidance behaviour towards physical activity). According to the Cochrane Library, both treatment strategies are effective in the short term for treating CFS patients (Price and Couper, 1998; Edmonds et al., 2004). Unfortunately, the studies examining the effectiveness of graded exercise therapy/ cognitive behavioural therapy in CFS did not use (musculoskeletal) pain as an outcome measure (e.g. Deale et al., 1997; Fulcher and White, 1997; Powell et al., 2001; Prins et al., 2001). Secondly, none of the studies referenced here applied the current diagnostic criteria for CFS (Fukuda et al., 1994), making it difficult to extrapolate these results to other settings. Thirdly, from a large treatment audit among British CFS patients, it was concluded that approximately 50% of the patients stated that graded exercise therapy worsened their condition (Shephard, 2001). Finally, graded exercise therapy does not comply with our current understanding of CFS exercise physiology. As outlined above, experimental evidence is now available showing increased oxidative stress in response to (sub)maximal exercise and subsequent increased fatigue and musculoskeletal pain (postexertional malaise). Pacing, a strategy where patients are encouraged to achieve an appropriate balance between activity and rest in order to avoid exacerbation and to set realistic goals for increasing activity, is an alternative for the cognitive behavioural approach (CFS/ME Working Group, 2001; Shephard, 2001). This energy management strategy involves avoiding activities to a degree that exacerbates

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symptoms or interspersing activity with periods of rest (CFS/ME Working Group, 2001; Shephard, 2001). Contrary to the cognitive behavioural approach, pacing takes into account the considerable fluctuations in symptom severity (Shephard, 2001) and the delayed recovery from exercise (Paul et al., 1999) that typically occurs in patients with CFS. The pacing approach is consistent with the recent observations regarding the interactions between malfunctioning of the immune system, physical activity, and musculoskeletal pain in CFS patients. The first goal of the pacing approach is to enable the CFS patient to manage his/her daily activities in a way he/she no longer experiences fluctuations in symptoms (stabilization phase). Next, the physiotherapist can start to grade activity and exercise levels (grading phase). During the grading phase, the same pacing techniques are applied to grade both activity level and exercise level (i.e. flexible, accounting for the fluctuating nature of the disorder). To prevent overactive patients in exceeding their own limits, heart rate monitoring can be applied for intensity control (heart rate guidelines are obtained from the exercise stress test with continuous cardiorespiratory monitoring). This type of graded exercise has been found to be superior over relaxation and flexibility training in CFS patients (Wallmann et al., 2004). Finally, pain neurophysiology education might be indicated for CFS patients with musculoskeletal pain. As outlined above, pain processing is likely to be abnormal in CFS patients, and evidence showing that pain catastrophizing accounts for a substantial portion of musculoskeletal pain in CFS has been provided. Pain neurophysiology education was found to be effective in reducing pain catastrophizing in chronic low back pain patients (Moseley, 2002; Moseley et al., 2004).

5. Conclusion Recent studies have provided new insights into our understanding of chronic widespread musculoskeletal pain in CFS patients. Generalized joint hypermobility and BJHS appear to be highly prevalent among CFS sufferers, but they do not seem to be of any clinical importance. On the other hand, pain catastrophizing accounts for a substantial portion of musculoskeletal pain and exercise performance in CFS patients. The evidence concerning pain catastrophizing is supportive of the indirect evidence of a dysfunctional pain processing system in CFS patients with musculoskeletal pain. CFS sufferers respond to incremental exercise with a lengthened and accentuated oxidative stress response, explaining muscle pain, postexertional malaise, and the decrease in pain threshold following graded exercise in CFS patients. Applying the scientific evidence on musculoskeletal pain to the practise of manual phy-

siotherapy, pacing self-management techniques, and pain neurophysiology education are indicated for the treatment of musculoskeletal pain in CFS patients. Studies examining the effectiveness of these strategies for CFS patients are warranted. References Banic B, Petersen-Felix S, Andersen OK, et al. Evidence for spinal cord hypersensitivity in chronic pain after whiplash injury and in fibromyalgia. Pain 2004;107:7–15. Bazan NG. COX-2 as a multifunctional neuronal modulator. Nature Medicine 2001;7:414–5. Beighton PH, Solomon L, Soskolne CL. Articular mobility in an African population. Annals of the Rheumatic Diseases 1973;32: 413–7. Bombardier CH, Buchwald D. Chronic fatigue, chronic fatigue syndrome, and fibromyalgia. Disability and health-care use. Medical Care 1996;34:924–30. CFS/ME Working Group. Report to the Chief Medical Officer of an independent working group, Department of Health, London, 2001. www.doh.gov.uk/cmo/cfsmereport/index.htm. Deale A, Chalder T, Marks I, Wessely S. Cognitive behavior therapy for chronic fatigue syndrome: a randomized controlled trial. American Journal of Psychiatry 1997;154:408–14. Edmonds M, McGuire H, Price J. Exercise therapy for chronic fatigue syndrome. Cochrane Database Systematic Reviews. 2004;3:CD003200.pub2. doi:10.1002/14651858.CD003200.pub2. Evengard B, Nilsson CG, Lindh G, Lindquist, Eneroth P, Fredrikson S, et al. Chronic fatigue syndrome differs from fibromyalgia. No evidence for elevated substance P levels in cerebrospinal fluid of patients with chronic fatigue syndrome. Pain 1998;78:153–5. Fischler B, Dendale P, Michiels V, Cluydts R, Kaufman L, De Meirleir K. Physical fatigability and exercise capacity in chronic fatigue syndrome: association with disability, somatization and psychopathology. Journal of Psychosomatic Research 1997;42:369–78. Fukuda K, Straus S, Hickie I, et al. The chronic fatigue syndrome: a comprehensive approach to its definition and study. Annals of Internal Medicine 1994;121:953–9. Fulcher KY, White PD. Randomised controlled trial of graded exercise in patients with the chronic fatigue syndrome. British Medical Journal 1997;314:1647–52. Grahame R, Bird HA, Child A. The revised (Brighton 1998) criteria for the diagnosis of benign joint hypermobility syndrome (BJHS). Journal of Rheumatology 2000;27:1777–9. Holmes G, Kaplan J, Gantz J, et al. Chronic fatigue syndrome: a working case definition. Annals of Internal Medicine 1988;108:387–9. Jammes Y, Steinberg JG, Mambrini O, Bre´geon F, Delliaux S. Chronic fatigue syndrome: assessment of increased oxidative stress and altered muscle excitability in response to incremental exercise. Journal of Internal Medicine 2005;257:299–310. Johnson SK, DeLuca J, Natelson BH. Assessing somatization disorder in the chronic fatigue syndrome. Psychosomatic Medicine 1996;58:50–7. Kennedy G, Spence VA, McLaren M, Hill A, Underwood C, Belch JJ. Oxidative stress levels are raised in chronic fatigue syndrome and are associated with clinical symptoms. Free Radical Biology and Medicine 2005;39(5):584–9. Kurup RK, Kurup PA. Hypothalamic digoxin, cerebral chemical dominance and myalgic encephalomyelitis. International Journal of Neuroscience 2003;113:683–701. Levine PH, Whiteside TL, Friberg D, et al. Dysfunction of natural killer cell activity in a family with chronic fatigue syndrome. Clinical Immunology and Immunopathology 1998;88(1):99–104.

ARTICLE IN PRESS J. Nijs et al. / Manual Therapy 11 (2006) 187–191 Maier SF, Watkins LR. Cytokines for psychologists: implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychological Review 1998;105: 83–107. Meyer RA, Campbell JN, Raja SN. Peripheral neural mechanisms of nociception. In: Wall PD, Melzack R, editors. Textbook of Pain. third ed. Edinburgh: Churchill Livingstone; 1995. p. 13–44. Moseley L. Combined phsyiotherapy and education is efficacious for chronic low back pain. Australian Journal of Physiotherapy 2002;48:297–302. Moseley GL, Nicholas MK, Hodges PW. A randomized controlled trial of intensive neurophysiology education in chronic low back pain. Clinical Journal of Pain 2004;20:324–30. Nijs J. Generalized joint hypermobility: an issue in fibromyalgia and chronic fatigue syndrome? (review). Journal of Bodywork and Movement Therapies 2005;9:310–7. Nijs J, Nicolson GL, De Becker P, Coomans D, De Meirleir K. High prevalence of Mycoplasma infections among European chronic fatigue syndrome patients. Examination of four Mycoplasma species in blood of chronic fatigue syndrome patients. FEMS Immunology and Medical Microbiology 2002;34:209–14. Nijs J, Vaes P, McGregor N, Van Hoof E, De Meirleir K. Psychometric properties of the Dutch Chronic Fatigue Syndrome Activities and Participation Questionnaire (CFS-APQ). Physical Therapy 2003a;83:444–54. Nijs J, De Becker P, De Meirleir K, Demanet C, Vincken W, Schuermans D, et al. Associations between immune cell parameters and bronchial hyperresponsiveness in patients with chronic fatigue syndrome. Chest 2003b;123:998–1007. Nijs J, Cloostermans B, McGregor N, Vaes P, De Meirleir K. Construct validity and internal consistency of the chronic fatigue syndrome activities and participation questionnaire (CFS-APQ). Physiotherapy Theory and Practice 2004a;20:31–40. Nijs J, De Meirleir K, Truyen S. Hypermobility in patients with chronic fatigue syndrome: preliminary observations. Journal of Musculoskeletal Pain 2004b;12:9–17. Nijs J, De Meirleir K, Duquet W. Kinesiophobia in chronic fatigue syndrome: assessment and associations with disability. Archives of Physical Medicine and Rehabilitation 2004c;85:1586–92. Nijs J, Vanherberghen K, Duquet W, De Meirleir K. Chronic fatigue syndrome: lack of association between pain-related fear of movement and exercise capacity and disability. Physical Therapy 2004d;84:696–705. Nijs J, Meeus M, McGregor NR, Meeusen R, De Schutter G, Van Hoof E, et al. Chronic fatigue syndrome: exercise performance related to immune dysfunction. Medicine and Science in Sports and Exercise 2005;37:1647–54. Nijs J, Aerts A, De Meirleir K. Generalized joint hypermobility is more common in chronic fatigue syndrome than in healthy controls. Journal of Manipulative and Physiological Therapeutics 2006;29:32–9. Nijs, J., Van de Putte, K., Louckx, F., Truyen, S., De Meirleir, K. under review. Exercise performance and chronic pain in chronic fatigue syndrome: the role of pain catastrophizing. Nishikai M, Tomomatsu S, Hankins RW, Takagi S, Miyachi K, Kosaka S, et al. Autoantibodies to a 68/48 kDa protein in chronic fatigue syndrome and primary fibromyalgia: a possible marker for hypersomnia and cognitive disorders. Rheumatology 2001;40:806–10. Paul L, Wood L, Behan WMH, Maclaren WM. Demonstration of delayed recovery from fatiguing exercise in chronic fatigue syndrome. European Journal of Neurology 1999;6:63–9.

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Price JR, Couper J. Cognitive behaviour therapy for chronic fatigue syndrome in adults. Cochrane Database Systematic Reviews 1998;4:CD001027. doi:10.1002/14651858.CD001027. Price DD, Staud R, Robinson ME, et al. Enhanced temporal summation of second pain and its central modulation in fibromyalgia patients. Pain 2002;99:49–59. Prins JB, Bleijenberg, Bazelmans E, Elving LD, de Boo TM, Severens JL, et al. Cognitive behaviour therapy for chronic fatigue syndrome: a multicenter randomised controlled trial. Lancet 2001;357:841–7. Powell P, Bentall RP, Nye FJ, Edwards RHT. Randomised controlled trial of patient education to encourage graded exercise in chronic fatigue syndrome. British Medical Journal 2001 322-1-5. Richards RS, Roberts TK, McGregor NR, Dunstan RH, Butt HL. Blood parameters indicative of oxidative stress are associated with symptom expression in chronic fatigue syndrome. Redox Report 2000;5:35–41. Samad TA, Moore KA, Sapirstein A, Billet S, Allchorne A, Poole S, et al. Interleukin-1 beta-mediated induction of COX-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 2001;410:471–5. Shephard C. Pacing and exercise in chronic fatigue syndrome. Physiotherapy 2001;87:395–6. Staud R, Vierck CJ, Cannon RL, et al. Abnormal sensitization and temporal summation of second pain (wind-up) in patients with fibromyalgia syndrome. Pain 2001;91:165–75. Staud R, Robinson ME, Vierck Jr. CJ, Price DD. Diffuse noxious inhibitory controls (DNIC) attenuate temporal summation of second pain in normal males but not in normal females or fibromyalgia patients. Pain 2003;101:167–74. Suhadolnik RJ, Peterson DL, O’Brien K, et al. Biochemical evidence for a novel low molecular weight 2–5A-dependent RNase L in chronic fatigue syndrome. Journal of Interferon and Cytokine Research 1997;17:377–85. Tan EM, Sugura K, Gupta S. The case definition of chronic fatigue syndrome. Journal of Clinical Immunology 2002;22:8–12. Vecchiet J, Cipollone F, Falasca K, Mezzetti A, Pizzigallo E, Bucciarelli T, et al. Relationship between musculoskeletal symptoms and blood markers of oxidative stress in patients with chronic fatigue syndrome. Neuroscience Letters 2003;335:151–4. Vikman KS, Hill RH, Backstro¨m E, Robertson B, Kristensson K. Interferon-gamma induces characteristics of central sensitization in spinal dorsal horn neurons in vitro. Pain 2003;106:241–51. Vojdani A, Choppa PC, Tagle C, Andrin R, Samini B, Lapp CW. Detection of Mycoplasma genus and Mycoplasma fermentans by PCR in patients with chronic fatigue syndrome. FEMS Immunology and Medical Microbiology 1998;22:355–65. Wallmann KE, Morton AR, Goodman C, Grove R, Guilfoyle AM. Randomised controlled trial of graded exercise in chronic fatigue syndrome. Medical Journal of Australia 2004;180:444–8. Watkins LR, Maier SF. Implications of immune-to-brain communication for sickness and pain. Proceedings of the National Academy of Science USA 1999;96:7710–3. Whiteside A, Hansen S, Chaudhuri A. Exercise lowers pain threshold in chronic fatigue syndrome. Pain 2004;109:497–9. Yamamoto S, Ouchi Y, Onoe H, Yoshikawa E, Tsukawa E, Takahashi T, et al. Reduction of serotonin transporters of patients with chronic fatigue syndrome. NeuroReport 2004;15:2571–4. Zusman M. Forebrain-mediated sensitization of central pain pathways: ‘non-specific’ pain and a new image for MT. Manual Therapy 2002;7:80–8.

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Original article

Musculoskeletal adaptations to resistance training in old age N.D. Reeves, M.V. Narici, C.N. Maganaris Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, MMU Cheshire, Alsager Campus, Hassall Road, Alsager, Cheshire ST7 2HL, UK Received 27 October 2005; accepted 6 April 2006

Abstract Muscle weakness experienced in old age has many detrimental consequences for activities of daily life. Given the serious problems presented by weakness in old age, strategies to prevent or mitigate this process are of paramount importance. In recent years resistance training has emerged as an effective method for increasing strength in the elderly. Despite this, little is known regarding the muscular, neural and tendinous adaptations that occur with resistance training in old age. Hence, we have conducted a series of experiments to investigate these adaptations. We have found increases in maximal isometric and concentric torque by 9–37% after resistance training in older people (65–81 years). Associated with these strength gains were increases in agonist muscle neural drive without any change in the co-activation of antagonist muscles. Resistance training can cause increases in muscle size and also adaptations to the internal muscle structure. Tendons of older adults adapt to resistance training by increasing their stiffness and Young’s modulus. In conclusion, many of the musculoskeletal factors characterizing ageing can be at least partially mitigated by resistance training. r 2006 Elsevier Ltd. All rights reserved. Keywords: Old age; Exercise; Muscle; Tendon

Ageing is characterized by a loss of muscle size known as senile sarcopenia and a progressive decline in strength that accelerates after the sixth decade of life. Crosssectional comparisons of young and older adults have shown that adults 70–80 years of age are 40% weaker in terms of knee extension and plantarflexion torque as compared to young adults 20–30 years of age (Roos et al., 1999; Klein et al., 2001; Macaluso et al., 2002; Morse et al., 2004). Senile sarcopenia affecting various muscle groups is evident from cross-sectional studies showing that muscle size is 20% smaller in older adults as compared to young adults (Klein et al., 2001; Narici et al., 2003; Morse et al., 2004). The extensor muscle groups, particularly the knee and ankle extensors are most severely affected by ageing-induced declines in strength and size (Winegard et al., 1996; Lynch et al., Corresponding author. Tel.: +44 161 2475429; fax: +44 161 2476375. E-mail address: [email protected] (N.D. Reeves).

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1999; Frontera et al., 2000). This is primarily important because the extensors of the knee and ankle are the major muscle groups responsible for locomotion and will therefore impact upon many activities of daily living. For example, the loss of leg extension power with ageing has been shown to correlate with the decline in maximal gait velocity (Rantanen and Avela, 1997). As maximal leg extension power (normalized to body mass) declines, the maximal attainable gait velocity also declines. Power (the product of joint torque and velocity) declines at a faster rate than joint torque with ageing (Skelton et al., 1994), likely due to the fact that not only strength (joint torque) declines with ageing but also the velocity of muscle shortening. Given the detrimental consequences of muscle weakness in old age described above, it is of paramount importance to find ways in which this ageing-induced strength decline can be delayed or even reversed to a certain extent. In relatively recent years resistance exercise training has been shown as an effective method for reducing

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ageing-induced muscle weakness (for review see Macaluso and De Vito, 2004). Perhaps contrary to popular belief, strength gains can be achieved in old age and have been observed in 70–80 year old adults following resistance exercise training programmes (e.g. Fiatarone et al., 1990). Many studies however, have assessed strength only in terms of the repetition maximum on the exercise device used for training. Whilst this will clearly provide an important indication of any possible strength gains occurring with exercise training, due to the specific nature of the task it is likely to overestimate the ‘‘true’’ strength gains. Dynamometry based measurements of isometric and dynamic torque are required to accurately quantify any training-induced changes following exercise programmes in older adults. Furthermore, it is important to understand the origin of any possible strength gains with resistance training and identify the adaptations occurring in the different motor system components of older adults. In order to address the above issues we have conducted a series of studies investigating the musculoskeletal adaptations to resistance training in older adults. Nine older adults completed a 14-week resistance exercise training programme and nine older adults served as non-exercising controls (aged 65–81 years). The training programme was performed using resistance exercise machines (Technogym, Gambettola Italy). Exercises were performed for the major muscle groups of the upper and lower body in order to provide a wholebody conditioning stimulus. The major muscle groups of interest from an experimental perspective in the present study were the knee extensors. This muscle group was studied because of its crucial role in all locomotor activities. The main exercises performed to target the knee extensors were the leg-press and leg-extension. A 5-repetition maximum (5RM) was established for each exercise (the maximum load that could be raised and lowered under control, 5 times only). The training load corresponded to 80% of the 5RM and the repetition maximum was tested every 2 weeks in order to maintain the same relative training load. Two series of 10 repetitions were performed for each exercise and sessions were performed three times each week for 14 weeks. Pre- and post-intervention maximal isometric, concentric and eccentric knee extension torque was assessed using an isokinetic dynamometer. This device allows torque measurements to be taken in all modes of contraction whilst allowing the external angular velocity to be manipulated. These measurements enable construction of the torque–velocity relationship (Fig. 1). After training, older adults significantly increased maximal isometric torque by 9% and maximal concentric torque by 22–37% across the angular velocities tested (Reeves et al., 2005). In contrast to isometric and concentric torque, resistance training did not significantly alter eccentric torque (Fig. 1). In the control

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Fig. 1. Knee extensor torque–velocity relationship pre- and posttraining. Values are means and SD. * and ** denote significantly (Po0:05 and Po0:01, respectively) increased torque after 14 weeks of resistance training. Modified from the data presented in Reeves et al. (2005).

group, there were no changes in concentric or eccentric torque, but there was a significant decrease in isometric torque post-intervention. The strength gains brought about by resistance training may be partly attributed to increased agonist (knee extensor muscles) neural drive. Measurements of electromyographic (EMG) activity taken from the vastus lateralis muscle showed increases ranging from 28% to 38% compared to pre-training values. During voluntary contractions, muscle force and torque is produced not only by the agonist muscles but also by the antagonist muscles, which are co-activated. During knee extension contractions, antagonist muscle co-activation (knee flexors) has been shown to be higher in the elderly compared to young adults (Macaluso et al., 2002). This may be regarded as a strategy to maintain a higher degree of knee joint stability in the elderly. However, co-activation also functions to apply an opposing torque to the intended direction of effort. Higher levels of antagonist muscle co-activation therefore contribute to strength deficits in old age. Some studies suggest that resistance exercise training in older adults can reduce the level of antagonist muscle coactivation (Hakkinen et al., 1998; Hakkinen et al., 2001), an independent factor that would serve to increase strength. In our study however, the level of antagonist muscle co-activation was unaltered by resistance training, indicating that only changes in agonist muscle activation contributed to the observed strength gains. An interesting finding is that older adults did not increase eccentric torque after resistance

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training. Explanations for this finding may include the preservation of eccentric force with ageing and underloading of the eccentric contraction phase during training. It has been shown from both animal and human studies that eccentric force is relatively well preserved with ageing in relation to isometric and concentric force (Vandervoort et al., 1990; Phillips et al., 1991; Hortobagyi et al., 1995). This relative force preservation may reduce the adaptability of this muscle contraction type in response to exercise training. As illustrated by the force-velocity relationship (Fig. 1), higher forces can be generated during eccentric contractions as compared to during isometric and concentric contractions (Cook and McDonagh, 1995). During exercise training using the constant external load devices employed in our study, the repetition maximum is limited by the concentric contraction and therefore the eccentric contraction phase of the same movement will be under-loaded and may partly explain the lack of adaptation in this contraction type with training. A number of studies have shown that skeletal muscle can still adapt to an exercise training stimulus even in old age (e.g. Fiatarone et al., 1990; Hakkinen et al., 1998; Harridge et al., 1999). Using imaging techniques such as magnetic resonance imaging (MRI) and computed tomography (CT) enlargement of muscle anatomical cross-sectional area (ACSA) by 5–17% has been reported in the elderly after resistance training programmes lasting 3 months (Brown et al., 1990; Ferri et al., 2003). Indeed data from our laboratory agrees with these reports as we have found increased ACSA of the vastus lateralis muscle by 3–10% along the length of the muscle following 14 weeks of resistance training (Reeves et al., 2004b). These findings suggest a certain degree of reversal to the muscle atrophy experienced with ageing. Although the enlargement of muscle size with resistance training is a major factor contributing to the observed strength gains, it is not the sole factor. As discussed above, neural factors contribute substantially to increases in strength and other muscular and tendinous factors are also involved. In most human muscles, fascicles do not lie parallel to the length of the muscle but insert into the tendinous sheath known as the aponeurosis at an angle. The internal arrangement of muscle fascicles is referred to as muscle architecture. We have previously observed that muscle architecture is altered in old age. Gastrocnemius muscle fascicles were found to be shorter by 10% in the elderly compared to young adults and the angle at which the fascicles inserted into the aponeurosis, known as the pennation angle, was smaller by 13% in the elderly (Narici et al., 2003). We have recently shown in the vastus lateralis muscle that following 14 weeks of resistance training muscle fascicle lengths increase by 9% and pennation angles increase by 30% (Reeves et al., 2004a). These findings suggest that sarcomere

number has increased both in-series (increased fascicle length) and in-parallel (pennation angle increase) and have implications for maximal force production and the operating range length range of the muscle. Pennation is a strategy to allow more contractile material to be packed along the length of the muscle, so theoretically a greater number of sarcomeres in-parallel suggests that the muscle would be able to generate a greater maximum force. Although an increased number of sarcomeres in-series suggests that the muscle may be able to produce force over a greater length range as compared to the situation before training with fewer sarcomeres in-series, in vivo this is limited by joint constraints. Resistance training programmes for older adults can therefore not only increase gross muscle area but also cause alterations to the internal muscle structure. In addition to changes in gross muscle area, changes in muscle architecture are another muscularbased factor contributing to the strength gains observed after resistance training. Whilst most attention may intuitively be focused on the muscular adaptations to resistance training programmes, potential adaptations occurring in other musculoskeletal structures should be considered. For example, tendons are the force-transmitting structures connecting muscle to bone, thus allowing the effective transformation of contractile force in the muscle to joint movement. Tendons are not inextensible bodies, but elongate when they are subjected to the tensile load generated by muscle contraction (for review see Butler et al., 1978). The tendon’s dimensions and mechanical properties influence the degree of deformation that will take place in response to the application of a given tensile load. Information on the modification of tendon mechanical properties with changes in activity level is scanty as compared to the information available on skeletal muscle. Some inferences however, can be drawn from in vitro experiments on isolated tissues. In vitro studies suggest that ageing reduces tendon stiffness, causing a greater tendon elongation for any given force applied compared to younger tendons (Tkaczuk, 1968; Noyes and Grood 1976). Indeed the findings from experiments performed on humans in our laboratory agree with in vitro reports (Maganaris, 2001). Animal models (Woo et al., 1980, 1981, 1982; Buchanan and Marsh, 2001) have shown that when tendons undergo exercise loading above that normally experienced under habitual conditions, they respond by increasing their stiffness (i.e. they become more resistant to elongation, shown by a steeper slope of the force-elongation curve). By using ultrasound imaging to scan tendon elongation in vivo during an isometric contraction, we investigated the influence of resistance training on the mechanical properties (stiffness and Young’s modulus—stiffness normalized to the tendon’s dimensions) of the patellar tendon in older adults. After 14 weeks of resistance

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training we found that both tendon stiffness and the normalized stiffness, Young’s modulus increased by 65% and 69%, respectively (Reeves et al., 2003). The increase in the tendon Young’s modulus suggests that the stiffness increase occurred to due a change in the material properties of the tendon. These findings indicate a certain degree of reversal of the ageing effects on human tendons. The modification of tendon mechanical properties following resistance training in old age have a number of important functional implications. Firstly, depending upon their degree of elongation they can influence the speed of force transmission. The increase in tendon stiffness found after training would be expected to increase the velocity of force transmission and indeed this was shown as a faster rate of torque development at the level of the whole joint system. This may suggest that movements requiring a rapid generation of joint torque would benefit, such as the motor response to a loss of balance. Tendon stiffness and any changes with resistance training can affect the extent of muscle fibre shortening. The increase in tendon stiffness observed after resistance training would be expected to reduce the extent to which fibres in the knee extensor muscles could shorten. This was in fact the case as we observed that the vastus lateralis muscle fascicles shortened less after training, however, it was estimated that the operating range of this muscle remained unchanged (Reeves et al., 2004a). This finding was attributed to the fact that the changes occurring in both the muscle and tendon had opposite effects on fascicle shortening, interacting in order to maintain the muscle’s operating range constant pre- to post-intervention. After the resistance training programme the patellar tendons of older adults demonstrated a reduced strain (tendon elongation during contraction expressed relative to the resting tendon length) for any given level of tendon stress (tendon force divided by tendon CSA). Given that tendon strain injury or rupture is likely to occur at a given level of tendon strain when the integrity of the molecular bonds are disrupted, this finding would suggest that the likelihood of tendon strain injury in older adults might be reduced after a period of resistance training. In summary, substantial strength gains can be achieved by older adults following resistance training programmes. Strength gains can be attributed to neural, muscular and tendinous factors. Agonist muscle neural drive increases, whilst the co-activation of antagonist muscles remains unchanged after training. The muscular adaptations to resistance training include enlargement of gross muscle area and increases in fascicle lengths and pennation angles. The adaptations to training are not limited to the muscular system as tendon stiffness increases after resistance training. In conclusion, the musculoskeletal system retains its capacity for adaptation into old age and many of the musculoskeletal

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factors characterizing ageing can be at least partially mitigated by resistance training. The support received from Technogym and funding provided by the Italian Space Agency is acknowledged.

References Brown AB, McCartney N, Sale DG. Positive adaptations to weightlifting training in the elderly. Journal of Applied Physiology 1990;69(5):1725–33. Buchanan CI, Marsh RL. Effects of long-term exercise on the biomechanical properties of the Achilles tendon of guinea fowl. Journal of Applied Physiology 2001;90(1):164–71. Butler DL, Grood ES, Noyes FR, Zernicke RF. Biomechanics of ligaments and tendons. Exercise and Sport Sciences Reviews 1978; 6:125–81. Cook CS, McDonagh MJ. Force responses to controlled stretches of electrically stimulated human muscle-tendon complex. Experimental Physiology 1995;80(3):477–90. Ferri A, Scaglioni G, Pousson M, Capodaglio P, Van Hoecke J, Narici MV. Strength and power changes of the human plantar flexors and knee extensors in response to resistance training in old age. Acta Physiologica Scandinavica 2003;177(1):69–78. Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ. High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 1990;263(22):3029–34. Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. Journal of Applied Physiology 2000;88(4):1321–6. Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Malkia E, et al. Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. Journal of Applied Physiology 1998;84(4):1341–9. Hakkinen K, Kraemer WJ, Newton RU, Alen M. Changes in electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in middle-aged and older men and women. Acta Physiologica Scandinavica 2001;171(1):51–62. Harridge SD, Kryger A, Stensgaard A. Knee extensor strength, activation, and size in very elderly people following strength training. Muscle and Nerve 1999;22(7):831–9. Hortobagyi T, Zheng D, Weidner M, Lambert NJ, Westbrook S, Houmard JA. The influence of aging on muscle strength and muscle fiber characteristics with special reference to eccentric strength. Journals of Gerontology Series A—Biological Sciences and Medical Sciences 1995;50(6):B399–406. Klein CS, Rice CL, Marsh GD. Normalized force, activation, and coactivation in the arm muscles of young and old men. Journal of Applied Physiology 2001;91(3):1341–9. Lynch NA, Metter EJ, Lindle RS, Fozard JL, Tobin JD, Roy TA, et al. Muscle quality. I. Age-associated differences between arm and leg muscle groups. Journal of Applied Physiology 1999;86(1): 188–94. Macaluso A, De Vito G. Muscle strength, power and adaptations to resistance training in older people. European Journal of Applied Physiology 2004;91(4):450–72. Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De Vito G. Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle and Nerve 2002;25(6):858–63. Maganaris CN. In vivo tendon mechanical properties in young adults and healthy elderly. Active Life Span Research Symposium. The Plasticity of the Motor System: Adaptations to Increased Use,

ARTICLE IN PRESS 196

N.D. Reeves et al. / Manual Therapy 11 (2006) 192–196

Disuse and Ageing, Manchester Metropolitan University, UK; 2001. Morse CI, Thom JM, Davis MG, Fox KR, Birch KM, Narici MV. Reduced plantarflexor specific torque in the elderly is associated with a lower activation capacity. European Journal of Applied Physiology 2004;92(1-2):219–26. Narici MV, Maganaris CN, Reeves ND, Capodaglio P. Effect of aging on human muscle architecture. Journal of Applied Physiology 2003;95(6):2229–34. Noyes FR, Grood ES. The strength of the anterior cruciate ligament in humans and Rhesus monkeys. Journal of Bone and Joint Surgery of America 1976;58(8):1074–82. Phillips SK, Bruce SA, Woledge RC. In mice, the muscle weakness due to age is absent during stretching. Journal of Physiology (London) 1991;437:63–70. Rantanen T, Avela J. Leg extension power and walking speed in very old people living independently. Journals of Gerontology Series A—Biological Sciences and Medical Sciences 1997;52(4): M225–31. Reeves ND, Maganaris CN, Narici MV. Effect of strength training on human patella tendon mechanical properties of older individuals. Journal of Physiology (London) 2003;548(Part 3):971–81. Reeves ND, Narici MV, Maganaris CN. In vivo human muscle structure and function: adaptations to resistance training in old age. Experimental Physiology 2004a;89(6):675–89. Reeves ND, Narici MV, Maganaris CN. Effect of resistance training on skeletal muscle-specific force in elderly humans. Journal of Applied Physiology 2004b;96(3):885–92.

Reeves ND, Maganaris CN, Narici MV. Plasticity of dynamic muscle performance with strength training in elderly humans. Muscle and Nerve 2005;31(3):355–64. Roos MR, Rice CL, Connelly DM, Vandervoort AA. Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men. Muscle and Nerve 1999;22(8):1094–103. Skelton DA, Greig CA, Davies JM, Young A. Strength, power and related functional ability of healthy people aged 65–89 years. Age and Ageing 1994;23(5):371–7. Tkaczuk H. Tensile properties of human lumbar longitudinal ligaments. Acta Orthopaedica Scandinavica 1968;S115:1. Vandervoort AA, Kramer JF, Wharram ER. Eccentric knee strength of elderly females. ournal of Gerontology 1990;45(4):B125–8. Winegard KJ, Hicks AL, Sale DG, Vandervoort AA. A 12-year follow-up study of ankle muscle function in older adults. Journals of Gerontology Series A—Biological Sciences and Medical Sciences 1996;51(3):B202–7. Woo SL, Ritter MA, Amiel D, Sanders TM, Gomez MA, Kuei SC, et al. The biomechanical and biochemical properties of swine tendons—long term effects of exercise on the digital extensors. Connective Tissue Research 1980;7(3):177–83. Woo SL, Gomez MA, Amiel D, Ritter MA, Gelberman RH, Akeson WH. The effects of exercise on the biomechanical and biochemical properties of swine digital flexor tendons. Journal of Biomechanical Engineering 1981;103(1):51–6. Woo SL, Gomez MA, Woo YK, Akeson WH. Mechanical properties of tendons and ligaments. II. The relationships of immobilization and exercise on tissue remodeling. Biorheology 1982;19(3):397–408.

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Original article

Sensorimotor contribution to shoulder stability: Effect of injury and rehabilitation$ Joseph B. Myers, Craig A. Wassinger, Scott M. Lephart Department of Sports Medicine and Nutrition, Neuromuscular Research Laboratory, School of Health and Rehabilitation Sciences, UPMC Center for Sports Medicine, University of Pittsburgh, 3200 South Water Street, Pittsburgh, PA 15203, USA Received 27 October 2005; accepted 6 April 2006

Abstract Shoulder joint stability is the humeral head remaining or promptly returning to proper alignment within the glenoid fossa. This is mediated by both mechanical and dynamic restraint mechanisms. Coordination of these restraint systems is required for shoulder joint stability. The sensorimotor system is defined as all of the sensory, motor, and central integration and processing components involved in maintaining joint stability. The sensorimotor system is comprised of several components including proprioception, joint position sense, kinesthesia, sensation of force, and neuromuscular control. With joint injury, not only are the mechanical restraints disrupted (joint capsule, glenoid labrum, etc.) but also, the sensorimotor system is affected. Restoration of the sensorimotor system has been shown to occur through both surgical and conservative intervention and rehabilitation. Surgery has been shown to restore both mechanical restraints and the sensorimotor system. Specific rehabilitation techniques have also been effective at improving the sensorimotor system in healthy and pathological patients. r 2006 Elsevier Ltd. All rights reserved. Keywords: Proprioception; Neuromuscular control; Joint stability

1. Introduction Stability is defined as the state of remaining unchanged, even in the presence of forces that would normally change the state or condition (Thomas, 1993). Applying this definition to the shoulder, glenohumeral stability is the state of the humeral head remaining or promptly returning to proper alignment within the glenoid fossa through an equalization of forces. Joint stability is mediated by both mechanical and dynamic restraints. Mechanical restraints include the glenohumeral joint capsule, glenohumeral and extracapsular ligaments, glenoid labrum, bony geometry and intraarticular pressure. Dynamic restraint results from

activation and force production by the muscles surrounding the shoulder. Functional joint stability is defined as possessing adequate stability to perform functional activity and results from the interaction between the mechanical and dynamic restraints mentioned above (Lephart et al., 2000). As separate entities, neither the mechanical nor dynamic restraints can act alone in providing functional joint stability, but requires a mechanical-dynamic restraint interaction to achieve a stable shoulder. This mechanical-dynamic restraint interaction is mediated by the sensorimotor system.

2. Sensorimotor system $ Presented at: 2nd International Conference on Movement Dysfunction, pain, and performance: Evidence and effect. Corresponding author. Tel.: 412 432 3800; fax: 412 432 3801. E-mail address: [email protected] (J.B. Myers).

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The sensorimotor system is defined as all of the sensory, motor, and central integration and processing components involved in maintaining joint stability

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(Riemann and Lephart, 2002a, b). For example, the mechanical restraints about the shoulder not only provide physical restraint to the humeral head, but also contribute to stability by providing neural feedback (proprioception) to the central nervous system (CNS) where it is integrated with other somatosensory, vestibular, and visual input, and ultimately results in the generation of efferent control over the dynamic restraints about the shoulder joint (neuromuscular control). Proprioception is defined as the afferent information, arising from peripheral areas of the body (including the mechanical and dynamic restraints about the shoulder) that contributes to joint stability, postural control, and motor control (Lephart et al., 2000; Riemann and Lephart, 2002a, b). Proprioception has three submodalities including joint position sense, kinesthesia, and sensation of force (Riemann and Lephart, 2002a, b). Joint position sense is the appreciation and interpretation of information concerning one’s joint position and orientation in space. Kinesthesia is the ability to appreciate and interpret joint motions (Myers and Lephart, 2000). Sensation of force is the ability to appreciate and interpret force applied to or generated within a joint (Myers and Lephart, 2000). Proprioceptive information originates at the level of the mechanoreceptor. Mechanoreceptors are peripheral afferent sensory neurons present within muscle, tendons, fascia, joint capsule, ligaments, and skin about a joint (Kikuchi, 1968; Grigg, 1994; Vangsness et al., 1995). Mechanoreceptors are mechanically sensitive receptors that transduce mechanical tissue deformation as frequency modulated neural signals to the central nervous system (CNS) through afferent sensory pathways (Grigg, 1994). Mechanoreceptors including pacinian corpuscles, ruffini endings, golgi tendon organs, and muscle spindles have been identified at the shoulder (Vangsness et al., 1995; Solomonow et al., 1996; Gohlke et al., 1996; Ide et al., 1996; Gohlke et al., 1998). Neuromuscular control is the subconscious activation of the dynamic restraints about the shoulder in preparation and in response to joint motion and loading for the purpose of maintaining joint stability (Myers and Lephart, 2000). These neuromuscular control mechanisms include coordinated muscle activation during functional tasks, coactivation of the shoulder musculature (force coupling), muscular reflexes, and regulation of muscle tone and stiffness (Myers and Lephart, 2000, 2002). The forces provided by the muscles about the shoulder maintain centralization of the humeral head within the glenoid while still allowing for a high degree of mobility.

3. The effects of injury on the sensorimotor system Injury to the stabilizing structures of the shoulder (capsuloligamentous, articular, and musculotendinous)

whether caused by a traumatic or atraumatic mechanism, results in mechanical instability. Accompanying physical disruption of the mechanical stabilizers is decreased capsuloligamentous-musculotendinous mechanoreceptor stimulation thus altering the sensorimotor contribution to dynamic restraint and joint stability (Lephart and Henry, 1996). This combination of mechanical deficits and sensorimotor alterations contribute to deficits in functional stability (Lephart and Henry, 1996). Ultimately, the deficient function may contribute to reinjury patterns often seen at the shoulder joint. For example, with an acute glenohumeral dislocation-subluxation, the mechanical restraints including glenohumeral joint capsule, glenohumeral ligaments, and glenoid labrum are compromised. Yet within those structures are mechanoreceptors that contribute proprioeceptive information to the sensorimotor system that ultimately provides neuromuscular control over the dynamic restraints about the shoulder. Thus with joint injury, not only are the mechanical restraints affected, but also the sensorimotor contribution to dynamic stability is affected. Several studies have shown that instability at the shoulder has deleterious effects on proprioception (Smith and Brunolli, 1989; Lephart et al., 1994; Zuckerman et al., 2003; Barden et al., 2004). Both joint position sense and kinesthesia are altered in patients diagnosed with glenohumeral instability (Smith and Brunolli, 1989; Lephart et al., 1994; Zuckerman et al., 2003; Barden et al., 2004). Accompanying the disruption of the mechanical stabilizing structures, it is believed that decreased capsuloligamentous mechanoreceptor stimulation resulting from tissue deafferentation and/ or the increased tissue laxity limiting mechanoreceptors stimulation, thus decreasing proprioception (Lephart and Henry, 1996; Tibone et al., 1997). Barden et al. (2004) demonstrated errors bilaterally in joint position sense in subjects exhibiting unilateral instability. These results suggest that alterations in the central processing mechanisms may also be present. Interestingly, Tibone et al. (1997) reported that no significant differences existed between normal subjects and subjects with instability, using cortical evoked potential. Given that joint capsule mechanoreceptors were stimulated with electrical potentials rather then tissue deformation, these results suggest that capsular laxity alone rather than mechanoreceptor trauma resulting in deafferentation is responsible for proprioception deficits. Proprioceptive deficits have also been identified in patients diagnosed with osteoarthritis (Cuomo et al., 2005). Proprioceptive deficits were attributed to decreases in shoulder muscle activity levels combined with local muscle atrophy (Cuomo et al., 2005). Additionally, the increased afferent signals sent by pain receptors about the shoulder were believed to override and subsequently decrease proprioception afferents. The

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work by Safran et al. (2001) supports the role of pain in adversely affecting proprioception. These results demonstrated that throwers with shoulder pain have decreased proprioception most likely due to increased nociceptor activity in the painful shoulder of baseball players Safran et al. (2001). Subacromial impingement has also been linked to proprioceptive deficits. Machner et al. (2003) demonstrated decreased kinesthesia in subjects diagnosed with unilateral stage II subacromial impingement. The authors theorized that the subacromial bursa was deficient in relaying the movement sense signals (Machner et al., 2003). Given the proprioceptive deficits associated with shoulder joint injury, neuromuscular control is hypothesized to be altered as well (Myers and Lephart, 2000, 2002). Several investigators have assessed the neuromuscular control component of dynamic joint stability in subjects presenting with glenohumeral instability (Glousman et al., 1988; Kronberg et al., 1991; McMahon et al., 1996; Myers et al., 2004). Muscle activation alterations were identified in patients with glenohumeral instability during both simple elevation tasks (Kronberg et al., 1991; McMahon et al., 1996) and while throwing a baseball (Glousman et al., 1988). Deficits in coactivation of the rotator cuff and primary humeral movers were present, possibly leading to compromised dynamic joint stability and further exacerbating the existing instability. Our laboratory recently assessed reflexive characteristics of the shoulder muscles in patients diagnosed with anterior glenohumeral instability (Myers et al., 2004). The patients with instability demonstrated suppressed pectoralis major and biceps brachii mean reflexive activation, significantly slower biceps brachii reflex latency, and suppressed supraspinatus-subscapularis coactivation. The results suggested that in addition to the capsuloligamentous deficiency and proprioceptive deficits present in patients with anterior glenohumeral instability, muscle activation alterations are also present. The suppressed rotator cuff coactivation, slower biceps brachii activation, and decreased pectoralis major and biceps brachii mean activation may contribute to the recurrent instability episodes seen in patients with glenohumeral instability. Muscle activation abnormalities associated with subacromial impingement and rotator cuff lesions have also been identified (Ludewig and Cook, 2000; Reddy et al., 2000; Kelly et al., 2005). Common findings include increased activity in the middle deltoid, decreased activity in the supraspinatus, infraspinatus, and subscapularis, decreased coactivation of the rotator cuff musculature, and suppressed scapular stabilization by the trapezius and serratus anterior muscles during elevation. Kelly et al. (2005) assessed activation of the rotator cuff during functional tasks and demonstrated that patients with symptomatic rotator cuff tears exhibit activation alterations that may limit functional perfor-

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mance compared to both asymptomatic and normal subjects. Our laboratory recently identified that patients with subacromial impingement exhibited less subscapularis-infraspinatus, supraspinatus-subscapularis, and supraspinatus-infraspinatus coactivation (Myers et al., 2003). Increased middle deltoid and latissimus dorsi activity was exhibited by the impingement patients. The results indicate that patients with subacromial impingement exhibit suppressed rotator cuff coactivation and abnormal humeral mover alterations during humeral elevation. These demonstrated muscle activation alterations may contribute to impingement of the subacromial structures and subsequent pain during overhead elevation in patients with subacromial impingement.

4. Sensorimotor restoration There is evidence to suggest that the sensorimotor contributors to joint stability can be restored. For example, surgical intervention to restore mechanical stability has a demonstrated benefit in restoring proprioception (Lephart et al., 1994, 2002; Zuckerman et al., 2003; Potzl et al., 2004; Cuomo et al., 2005). The main goal of surgery for glenohumeral instability is to reestablish mechanical restraint to the humeral head. Yet as reported by several investigators, the surgery was also successful at restoring proprioception (Lephart et al., 1994, 2002; Zuckerman et al., 2003; Potzl et al., 2004; Cuomo et al., 2005). It is believed that by reestablishing tension with the glenohumeral joint capsule and ligaments, that mechanoreceptor stimulation is also reestablished (Lephart et al., 1994, 2002; Zuckerman et al., 2003; Potzl et al., 2004; Cuomo et al., 2005). Mechanoreceptors may also repopulate the joint capsule allowing reinnervation following surgery as a normal part of the histological healing process (Lephart et al., 1994, 2002). Potzl et al. (2004) found an increase in proprioception bilaterally following unilateral surgical intervention, thus hypothesizing an alteration in central mediation of proprioception may also contribute to normalization of proprioception. Subacromial decompression was also found to restore proprioception in patients with subacromial impingement (Machner et al., 2003). It was suggested that the painful subacromial bursa (and subsequent resection) was the cause for the initial deficit and subsequent restoration of proprioception. These results are supported by Cuomo et al. (2005) who found that both measures of kinesthesia and joint position sense returned to normal levels following total shoulder arthroplasty (Cuomo et al., 2005). It was suggested that a decrease in pain afferents with greater mechanoreceptor afferent activity following surgery was the mechanism for improved proprioception (Machner et al., 2003; Cuomo et al., 2005). Other potential mechanisms for

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restoration of proprioception following surgery included retensioning of the joint capsule and surrounding musculature, and restoration of anatomical alignment through greater joint congruence following arthroplasty (Cuomo et al., 2005). As with any injury, rehabilitation should address inflammation and pain reduction, a return to normal range of motion and flexibility, and restoration of strength through traditional rehabilitation exercises. Yet return to vigorous physical activity and athletic participation requires additional rehabilitation considerations. Lephart and Henry (1995) promote the use of functional rehabilitation for return to athletic and highly demanding activities of daily living (Lephart and Henry, 1996). A large component of functional rehabilitation is the ability to replicate the demands placed on the joint in a controlled manner to decrease the initial impact upon return to physical activity. Some of the expected benefits of functional rehabilitation include increasing proprioceptive awareness, increasing dynamic stabilization, eliciting preparatory and reactive muscle activation, and restoration of functional movement patterns (Lephart and Henry, 1996). Proprioceptive awareness training ins believed to reestablish afferent pathways from the mechanoreceptors a to the central nervous system, and facilitate supplementary afferent pathways as a compensatory mechanism for proprioceptive deficits that resulted from joint injury (Myers and Lephart, 2000). Dynamic stabilization is paramount in restoring functional joint stability and should focus on restoring both coordinated muscle activation patterns during functional tasks as well as muscle coactivation and the resulting force coupling restraint. Elicitation of preparatory and reactive muscle activation around the shoulder helps to establish reflex loops and muscle stiffness around the joint thus creating stability during destabilizing events. To further ease the transition from rehabilitation to the functional demands of sports or occupation, allowing controlled simulation of tasks is beneficial. Recreating the activities which will be required of the joint during sports in the clinical setting allows a controlled environment to practice and evaluate techniques prior to actual specific performance. There is some evidence of the effectiveness of exercise in restoring sensorimotor mechanisms at the shoulder. Shoulder plyometric training has been shown to increase proprioception in swimmers (Swanik et al., 2002). It was theorized that repeated eccentric loading and subsequent length/tension changes in the shoulder stabilizers at end-range of motion, created increased proprioceptive awareness of by both the mechanical and dynamic stabilizers (Swanik et al., 2002). Additionally, increases in central processing may have resulted from performing the repeating, perturbing plyometric tasks. This creates increased muscle tension in preparation to the task being performed, which may have increased awareness of joint

position (Swanik et al., 2002). Furthermore, both open and closed kinetic chain exercises have been shown to causes improvements in joint position sense at the shoulder (Rogol et al., 1998). It has also been shown that closed kinetic chain upper extremity activities facilitates co-coactivation of the muscles around the shoulder, increasing functional joint stability (Ubinger et al., 1999; Henry et al., 2001). By utilizing closed chain exercises, an increase in joint stability can be obtained by creating greater joint congruency and stimulation of articular mechanoreceptors (Ubinger et al., 1999; Henry et al., 2001). There also appears to be a central component trained during closed chain exercise, as increases were in both shoulders in subjects training unilaterally (Ubinger et al., 1999). It has also been shown through a randomized controlled trial that enhancing neuromuscular control through exercises designed to enhance coactivation about the shoulder leads to faster recovery of chronic shoulder pain than natural course of recovery (Ginn and Cohen, 2005). It was also shown to be equivalent in recovery time as steroid injection and physical modalities. The authors advocate retraining as it is more cost effective than modalities and has less inherent risk than injection (Ginn and Cohen, 2005).

5. Summary Functional joint stability results from a coordination of both mechanical restraints (provided by capsuloligamentous, articular, and musculotendinous structures) and dynamic restraints that result from contraction of the musculature that surrounds the joint. Acting independently, neither the mechanical nor dynamic restraints alone can provide joint stability. There must be coordination between the mechanical and dynamic restraints. The coordination between the mechanical and dynamic restraints is mediated by the sensorimotor system. The sensorimotor system includes the sensory, motor, and central integration/processing components of the central nervous system that contribute to joint stability. Sensory information provided by the joint (proprioception) travels through afferent pathways to the central nervous system, where it is integrated with information from other levels of the nervous system. The central nervous system, in turn, elicits efferent motor responses (neuromuscular control) vital to coordinated movement patterns and functional stability. With joint injury, not only are the mechanical restraints disrupted (instability, lesion, etc.) but also, the sensorimotor system is affected. Demonstrated deficits in both proprioception and neuromuscular control accompany joint injury. Both surgical intervention and rehabilitation have been demonstrated to restore not only the

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mechanical restraints that are disrupted with injury, but also the sensorimotor contributors to joint stability.

References Barden JM, Balyk R, Raso VJ, Moreau M, Bagnall K. Dynamic upper limb proprioception in multidirectional shoulder instability. Clinical Orthopaedics and Related Research 2004(420):181–9. Cuomo F, Birdzell MG, Zuckerman JD. The effect of degenerative arthritis and prosthetic arthroplasty on shoulder proprioception. Journal of Shoulder and Elbow Surgery 2005;14(4):345–8. Ginn KA, Cohen ML. Exercise therapy for shoulder pain aimed at restoring neuromuscular control: a randomized comparative clinical trial. Journal of Rehabilitation Medicine 2005;37(2): 115–22. Glousman R, Jobe F, Tibone J, Moynes D, Antonelli D, Perry J. Dynamic electromyographic analysis of the throwing shoulder with glenohumeral instability. Journal of Bone and Joint Surgery of America 1988;70(2):220–6. Gohlke F, Janssen E, Leidel J, Eulert J. Histopathological findings in the proprioception of the shoulder joint. Orthopade 1998;27(8): 510–7. Gohlke F, Muller T, Sokeland T, Schmitz F, Messllinger K. Distribution and morphology of mechanoreceptors in the rotator cuff. Journal of Shoulder and Elbow Surgery 1996;5(Supp):S72. Grigg P. Peripheral neural mechanism in proprioception. Journal of Sport Rehabilitation 1994;3:2–17. Henry TJ, Lephart SM, Giraldo J, Stone D, Fu FH. The effect of muscle fatigue on muscle force-couple activation of the shoulder. Journal of Sport Rehabilitation 2001;10(4):246–56. Ide K, Shirai Y, Ito H. Sensory nerve supply in the human subacromial bursa. Journal of Shoulder and Elbow Surgery 1996;5(5):371–82. Kelly BT, Williams RJ, Cordasco FA, Backus SI, Otis JC, Weiland DE, Altchek DW, Craig EV, Wickiewicz TL, Warren RF. Differential patterns of muscle activation in patients with symptomatic and asymptomatic rotator cuff tears. Journal of Shoulder and Elbow Surgery 2005;14(2):165–71. Kikuchi T. Histological studies on the sensory innervation of the shoulder joint. Journal of the Iwate Medical Association 1968;20: 554–67. Kronberg M, Brostrom LA, Nemeth G. Differences in shoulder muscle activity between patients with generalized joint laxity and normal controls. Clinical Orthopaedics 1991;269:181–92. Lephart SM, Henry TJ. Functional rehabilitation for the upper and lower extremity. Ortho Clin N Am 1995;26(3):579–92. Lephart SM, Henry TJ. The physiological basis for open and closed kinetic chain rehabilitation for the upper extremity. J Sport Rehab 1996;5:71–87. Lephart SM, Warner JP, Borsa PA, Fu FH. Proprioception of the shoulder joint in healthy, unstable, and surgically repaired shoulders. Journal of Shoulder and Elbow Surgery 1994;3(6): 371–80. Lephart SM, Riemann BL, Fu F. Introduction to the sensorimotor system. In: Lephart SM, Fu FH, editors. Proprioception and Neuromuscular Control in Joint Stability. Champaign: Human Kinetics; 2000. p. xvii–xiv. Lephart SM, Myers JB, Bradley JP, Fu FH. Shoulder proprioception and function following thermal capsulorraphy. Arthroscopy 2002;18(7):770–8. Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther 2000;80(3):276–91.

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Machner A, Merk H, Becker R, Rohkohl K, Wissel H, Pap G. Kinesthetic sense of the shoulder in patients with impingement syndrome. Acta Orthop Scand 2003;74(1):85–8. McMahon PJ, Jobe FW, Pink MM, Brault JR, Perry J. Comparative electromyographic analysis of shoulder muscles during planar motions: anterior glenohumeral instability versus normal. Journal of Shoulder and Elbow Surgery 1996;5(2 Pt 1):118–23. Myers JB, Lephart SM. The role of the sensorimotor system in the athletic shoulder. Journal of Athletic Training 2000;35(3):351–63. Myers JB, Hwang JH, Pasquale MR, Rodosky MW, Ju YY, Lephart SM. Shoulder muscle coactivation alterations in patients with subacromial impingement. Paper presented at: 2003 American College of Sports Medicine Annual Meeting, 2003, San Francisco, CA. Myers JB, Ju YY, Hwang JH, McMahon PJ, Rodosky MW, Lephart SM. Reflexive muscle activation alterations in shoulders with anterior glenohumeral instability. American Journal of Sports Medicine 2004;32(4):1013–21. Myers JB, Lephart SM. Sensorimotor deficits contributing to glenohumeral instability. Clinical Orthopaedics 2002(400):98–104. Potzl W, Thorwesten L, Gotze C, Garmann S, Steinbeck J. Proprioception of the shoulder joint after surgical repair for Instability: a long-term follow-up study. American Journal of Sports Medicine 2004;32(2):425–30. Reddy AS, Mohr KJ, Pink MM, Jobe FW. Electromyographic analysis of the deltoid and rotator cuff muscles in persons with subacromial impingement. Journal of Shoulder and Elbow Surgery 2000;9(6):519–23. Riemann BL, Lephart SM. The sensorimotor system, part 1: the physiological basis of functional joint stability. Journal of of Athletic Training 2002a;37(1):71–7. Riemann BL, Lephart SM. The sensorimotor system, part 2: the role of proprioception in motor control and functional joint stability. Journal of Athletic Training 2002b;37(1):80–4. Rogol IM, Ernst GP, Perrin DH. Open and closed kinetic chain exercises improve shoulder joint reposition sense equally in healthly subjects. Journal of Athletic Training 1998;33(4):315–8. Safran MR, Borsa PA, Lephart SM, Fu FH, Warner JJ. Shoulder proprioception in baseball pitchers. Journal of Shoulder and Elbow Surgery 2001;10(5):438–44. Smith RL, Brunolli J. Shoulder kinesthesia after anterior glenohumeral dislocation. Physical Thererapy 1989;69:106–12. Solomonow M, Guanche CA, Wink CA, Knatt T, Barratta RM, Lu Y. Shoulder capsule reflex arc in the feline shoulder. Journal of Shoulder and Elbow Surgery 1996;5:139–46. Swanik KA, Lephart SM, Swanik CB, Lephart SP, Stone DA, Fu FH. The effects of shoulder plyometric training on proprioception and selected muscle performance characteristics. Journal of Shoulder and Elbow Surgery 2002;11(6):579–86. Thomas C. Taber’s cyclopedic medical dictionary. Philadelphia: FA Davis Company; 1993. Tibone JE, Fechter J, Kao JT. Evaluation of a proprioception pathway in patients with stable and unstable shoulders with cortical evoked potentials. Journal of Shoulder and Elbow Surgery 1997;6(5): 440–3. Ubinger ME, Prentice WE, Guskiewicz KM. Effects of closed kinetic chain training on neuromuscular control in the upper extremity. Journal of Sport Rehabilitation 1999;8(3):184–94. Vangsness CT, Ennis M, Taylor JG, Atkinson R. Neural anatomy of the glenohumeral ligaments, labrum, and subacromial bursa. Arthroscopy 1995;11(2):180–4. Zuckerman JD, Gallagher MA, Cuomo F, Rokito A. The effect of instability and subsequent anterior shoulder repair on proprioceptive ability. Journal of Shoulder and Elbow Surgery 2003;12(2): 105–9.

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Original Article

Lumbar spine reposition sense: The effect of a ‘slouched’ posture Katherine J. Dolan, Ann Green Department of Physiotherapy, Faculty of Health and Life Sciences, Coventry University, Priory Street, Coventry CV1 5FB, UK Received 27 October 2005; received in revised form 14 February 2006; accepted 2 March 2006

Abstract Proprioceptive control is considered important for spinal stability and prevention of injury. However there is evidence that proprioceptive structures, that are reflexive and viscoelastic, are challenged by commonly adopted ‘slouched’ postures. The aim of this study was to investigate the effect of such postures on proprioceptive control. The reliability of a flexible electrogoniometer was established (ICC ¼ 0.89). Using a repeated measures design (n ¼ 32, 80% power detecting 0.51 difference at 95% significance) subjects repositioned their lumbar spine immediately (3 s) and following 300 s in a ‘slouched’ posture, with a 15-min interval in between. Results showed a significantly reduced lumbar spine reposition sense following 300 s in a ‘slouched’ posture as compared with 3 s in a ‘slouched’ posture ðPo0:001Þ, mean difference 3.921 (SD 4.35). Based on this sample, there was evidence that a ‘slouched’ posture, of 5 min duration, would increase reposition error by more than 2.351 and less than 5.481 (n ¼ 32, CI 95%). These findings support the practice of postural education to reduce potential to proprioceptive loss and injury. The electrogoniometer shows potential for use in clinical practice. r 2006 Elsevier Ltd. All rights reserved. Keywords: Reposition sense; Lumbar spine; Proprioception; Posture

1. Introduction Low back pain is considered to be a major clinical and public health problem in the UK (CSAG, 1994; Waddell, 1998). It is described as having reached epidemic proportions in most western industrialized countries with 60–80% of all adults suffering from low back pain at some point during their lives (Waddell, 1998). A survey by CSAG in 1993 reported that 52 million working days were lost due to back pain in the UK (CSAG, 1994). It has been suggested that a slouched posture is one factor that may contribute to low back pain (Dolan et al., 1988; Kendall et al., 1993). A slouched or flexed posture commonly occurs in dayto-day sitting activities and is defined as a relaxed sitting posture with a flexed lumbar spine (Dolan et al., 1988; Kendall et al., 1993). In this posture, the neutral

Corresponding author. Tel.: +44 2476 888561.

E-mail address: [email protected] (K.J. Dolan). 1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.03.003

position is lost and the spine is potentially exposed to injury (Panjabi, 1992a, b). Panjabi (1992a, b) has identified a ‘neutral zone’ described as a few degrees of spinal movement that is controlled by proprioceptive neuromuscular reflexes. A possible link between slouched postures and predisposition to low back pain is the loss of neutral zone control due to loss of proprioceptive reflexes. Loss of neutral zone control has been associated with degenerative changes (Panjabi and Goel, 1982) and linked with pain symptoms (Panjabi, 2003) and loss of proprioceptive control has been associated with low back pain populations (Gill and Callaghan, 1998; Koumantakis et al., 2002; O’Sullivan et al., 2003). There is evidence that reflexive activity of proprioceptive structures and viscoelastic properties of spinal tissues are challenged by stretch or by flexed postures (McGill and Brown, 1992; Adams and Dolan, 1996; Solomonow et al., 2001). Reflexive muscle activity has been found to be reduced by application of a stretch to spinal ligaments (Solomonow et al., 2001), and in looking at in vivo cat spines

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they found that a 10 s stretch applied to the supraspinous ligament reduced multifidus activity by 50%. In humans there is evidence of a direct link between lumbar muscle activity and proprioceptive control (Brumagne et al., 1999b) and evidence of rapid viscoelastic changes in ligaments and other spinal tissues in response to stretch (McGill and Brown, 1992; Adams and Dolan, 1996). Examining cadaveric spines, Adams and Dolan (1996) found a 42% change in ligament tension in response to a 5-min stretch and McGill and Brown (1992) identified a creep response of a 51 increase in flexion when maintaining a slouched posture for 20 min. If individuals spend time in flexed postures, the implication is that their spinal proprioceptive neuromuscular reflexes will be affected. Physiotherapy advocates postural awareness and re-education, and for a modern lifestyle where there is a tendency towards flexed postures, the ability to reposition after a period of time in flexion is important for prevention of low back pain and injury. The aim of this study was to evaluate the effect of prolonged ‘slouched’ posture on lumbar spine reposition sense compared to immediate reposition sense in asymptomatic subjects. It was hypothesized that the accuracy of lumbar spine repositioning would be reduced in those subjects that sat in a prolonged ‘slouched’ posture compared to those that did not.

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2.3. Inclusion and exclusion criteria The inclusion criterion was an age range of 18–40 years (Kaplan et al., 1985; Parkhurst and Burnett, 1994). Exclusion criteria was a previous history of low back pain and/or back surgery (Brumagne et al., 1999a), current or recent ear infection or vestibular disorder (McCloskey, 1978; Brumagne et al., 1999a) and previous hip pain or injury (Brumagne et al., 1999a; O’Sullivan et al., 2003). Ethical approval was obtained and participants received information sheets and gave informed consent. 2.4. Measurement Lumbar spine reposition sense was measured using a flexible M180B electrogoniometer (Biometrics Ltd., UK) connected to a dual channel data logger (Biometrics DL1001). Results were uploaded onto an IBMcompatible computer using Biometrics DL1001 Version 3.2 software. Subjects sat on the end of the plinth, hips and knees at approximately 901, facing a blank wall 1 m away. Two electrodes were placed at L1 and S1, as recommended by Biometrics (2002). The ‘upright’ starting posture was aligned, by the researcher, as the anterior and posterior superior iliac spines being level in the horizontal plane (Maffrey-Ward et al., 1996). 2.5. Procedure

2. Methods 2.1. Design A repeated measures design was used to determine the effect of ‘slouched’ posture on reposition sense. The order of testing was randomly allocated to either repositioning after 3 s slouch or after 300 s slouch. Lumbar spine position was measured with an electrogoniometer that stored the data. The researcher was blind to the results since the data was not displayed during data collection. All measurements were taken on one occasion to reduce error. The outcome measure was reposition error as a measure of proprioception (McCloskey, 1978).

2.2. Sample A convenience sample of 32 was selected based upon a power calculation (P40:05, 80% power, Sim and Wright, 2000) for clinical significance with a detectable difference of 0.51. The sample included 12 males and 20 females with a mean age of 22.66 (SD 5.16) and body mass index 25.68 (SD 3.23).

The subject was requested to ‘sit in an upright posture’ by the researcher. Prior to each test, ten practice repetitions of repositioning to ‘upright’ posture were performed with the researcher providing manual facilitation and verbal feedback. For each reposition test the subject was asked firstly either to ‘slouch and return immediately to your upright posture’ (3 s, test 1) or requested to ‘slouch and return to your upright posture when instructed’ (300 s, test 2) depending on randomized order of testing (Figs. 1 and 2). A rest period of 15 min between tests allowed for tissue recovery (McGill and Brown, 1992). 2.6. Reliability The reliability study was to determine the extent that the measures were repeatable for serial measurements. The time period or placing of the electrogoniometer were not considered to be a potential source of error as the electrogoniometer remained in position throughout. Stability was determined for a single investigator collecting data from the same individuals. Intra-rater reliability of reposition measurement was calculated from the first 18 subjects (80% power to detect intraclass correlation coefficient (ICC) 0.7–0.9 at 95% significance, Walter et al., 1998) from the planned study

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sample who were tested according to the above protocol using only 3 s (test 1).Two measurements were taken at the proposed 15-min interval. During the rest period the subject was allowed to get up and move freely around the room. 2.7. Data analysis

Fig. 1. Measurement of upright posture.

Analyses were undertaken using the Statistical Package for the Social Sciences (SPSS version 10) and all statistical tests were performed at the 5% significance level. All data were considered interval in nature and the Kolmogorov–Smirnov goodness-of-fit test was used to confirm the presence of a normal distribution for both the reliability data and the main experiment data ðP40:05Þ. Descriptive data including means, standard deviations and ranges of measurement were calculated. Data were depicted using box plots and a related twotailed t-test was performed to determine whether reposition sense varied significantly between 3 and 300 s slouch. Intra-rater reliability was determined by ICC and complemented by Bland and Altman’s 95% limits of agreement test comparing mean of two measurements with the difference between them (Bland and Altman, 1986).

3. Results

Fig. 2. Measurement of ‘slouched’ posture.

The flexible electrogoniometer showed good reliability with ICC (2,1) ¼ 0.89 and confidence intervals of 0.74–0.99 (n ¼ 18, 95%CI) (Portney and Watkins, 1993). This was confirmed by Bland and Altman’s 95% limits of agreement indicating a small bias between measurements of 0.221 (SD 0.58), and limits of agreement of
0.941 to +1.381 (within dashed lines, Fig. 3). Based on this sample, the mean difference between

Difference in Reposition Error (degrees)

1.5

Mean + 2SD

1.0

0.5 Mean 0.0

-0.5 Mean - 2SD -1.0 -3

-2

-1 0 1 Mean Reposition Error (degrees)

2

3

Fig. 3. Scatterplot showing difference against mean for reliability of reposition error measurements (Bland and Altman, 1986).

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repeated measurements would lie between
0.081 and +0.521 (n ¼ 18, 95% CI). The difference in reposition error between test 1 and test 2 is demonstrated by box plots in Fig. 4. There was greater variability in reposition error in test 2 than in test 1, indicated in the spread of interquartile ranges and whiskers of the box plots and by the wide range of reposition values (Table 1). The box plots indicate that 75% of subjects undershot the target position into relative flexion (negative values, Table 1). When asked to adopt a ‘slouched’ posture, all subjects flexed their lumbar spine by a variable amount, mean flexion ¼ 13.711 (SD 11.30). A related t-test showed a statistically significant difference between test 1 reposition error (–0.21, SD 0.83) and test 2 reposition error (
4.121, SD 4.20), t ¼ 5:09, Po0:05, Tables 1 and 2. This indicates that lumbar spine reposition sense following prolonged ‘slouched’ posture was significantly reduced compared to immediate lumbar spine reposition sense. On the basis of this sample, there is evidence that in the population reposition error would increase by

Reposition Error (degrees)

10

0

-10

-20 Test 1

Test 2

Fig. 4. Box plots showing data dispersion and median values for reposition. Error in test 1 (3 s flexion)and test 2 (300 s flexion).

205

between 2.351 and 5.481 following a prolonged flexion of 5 min (n ¼ 32, 95% CI).

4. Discussion The results of this study indicated that lumbar spine reposition sense following prolonged ‘slouched’ posture was significantly different to immediate lumbar spine reposition sense. The subjects in this sample showed a significantly reduced lumbar spine repositioning accuracy following 300 s in ‘slouched’ posture as compared with 3 s ðPo0:001Þ, with a mean difference of 3.921 (SD 4.35). On the basis of this sample, there is evidence that prolonged ‘slouched’ posture for 5 min (300 s) would increase reposition error by between 2.351 and 5.481 (n ¼ 32, CI 95%). The effect of prolonged ‘slouched’ posture in reducing reposition sense accuracy has not been previously studied, but may be due to viscoelastic effects on soft tissues (McGill and Brown, 1992; Adams and Dolan, 1996) and alterations to proprioceptive neuromuscular reflexes (Brumagne et al., 1999b; Solomonow et al., 2001). Solomonow et al. (2001) found that if the flexionextension cycle of cat spines was increased from 1 to 10 s, the reflexive multifidus muscle activity was reduced by 50%. If the results of the present study are analysed in similar terms of flexion-extension cycles, then the flexion-extension cycle of test 1(3 s) could be described as 100 times faster than that of test 2 (300 s). The accurate immediate repositioning of test 1, 0.21 (SD 0.83), may therefore be due to reflexive muscle activity. Following prolonged ‘slouch’ the majority of subjects undershot the target position, by a mean of
4.211 (SD 4.20), this is similar to results of a study by Brumagne et al. (1999b) indicating that one effect of prolonged

Table 1 Summary of descriptive data for reposition error tests 1 and 2 Outcome variable

Mean (deg)

Standard deviation 95% confidence interval (deg) (deg) (SD) Lower Upper

Range Min, Max (deg)

Standard error of the mean (deg)

Test 1 (3 s) Test 2 (300 s)


0.20
4.12

0.83 4.20


2.07, 1.39
11.50, 3.20

0.15 0.74

0.09
2.60


.50
5.64

Table 2 Summary of T-test results for reposition error tests 1 and 2 Mean difference (deg)

RE1–RE2

3.92

Standard deviation t (deg)

4.35

5.09

df

31

Sig. (2-tailed)

0.000

95% confidence interval of the difference (deg) Lower

Upper

2.35

5.48

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‘slouched’ posture may have been to alter muscle spindle activity and therefore reduce reflexive muscle activity. The increased variability in reposition sense with prolonged ‘slouch’ may reflect the variation in load on proprioceptive structures indicated by the wide range of flexed postures adopted by the subjects, 13.711 (SD11.30). It may also indicate presence of individual differences in the levels of mechanoreceptor sensitivity, viscoelastic response, concentration and cognitive processes (Solomonow et al., 2001). The reliability study results (ICC (2,1) ¼ 0.89 and a bias of 0.221 (SD 0.58)) indicate that the effect would not be due to measurement error or individual differences. It is debatable whether the 2.35–5.481 (CI 95%, n ¼ 32) of reposition error identified by this study would challenge Panjabi’s neutral zone and compromise spinal stability. Panjabi identified the range of neutral zone movement to be 1–31 in a normal upright spine, approximately 20% of full range of lumbar spine movement. In this study, proprioceptive accuracy is reduced and therefore the neutral zone is challenged, although there may be fewer tendencies to compromise spinal stability where reposition sense error is less than 31. However, compromise of spinal stability may be greater with more prolonged loading in a ‘slouched’ posture or repetitive slouching that may occur during daily activities. Jackson et al. (2001) found 20 min stretch to in vivo cat spines inhibited muscle activity for 7 h. Similarly, repetitive flexion periods of 10 min have been shown to have a cumulative effect on muscle activity and soft tissues, also taking over 7 h to recover (Solomonow et al., 2003). Within physiotherapy practice, the ability to reposition to an upright posture is considered important for postural education (Kendall et al., 1993; Richardson et al., 1999). The results suggest that following education of an upright posture using 10 practice repetitions and verbal prompting, there was an immediate reposition sense accuracy of
0.501 to 0.091 (n ¼ 32,CI 95%) and that this accuracy was reduced within 5 min in a ‘slouched’ posture. Previous research indicates that this is likely to be due to the effects of soft tissues on reflexive activity. Additional teaching tools may be useful in enhancing reposition sense during day-to-day activities, e.g. visual input, cognitive input or use of an electrogoniometer as a feedback tool. The electrogoniometer, having been validated as a measure of joint kinematics against the VICON VX movement analysis system (Rowe et al., 2001), has demonstrated its ease of application and potential for use in physiotherapy practice as an accurate outcome measure for rehabilitation and postural education. Its reasonable reliability of mean difference 0.081 to +0.521 (n ¼ 18, 95% CI) makes it a potential reposition sense tool for detection of clinical differences of greater than 0.51. Previous studies have used the 3-space Fastrak to measure

reposition sense although reliability was not rigorously tested (Maffrey-Ward et al., 1996; Lam et al., 1999; O’Sullivan et al., 2003) and the cost and cumbersome set up may make its use prohibitive in the clinical environment. Before advocating the use of the electrogoniometer for reposition measurement in clinical practice, where there may be a transfer of the tool between sessions and between physiotherapists, interrater reliability with equipment removal between tests will need to be properly established.

5. Conclusion This study has shown that time spent in a ‘slouched’ lumbar spine posture challenges reposition sense. Findings support the use of postural education in promoting spinal proprioception. The electrogoniometer shows potential for use in clinical practice. Further research could provide information on ‘slouched’ postures as commonly adopted day-to-day postures and the proposed changes in proprioceptive muscle activity could be confirmed with fine wire electrodes. The significance of the results for prevention of low back pain is to some degree dependent on establishing a direct causal link between reposition sense loss and low back pain.

References Adams MA, Dolan P. Time dependent changes in the lumbar spine’s resistance to bending. Clinical Biomechanics 1996;11(4):194–200. Biometrics. Goniometer and torsiometer operating manual. Gwent, UK: Biometrics Ltd; 2002. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986;1: 307–10. Brumagne S, Lysens R, Spaepen A. Lumbosacral position sense during pelvic tilting in men and women without low back pain: test development and reliability assessment. Journal of Orthopaedic and Sports Physical Therapy 1999a;29(6):345–51. Brumagne S, Lysens R, Swinnen S, Verscheuren S. Effect of paraspinal muscle vibration on position sense of the lumbosacral spine. Spine 1999b;24(13):1328–31. CSAG. Clinical Standards Advisory Group, Report on back pain. London. UK: HMSO; 1994. Dolan P, Adams MA, Hutton WC. Commonly adopted postures and their effect on the lumbar spine. Spine 1988;13(2):197–201. Gill KP, Callaghan MJ. The measurement of lumbar proprioception in individuals with and without low back pain. Spine 1998;23(3): 371–7. Jackson M, Solomonow M, Zhou EE, Baratta RV, Harris M. Multifidus EMG and tension-relaxation recovery after prolonged static lumbar flexion. Spine 2001;26(7):715–23. Kaplan FS, Nixon JE, Reitz M, Rindfleish L, Tucker J. Age related changes in proprioception and sensation of joint position. Acta Orthopaedic Scandinavia 1985;56:72–4. Kendall FP, McCreary EK, Provance PG. Muscles: testing and function, 4th ed. London, UK: Williams and Wilkins; 1993. Koumantakis GA, Winstanley J, Oldham JA. Thoracolumbar proprioception in individuals with and without low back pain:

ARTICLE IN PRESS K.J. Dolan, A. Green / Manual Therapy 11 (2006) 202–207 intratester reliability, clinical applicability, and validity. Journal of Orthopaedic and Sports Physical Therapy 2002;32(7):327–35. Lam S, Jull G, Treleaven J. Lumbar spine kinesthesia in patients with low back pain. Journal of Orthopaedic and Sports Physical Therapy 1999;29(5):294–9. Maffrey-Ward L, Jull G, Wellington L. Toward a clinical test of lumbar spine kinesthesia. Journal of Orthopaedic and Sports Physical Therapy 1996;24(6):354–8. McCloskey DI. Kinesthetic sensibility. Physiological Review 1978;58: 763–820. McGill SM, Brown S. Creep response of the lumbar spine to prolonged full flexion. Clinical Biomechanics 1992;7:43–6. O’Sullivan PB, Burnett A, Floyd AN, Gadson K, Logiudice J, Miller D, Quike H. Lumbar repositioning deficit in a specific low back pain population. Spine 2003;28(10):1074–9. Panjabi MM. The stabilising system of the spine. Part 1. Function, dysfunction, adaptation, and enhancement. Journal of Spinal Disorders 1992a;5(4):383–9. Panjabi MM. The stabilising system of the spine. Part II. Neutral zone and instability hypothesis. Journal of Spinal Disorders 1992b;5(4):390–7. Panjabi MM. Clinical spinal instability and low back pain. Journal of Electromyographic Kinesiology 2003;13(4):371–9. Panjabi MM, Goel V. Relationship between chronic instability and disc degeneration. Toronto, Canada: International Society for the Study of the Lumbar Spine; 1982.

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Parkhurst TM, Burnett CN. Injury and proprioception in the lower back. Journal of Orthopaedic and Sports Physical Therapy 1994;19(5):282–95. Portney LG, Watkins MP. Foundations of clinical research: applications to practice. Norwalk, USA: Appletone and Lange; 1993. Richardson CA, Jull G, Hodges P, Hides J. Therapeutic exercise for spinal segmental stabilization in low back pain: scientific basis and clinical approach. Edinburgh, UK: Churchill Livingstone; 1999. Rowe PJ, Myles CM, Hillmann SJ, Hazlewood ME. Validation of flexible electrogoniometry as a measure of joint kinematics. Physiotherapy 2001;87(9):479–88. Sim J, Wright C. Research in health care: concepts, designs and methods. Cheltenham, UK: Nelson Thornes; 2002. Solomonow M, Eversull E, Zhou BH, Baratta RV, Zhu M- P. Neuromuscular neutral zones associated with viscoelastic hysteresis during cyclic lumbar flexion. Spine 2001;26(14):314–24. Solomonow M, Baratta RV, Zhou BH, Burger E, Zieske A, Gedalia A. Muscular dysfunction elicited by creep of lumbar viscoelastic tissue. Journal of Electromyographic Kinesiology 2003;13(4): 381–96. Waddell G. The back pain revolution. Edinburgh, UK: Churchill Livingston; 1998. Walter SD, Eliasziw M, Donner A. Sample size and optimal designs for reliability studies. Statistics in Medicine 1998;17:101–10.

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Manual Therapy 11 (2006) 208–213 www.elsevier.com/locate/math

Original article

Motor control and the management of musculoskeletal dysfunction Paulette M. van Vlieta,, Nicola R. Heneghanb a

School of Health Sciences, University of Birmingham, 52 Pritchatt’s Road, Edgbaston B15 2TT, UK b School of Health Sciences, University of Birmingham, UK Received 29 October 2005; received in revised form 28 February 2006; accepted 30 March 2006

Abstract This paper aims to develop understanding of three important motor control issues—feedforward mechanisms, cortical plasticity and task-specificity and assess the implications for musculoskeletal practice. A model of control for the reach-to-grasp movement illustrates how the central nervous system integrates sensorimotor processes to control complex movements. Feedforward mechanisms, an essential element of motor control, are altered in neurologically intact patients with chronic neck pain and low back pain. In healthy subjects, cortical mapping studies using transcranial magnetic stimulation have demonstrated that neural pathways adapt according to what and how much is practised. Neuroplasticity has also been demonstrated in a number of musculoskeletal conditions, where cortical maps are altered compared to normal. Behavioural and neurophysiological studies indicate that environmental and task constraints such as the goal of the task and an object’s shape and size, are determinants of the motor schema for reaching and other movements. Consideration of motor control issues as well as signs and symptoms, may facilitate management of musculoskeletal conditions and improve outcome. Practice of entire everyday tasks at an early stage and systematic variation of the task is recommended. Training should be directed with the aim of re-educating feedforward mechanisms where necessary and the amount of practice should be sufficient to cause changes in cortical activity. r 2006 Elsevier Ltd. All rights reserved. Keywords: Musculoskeletal dysfunction; Motor control; Rehabilitation

1. Introduction An understanding of motor control is central to management of patients with a damaged central nervous system (CNS) but recent research (Falla et al., 2004a, b; On et al., 2004) indicates it is also of great importance in the management of musculoskeletal dysfunction in patients with an intact CNS. Historically, an in depth understanding of motor control has not been central to musculoskeletal practice, although discussion of certain motor control issues in a recent authoritative text (Boyling and Jull, 2004) indicates that this is changing. This paper aims to develop understanding of three important motor control issues—feedforward mechanCorresponding author. Tel.: +44 121 4158145; fax: +44 121 4143158. E-mail address: [email protected] (P.M. van Vliet).

1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.03.009

isms, cortical plasticity and task-specificity. First, a model is presented that illustrates how the sensorimotor processes needed to perform a typical movement are integrated. Then, evidence is presented indicating that the feedforward mechanisms used to monitor movement and the functional organization of the cortex can change in response to musculoskeletal dysfunction. The authors also show that the motor plan generated depends on the specificity of the task being performed. The implications of these findings for management of patients with musculoskeletal dysfunction are discussed.

2. A model of motor control for reach to grasp In this section, a model of the control of reach to grasp movements will be used to illustrate the integration of

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sensorimotor processes in performing a movement. Reach to grasp has been chosen because there is sufficient knowledge available to build up a representation of CNS control, and because it is an essential everyday movement. Research on CNS control of reach-to-grasp in healthy subjects is encapsulated in a model shown in Fig. 1 and this model is supported by substantive data from both computer simulation and human studies (Hoff and Arbib, 1993). The model is an example of a ‘motor program’, defined as ‘‘a set of motor commands that is pre-structured and that defines the essential details of a skilled action’’ (Schmidt and Wrisberg, 2000). It is likely that we use motor programs for many actions (Schmidt and Wrisberg, 2000). According to this model, the reach is planned with respect to the end goal of the movement, by ensuring that the time to close the hand from maximum aperture is constant. In the model, it is proposed that the parameter used to control the path of the hand through space is the third derivative of wrist position, called jerk (velocity is the first derivative and acceleration the second). The CNS tries to minimize the amount of jerk during the reach. Two important parameters for controlling the movement are therefore, time to close the hand and minimum jerk. There is a two-way interaction between the neural processes controlling transport and grasp, so that the expected duration to the target, of each of these elements, is monitored and adjusted to ensure temporal matching. Although there is much evidence that reaching movements are planned in advance of the movement via such a motor program (e.g. Jeannerod, 1988), there must be ongoing monitoring of transport and grasp, especially if conditions change after movement onset or where more accurate movements are required. The model proposes two mechanisms for this function—

Activation of reaching and grasping

Preshape

Transport Time needed Duration

Visual and tactile input

Time-based co-ordination Duration + _

Time needed

Time needed

Enclose

209

feedback and feedforward (anticipatory control). Feedback from vision and proprioception about hand location and hand aperture is useful in the latter part of the reach, since the minimum time needed for a response to this information is estimated at about 100 ms (Jeannerod, 1988). Before this, feedforward mechanisms are responsible for on-line movement adjustments (Desmurget et al., 1999). There is evidence that the feedforward mechanism for reaching works by comparing target position with an instantaneous internal predictive estimate of hand position (efferent copy), and this information is used to modify the ongoing motor command (Desmurget et al., 1999; Desmurget and Grafton, 2000).

3. Evidence of disruption to feedforward mechanisms in musculoskeletal dysfunction 3.1. Feedforward mechanisms in healthy subjects As well as in grasp, feedforward mechanisms have been identified in a number of muscle groups involved in other movements. Most of the empirical studies consider muscle activity that occurs 100 ms before to 50 ms after the onset of the prime mover to represent feedforward control (Aruin and Latash 1995). In the reach-to-grasp model described earlier, feedforward operated to adjust the position of the hand. Feedforward also occurs in order to move the centre of mass prior to limb displacement, maintain the stability of the vestibular system and visual field during neck movement, prepare for the anticipated reactive forces or to act synergically to maintain local muscular stability surrounding spinal joints during large torque generating movements (Falla et al., 2004b). Feedforward control is ongoing during the movement as well as occurring before the movement begins. In healthy subjects Falla et al. (2004b) have shown that the sternocleidomastoid and cervical extensor muscles demonstrate feedforward activation during rapid unilateral and bilateral upper limb flexion, extension and abduction. These muscles were activated within 50 ms of the onset of deltoid muscle activity. The authors suggest that as well as opposing the reactive forces during arm movements, this mechanism is necessary to achieve stability for the visual and vestibular systems during movement. 3.2. Feedforward mechanisms and musculoskeletal dysfunction

Time needed

Fig. 1. An example of a co-ordinated control program made up of three motor schemas. Whichever schema needs more time sets the total duration specified by the time-based coordination model (Reproduced by kind permission of Elsevier, Hoff and Arbib, 1993).

Falla et al. (2004a) compared onset of neck muscle activation in people with chronic neck pain to healthy subjects during flexion and extension of the upper limb. In contrast to healthy subjects, during flexion, activation

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of deep cervical flexors, contralateral sternocleidomastoid and anterior scalene muscles were significantly delayed in the patients. Further exploration of feedforward mechanisms could examine more purposeful movements, as it is not known whether similar findings will occur with tasks such as reaching for an object or combing the hair. Feedforward mechanisms have been shown to be compromised in the trunk muscles in the presence of low back pain (Hodges, 2001; Hodges et al., 2003) and isometric muscle fatigue (Allison and Henry, 2002). Also, the feed-forward activation of transverses abdominus was found to be delayed in the presence of longstanding groin pain (Cowan et al., 2004). Feedforward mechanisms were even found to be absent during rapid upper limb activity in patients with chronic recurrent low back pain (Hodges and Richardson, 1999). The exact mechanism is poorly understood but the loss of anticipatory control of the proximal segment/spine during limb movement (changing the centre of mass) may adversely affect articular stability. From in vitro studies Panjabi (1992) proposed that 80% of cervical stability was attributable to the muscular system (active subsystem) compared with the passive stability of ligaments and capsule, etc. Where muscular stability is compromised additional strain may be placed on the articular structures further exacerbating instability and/ or pain. Alternatively, the pain itself might cause an inhibition of feedforward activity. Hodges et al. (2003) provide some evidence for this by demonstrating that experimentally induced pain can change the feedforward activity of trunk muscles in anticipation of arm movements. Also, afferent information to the CNS encapsulates more than nociceptive information and the influence of factors such as altered proprioception, muscle length and muscle tension, on feedforward activity, needs to be elucidated. For optimal movement a combination of both feedback and feedforward processes are likely to be required (Desmurget and Grafton, 2000). There has been little work to date considering the implications for clinical practice of altered feedforward mechanisms in patients with dysfunction. For example at what stage of neuromusculoskeletal dysfunction do these mechanisms begin to manifest themselves? Do they follow the onset of pain or more importantly do they precede the pain? How may they be rehabilitated? The authors are aware of only one study to date that has considered whether a loss of feedforward control can be rehabilitated with physiotherapy. Cowan et al. (2003) reported that a 6week conventional programme of physiotherapy for 40 subjects with patellofemoral pain, including specific muscle retraining, biofeedback and taping aimed at restoring coordination and control of the vasti muscles, was effective in restoring feedforward recruitment of these muscles. The programme demonstrated that

physiotherapy can be effective in the restoration of feedforward mechanisms. However, it was not clear which component of the treatment was responsible. Also, EMG measurements were taken during a ‘rise’ and ‘rock’ task, which, although reliable in the laboratory, may not closely resemble use of the vasti muscles in everyday activities. Despite good support for the use of management approaches which utilize aspects of motor control theory through muscle retraining programmes for rehabilitation of lumbar muscles (O’Sullivan et al., 1997) and cervical muscles (Jull et al., 2002), there is a paucity of studies specifically evaluating the effect of therapy on feedforward control within the spine.

4. Evidence relating to cortical plasticity 4.1. Practice and cortical plasticity Recent research has indicated that the functional organization of the primary motor cortex, rather than being fixed, can change in response to practice. The commonly used method in such studies is by measuring the motor evoked potentials (MEPs) in response to transcranial magnetic stimulation (TMS). TMS is noninvasive and is delivered via a magnetic coil placed near the skull. A cortical map is constructed indicating cortical representation of muscles or movements. One study compared muscle representations in both hemispheres in people skilled at a volleyball ‘strike’ movement and in runners (Tyc et al., 2005). MEPs were recorded from the proximal medial deltoid and distal extensor carpi radialis muscles during magnetic stimulation, while subjects were seated and either aiming to hit a target or perform static wrist extension. The size of the cortical map for middle deltoid was larger for volleyballers than for runners. Furthermore, the total size representation for both muscles was larger for the dominant arm than the non-dominant arm, in the volleyball group. This finding supports the hypothesis that activity drives cortical plasticity, since there is different cortical organization between two groups with different levels of skill. Even a small amount of practice can cause cortical changes. Hayashi et al. (2002) found that the amplitudes of motor-evoked potentials and the size of the cortical map increased dramatically after 100 repetitions of simple index finger abduction. Such quick changes are likely to be due to changes in synaptic efficiency from a strengthening of existing synapses (Hayashi et al., 2002). With larger amounts of practice however, changes in the balance of excitation and inhibition may induce anatomical changes in synaptic organization. There is also evidence that this functional organization of somatosensory cortex may change dynamically according to and during task requirements. Braun et al.

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(2001) compared organization of somatosensory cortex when subjects were doing the well-learned task of writing compared to at rest. During the two conditions a tactile sensation with force of 1.6 N was delivered to the 1st and 5th digits. Cortical representations of the stimulated fingers were measured. The cortical representations of each finger were further apart during writing than at rest, indicating functional reorganization. The authors proposed that there are different preexisting maps, and the somatosensory cortex switches rapidly between them according to task requirements. This idea is supported by other studies of cortical plasticity (e.g. Karni et al., 1998). 4.2. Musculoskeletal dysfunction and cortical plasticity Changes in cortical maps have also been measured in a number of musculoskeletal conditions including chronic knee (On et al., 2004) and back pain (Flor, 2003), nerve injury (Braune and Schady, 1993), rheumatoid arthritis (Jones and Derbyshire, 1997), fibromyalgia (Salerno et al., 2000), amputation (Braune and Schady, 1993), and also with immobilization (Zanette et al., 2004). In patients with patellofemoral pain syndrome, On et al. (2004) found that the amplitude of the MEP for vastus medialis oblique (VMO) and vastus lateralis when TMS was applied was significantly increased compared to control subjects, especially in the VMO. It was argued that through a restriction of movement induced by pain, proprioceptive input to the CNS may have been reduced. The larger MEPs of the stabilizing muscles of the patella may be a response to these changes. In chronic back pain also, Flor (2003) have documented an expansion of the cortical representation related to nociceptive input and also an increased cortical excitation. Some of the changes seen after nerve injury may be due to cortical plasticity. One group of patients with microsurgically repaired median or ulnar nerve transections was subjected to tests of thermal and pain thresholds, vibration and tactile thresholds, stimulus– response curves, two point discrimination and locognosia (location of tactile stimuli) (Braune and Schady, 1993). The fingertips had better tactile sensitivity and recovered normal localization capacity before more proximal areas. As they should have the least reinnervated mechanoreceptors these findings were therefore attributable to central changes.

5. Task specificity of control of everyday actions There is ample evidence that the motor control of everyday actions is task-specific. For example, the kinematics of reaching movements requiring a pincer

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grasp, are characterized by a longer deceleration phase than those using whole hand grasp, allowing more time to adjust for potential spatial error (Bootsma et al., 1994). Neurophysiological evidence also demonstrates selective cortical activation for different types of grasp (Rizzolatti et al., 1988). Accordingly, studies have been undertaken to assess the effectiveness of delivering task-specific motor training to neurologically impaired patients. For example, in a well-designed randomized controlled trial, stroke patients’ sitting balance was trained using systematically varied reaching tasks such as changing the speed, direction, object weight, seat height and amplitude of the movement (Dean and Shepherd, 1997). The programme resulted in significantly better performance compared to a placebo control group who received sham training. Other studies in patients with stroke have also demonstrated the positive effect of task-specific training (Richards et al., 1993; Dean et al., 2000; Blennerhassett and Dite, 2004). Task-specific training is likely to also enhance the outcome for musculoskeletal conditions, but as yet this has not been systematically evaluated. The studies reviewed earlier demonstrate cortical changes in response to practice of specific movements, in neurologically intact subjects. Task-specific training is therefore likely to be useful in the rehabilitation of people with musculoskeletal dysfunction with intact CNS, to gain optimal skill acquisition.

6. Implications clinical practice The evidence presented points to several suggestions for musculoskeletal clinical practice. First, our general argument is that an understanding of the motor control for the task or movement that is targeted for rehabilitation is essential, including at the very least the processes involved in generating and monitoring movement commands and how these are integrated with feedforward and various sensory feedback modalities. For example, the evidence on cortical plasticity and task specificity suggests that practice of part of a task such as wrist extension, may not activate the same neuronal network as practice of wrist extension within the whole task such as reaching. Instead the part practice would develop and strengthen a motor programme for ‘wrist extension’. This may cause the lack of carry over between exercises and everyday activity, often seen in clinical practice. Therefore, it is recommended that functionally oriented exercise be incorporated as early as possible in the management, rather than after many repetitions of component parts of movements. In this way, the necessary feedforward and feedback mechanisms can be integrated with the appropriate motor programme, while function of the damaged part is

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regained. This contention needs to be formally evaluated by empirical research, to see whether outcome is more effective or is achieved more quickly. Second, because of the task specific nature of cortical control, therapists should consider asking patients to practice variations on the particular task or movement being rehabilitated, to ensure that the cortical connections necessary for different task requirements are also developed or strengthened. Otherwise, it is possible that the person’s performance might only be sufficient in some task conditions, and not others. For this, previous studies with stroke patients could lead the way, where factors such as speed, direction, object weight, seat height and amplitude of the movement could be varied systematically during practice (Dean and Shepherd, 1997). For example, a patient with a history of pain on cervical spine extension may be advised to extend the head with the deep neck flexors activated. This exercise could be performed while taking something out of a cupboard (task-specific practice), and within this practice, the speed, range of motion, loading, start position (head in rotation or side flexion), could be varied to strengthen the cortical connections associated with each variation of that task. Changes in feedforward that accompany some musculoskeletal conditions must be important for the patient’s functional outcome and the risk of future reoccurrence of the condition. It would seem very useful for therapists to know or work out the feedforward activity that would normally precede or occur during the movement being trained. In some cases, evidence will be available to describe the altered feedforward mechanisms for the condition, such as in the case of chronic neck pain (Falla et al., 2004a). It may be possible to reeducate the appropriate feedforward mechanisms (Cowan et al., 2003). In stroke rehabilitation, anticipatory postural adjustments can be retrained by identifying the necessary postural muscle activity and choosing an amplitude of movement for practise, which is just beyond the patient’s control, thereby challenging the CNS to increase the postural activity. Movement amplitude is slowly increased as performance improves. This approach may be useful in musculoskeletal rehabilitation. Another aspect is that if altered feedforward precedes the emergence of pain, it might be possible to predict which patients might develop a painful condition, and institute intervention to prevent it. Last, an important issue is the recognition of the flexible nature of cortical connections. Changes in cortical maps can occur relatively quickly (Hayashi et al., 2002). Implications from this are that injured people presenting to physiotherapists may already have altered cortical maps if the condition has caused them to move differently from normal, but that it might be possible to reverse these changes with practice. The

amount of practice necessary may be further elucidated by research that carefully records the amount of practice for a particular condition with particular chronicity, and uses measures of both cortical activity and motor performance to measure outcome. This approach could be expected to provide guidelines for amount of practice, which could be adapted to suit individual presentations of the condition. Conclusions about the amount of practice necessary to alter cortical connections will also need to be combined with guidelines for the amount of practice necessary to cause changes in strength or endurance, which are more commonly considered in musculoskeletal practice.

Clinical messages

   

Remedial practice of movement components should be practised within the whole task, from the outset, to encourage desired cortical activity. Task practice should be systematically varied. The possibility of changes in feedforward control should be considered and retrained if possible. Practice should be sufficient to cause changes in cortical activity.

Acknowledgements The authors are grateful to Alison Rushton for comments on the draft version of this paper.

References Allison GT, Henry SM. The influence of fatigue on trunk muscle responses to sudden arm movements, a pilot study. Clinical Biomechanics 2002;17:414–7. Aruin A, Latash M. Directional specificity of postural muscles in feedforward postural reactions during fast voluntary arm movements. Experimental Brain Research 1995;103(2):323–32. Blennerhassett J, Dite W. Additional task-related practice improves mobility and upper limb function early after stroke: a randomised controlled trial. Australian Journal of Physiotherapy 2004;50: 219–24. Bootsma RJ, Marteniuk RG, MacKenzie CL, Zaal FTJM. The speedaccuracy trade-off in manual prehension: effects of movement amplitude, object size and object width on kinematic characteristics. Experimental Brain Research 1994;98:535–41. Boyling JD, Jull GA. Grieve’s modern manual therapy: the vertebral column 2004. Edinburgh: Churchill Livingstone; 2004. Braun C, Heinz U, Schweizer R, Wiech K, Birbaumer N, Topka H. Dynamic organization of the somatosensory cortex induced by motor activity. Brain 2001;124:2259–67. Braune S, Schady W. Changes in sensation after nerve injury or amputation: the role of central factors. Journal of Neurology, Neurosurgery and Psychiatry 1993;56:393–9. Cowan SM, Bennell KL, Hodges PW, Crossley KM, McConnell J. Simultaneous feedforward recruitment of the vasti in untrained

ARTICLE IN PRESS P.M. van Vliet, N.R. Heneghan / Manual Therapy 11 (2006) 208–213 postural tasks can be restored by physical therapy. Journal of Orthoepaedic Research 2003;21:553–8. Cowan SM, Schache AG, Brukner P, Bennell KL, Hodges PW, Coburn P, et al. Delayed onset of transversus abdominus in longstanding groin pain. Medicine and Science in Sports and Exercise 2004;36(12):2040–5. Dean CM, Richards CL, Malouin F. Task-related circuit training improves performance of locomotor tasks in chronic stroke. Archives of Physical Medicine and Rehabilitation 2000;81:409–17. Dean CM, Shepherd RB. Task-related training improves performance of seated reaching tasks after stroke. Stroke 1997;28(4):722–8. Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE, Grafton ST. Role of the posterior parietal cortex in updating reaching movements to a visual target. Nature Neuroscience 1999;2(6):563–7. Desmurget M, Grafton S. Forward modelling allows feedback control for fast reaching movements. Trends in Cognitive Neurosciences 2000;4(11):423–31. Falla D, Jull G, Hodges PW. Feedforward activity of the cervical flexor muscles during voluntary arm movements is delayed in chronic neck pain. Experimental Brain Research 2004a;157:43–8. Falla D, Rainoldi A, Merletti R, Jull G. Spatio-temporal evaluation of neck muscle activation during postural perturbations in healthy subjects. Journal of Electromyography and Kinesiology 2004b;14:463–74. Flor H. Cortical reorganization and chronic pain: implications for rehabilitation. Journal of Rehabilitation Medicine 2003(Suppl 41):66–72. Hayashi S, Hasegawa Y, Kasai T. Transcranial magnetic stimulation study of plastic changes of human motor cortex after repetitive simple muscle contractions. Perceptual and Motor Skills 2002;95:699–705. Hodges P, Richardson C. Altered trunk muscle recruitment in people with low back pain with upper limb movement at different speeds. Archives of Physical Medicine and Rehabilitation 1999;80(9): 1005–12. Hodges PW. Changes in motor planning of feedforward postural responses of the trunk muscles in low back pain. Experimental Brain Research 2001;141:261–6. Hodges PW, Moseley GL, Gabrielsson A, Gandevia SC. Experimental muscle pain changes feedforward postural responses of the trunk muscles. Experimental Brain Research 2003;151:262–71. Hoff B, Arbib MA. Models of trajectory formation and temporal interaction of reach and grasp. Journal of Motor Behaviour 1993;25(3):175–92.

213

Jeannerod M. The neural and behavioural organisation of goal directed movements. Oxford: Clarendon Press; 1988. Jones AKP, Derbyshire SWG. Reduced cortical responses to noxious heat in patients with rheumatoid arthritis. Annals of Rheumatic Diseases 1997;56:601–7. Jull G, Trott P, Potter H, Zito G, Niere K, Shirley D, et al. A randomized control trial of exercise and manipulative therapy for cervicogenic headache. Spine 2002;27(17):1835–43. Karni A, Meyer G, Rey-Hiploito C, Jezzard P, Adams MM, Turner R. The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proceedings of the National Academy of Science USA 1998; 95:861–8. On AY, Uludag B, Taskiran E, Ertekin C. Differential corticomotor control of a muscle adjacent to a painful joint. Neurorehabilitation and Neural Repair 2004;18(3):127–33. O’Sullivan P, Twomey L, Allison G. Evaluation of specific stabilisation exercises in the treatment of chronic low back pain with radiologic diagnosis of spondylosis or spondylolithesis. Spine 1997;22(24):2959–67. Panjabi M. The stabilizing system of the spine. Part II. Neutral zone and instability hypothesis. Journal of Spinal Disorders 1992;5(4):390–6. Richards CL, Malouin F, Wood-Dauphinee S, Williams JI, Bouchard J-P, Brunet D. Task-specific physical therapy for optimization of gait recovery in acute stroke patients. Archives of Physical Medicine and Rehabilitation 1993;74:612–20. Rizzolatti G, Camarda R, Fogassi G, Gentilucci M, Lupping G, Matelli M. Functional organisation of inferior area 6 in the macque monkey. II Area 5 and the control of distal movements. Experimental Brain Research 1988;71:491–507. Salerno A, Thomas E, Olive P, Blotman F, Picot MC, Georgesco M. Motor cortical dysfunction disclosed by single and double magnetic stimulation in patients with fibromyalgia. Clinical Neurophysiology 2000;111:994–1001. Schmidt RA, Wrisberg CA. Motor learning and performance: a problem-based learning approach. Champaign, IL: Human Kinetics; 2000. Tyc F, Boyadjian A, Devanne H. Motor cortex plasticity induced by extensive training revealed by transcranial magnetic stimulation in human. European Journal of Neuroscience 2005; 21:259–66. Zanette G, Manganotti P, Fiaschi A, Tamburin S. Clinical Neurophysiology 2004;115:1264–75.

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Manual Therapy 11 (2006) 214–224 www.elsevier.com/locate/math

Original article

A preliminary investigation into the relationship between cervical snags and sympathetic nervous system activity in the upper limbs of an asymptomatic population Andrea Moulson, Tim Watson School of Paramedic Sciences, Physiotherapy & Radiography, Faulty of Health and Human Science, University of Hertfordshire, College Road, Hatfield, Hertfordshire AL10 9AB, UK Received 7 November 2005; received in revised form 9 March 2006; accepted 6 April 2006

Abstract Spinal manipulative therapy techniques are commonly employed by physiotherapists in the clinical setting for the management of neuromusculoskeletal pain and dysfunction, although their underlying mechanism is not fully understood. Mulligan’s sustained natural apophyseal glides (SNAGs) constitute one of these techniques. This preliminary investigation was undertaken to investigate the relationship between the application of cervical SNAGs to the C5/6 intervertebral joint (with cervical right rotation) and indirect measures of sympathetic nervous system (SNS) activity. Previous investigations have suggested that cervical manipulative therapy techniques, separate to cervical SNAGs, result in a sympatheoexcitatory effect and that this may be instrumental in producing an analgesic response. Sixteen asymptomatic subjects participated in a laboratory-based experiment. A single blind, randomized, within subject, repeated measures study design which included control, placebo and treatment comparisons was used. Measures of skin conductance (SC) and skin temperature (ST) in the right and left upper limbs were used as indicators of SNS activity. The cervical SNAG technique produced a sympathoexcitatory response demonstrated by a significant increase in SC during application of the treatment intervention (Po0:0005) and for a 2-min period after the intervention (P ¼ 0:001) compared with control. There was also a significant increase in SC for the placebo condition, both during intervention (P ¼ 0:015) and after intervention (P ¼ 0:011) compared with control. There was a statistically significant difference in SC between placebo and treatment conditions for the 2-min period after the intervention had been applied (P ¼ 0:01). A trend did emerge for ST change, illustrating a decrease in ST for the treatment and placebo conditions compared with control, however this did not reach statistically significant levels. There were no apparent left/right upper limb differences for SC and ST for each condition. The results of this study suggest that cervical SNAG techniques, performed on naı¨ ve asymptomatic subjects, have a sympathoexcitatory effect as measured by changes in SC and ST. The importance of this sympathoexcitatory effect in relation to potential mechanisms for manipulation induced analgesia are discussed, and further areas of research proposed. r 2006 Elsevier Ltd. All rights reserved. Keywords: Sympathoexcitation; Sustained natural apophyseal glides (SNAGs); Manual therapy

1. Introduction The Mulligan concept is integral to the clinical practice of many physiotherapists (Konstantinou et al., Corresponding author.

E-mail address: [email protected] (A. Moulson). 1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.04.003

2002) and includes techniques such as sustained natural apophyseal glides (SNAGs), natural apophyseal glides (NAGs) and mobilization with movements (MWMs). Several clinical studies have suggested that these techniques are an effective physiotherapeutic tool in the treatment of neuromuscular pain and dysfunction (Abbott, 1998, 2001; Folk, 2001; Vicenzino et al., 2001;

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Horton, 2002; Hsieh et al., 2002; Kochar and Dogra, 2002). Recent studies however have questioned Mulligan’s original belief that biomechanical factors such as the correction of ‘joint maltracking’ underpin their effect (Hearn and Rivett, 2002; Hseich et al., 2002) and consequently there appears to be a scarcity of quality evidence explaining their underlying mechanism (Wilson, 1995; Exelby, 2002). The limited understanding related to the underlying mechanism of Mulligan techniques is replicated in other commonly used manual therapy treatments such as spinal manipulative therapy (SMT) and it has been suggested that the application of these techniques has been largely based on clinical observations and hypothetical models (McGuiness et al., 1997; Zusman, 2004). A new theory as to the basic science of SMT has recently emerged. Several studies have examined the physiological correlates of manual therapy by investigating the effects of techniques on the nociceptive and sympathetic nervous system (SNS) (Peterson et al., 1993; Slater and Wright, 1995; Vicenzino et al., 1994, 1995; Wright and Vicenzino, 1995; Chiu and Wright, 1996; McGuiness et al., 1997; Vicenzino et al., 1998a b; Willett and Toppenberg, 2001; Perry, 2002). This research suggests a relationship between SMT and changes in SNS activity, specifically that SMT induces a pattern of sympathoexcitation which is reflected by generalized increases in skin conductance (SC) and concurrent decreases in skin temperature (ST). Furthermore, it has been theorized that patterns of sympathoexcitation may reflect primitive defensive ‘fight or flight’ reactions which are linked to endogenous analgesia (Lovick, 1991; Wright, 1995; Wright and Vicenzino, 1995; Bandler et al., 2000, 2002). The focus of this paper relates to cervical SNAGs. As yet, no study has investigated the relationship between SNAGs and the SNS, although several studies have investigated other cervical SMT, peripheral joint mobilization and SNS activity (Peterson et al., 1993; Vicenzino et al., 1995; Chiu and Wright, 1996; Abbott, 1998; Vincenzino et al., 1998a, b; Abbott, 2001; Sterling et al., 2001; Willet and Toppenberg, 2001; Hseich et al., 2002; Perry, 2002; Paungmali et al., 2003). Peterson et al. (1993) investigated SNS response in asymptomatic subjects to grade three PA mobilizations of C5, as measured by SC and ST changes in the upper limb. Results demonstrated a significant increase in SC for the treatment condition when compared to placebo and control. There was a corresponding small, but significant decrease in ST for the treatment condition compared to control, although this was not significant between treatment and placebo conditions. The study’s results indicated that SMT was associated with an increase in SNS activity. Similar results were found in a comparable study by Chiu and Wright (1996) which investigated the effects of different rates of application

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of C5 grade three PA mobilizations on SNS correlates in the upper limbs of an asymptomatic population. Chiu and Wright (1996) also speculated that SNS response to SMT may be affected by the duration and frequency of the technique performed. This concept has been supported by other studies investigating the association between dose of treatment and SNS activity over time (Vicenzino et al., 1994; McGuiness et al., 1997; Souvlis et al., 2001). Additional work exploring the relationship between SNS activity and SMT has been completed by Vicenzino et al. (1995) who investigated the effects of C5/6 lateral glide technique on SNS correlates in the upper limb. Results in this study supported previous research and found significant increases in SC for treatment condition over placebo and control in the asymptomatic population. However, they also found significant increases in ST for the treatment condition, results which contrasted with previous studies (Peterson et al., 1993; Chiu and Wright, 1996). From these studies it is apparent that there seems to be a consistent sympathoexcitatory relationship between SMT and SC, which appears to be less consistent with regard to ST. In trials which have investigated the SNS response to SMT in the patient population, there does appear to be a correlation between sympathoexcitation and analgesia (Vicenzino et al., 1998a; Sterling et al., 2001). Sterling et al. (2001) investigated the effects of C5, PA, grade three mobilizations on a population of neck pain sufferers with identified dysfunction at this level. Results suggested that the treatment condition stimulated a pattern of sympathoexcitation as measured by SC and ST changes in the upper limb. Sympathoexcitation changes occurred concurrently with significant reductions in measures of mechanical hyperalgesia, thus lending credence to a possible link between measures of SNS activity and manipulation induced analgesia. Similar conclusions were reached in a study by Vicenzino et al. (1998a) whereby the authors used confirmatory factor analysis to test the correlation between pain perception and parameters related to the SNS function in a population of patients with lateral epicondylalgia. The treatment investigated was a C5/6 lateral glide technique and SNS parameters included measurement of upper limb SC, ST and blood flux. This study found a strong correlation and suggested that those individuals who exhibited the most change in pain perception also were those who exhibited the most change in SNS parameters. The sympathoexcitatory relationship between SC and ST and response to SMT has lead to speculation regarding the nature of manipulation induced analgesia (Wright and Vicenzino, 1995; Wright, 1995, 2002). Patterns of sympathoexcitation have been elicited in animal models with direct stimulation of the dorsolateral periaqueductal grey region of the brain (dlPAG),

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and this has been demonstrated to have an association with the analgesia produced in ‘fight or flight’ situations (Bandler et al., 1991, 2000; Lovick, 1991). Manual therapists, in conjunction with other researchers, have speculated that manipulation induced analgesia may utilize a similar pathway and hypothesize that manipulative therapy may produce a non-opioid form of analgesia utilizing descending inhibitory pathways involving the PAG (Wright, 1995; Skyba et al., 2003; Zusman, 2004). Recent animal experiments support this concept (Sluka and Wright, 2001; Malisza et al., 2003; Skyba et al., 2003). Consequently, patterns of sympathoexcitation as demonstrated in studies investigating SMT may illustrate a link between manual therapy techniques, the dlPAG and the descending pain inhibitory pathways (Wright and Vicenzino, 1995; Wright, 1995, 2002). The purpose of this research was to investigate the relationship between cervical SNAGs and concurrent effects on SNS activity measured indirectly in the asymptomatic population. The results of this study may contribute to the growing body of information on the neurophysiological effects of manual therapy techniques, and may potentially contribute to a greater understanding of manipulation-induced analgesia.

2. Methodology 2.1. Subjects The study included 16 asymptomatic subjects (11 females and 5 males) aged 18–37 years (mean ¼ 23.06 years; SD ¼ 5.35 years). It was envisaged that this preliminary study would provide reliable data for use in future sample size and power calculations for similar studies (Altman, 1991). Exclusion criteria included: previous neuromusculoskeletal dysfunctions affecting the cervical spine and upper quadrant, previous experience of SMT and any subjects with contraindications to manual therapy (Grieve, 1989). Subjects were instructed to refrain from smoking, participating in strenuous exercise and consuming alcohol and caffeine for 1 h prior to the experiment because of their potential influence on the SNS (Andreassai, 1995; Nance and Hoy, 1996). All volunteers were given written information prior to the experiment and signed a consent form. Ethical approval was gained from the Radiography and Physiotherapy Ethics Committee at the University of Hertfordshire. 2.2. Research design The research design used was a single blind, randomized, within subject, repeated measures design which included control, placebo and treatment comparisons.

In overview, 16 subjects attended measurement sessions at the same time, on three different days to receive an intervention of either: treatment, placebo or control. Bilateral upper limb SC and ST were simultaneously recorded before, during and after intervention. Subjects received all three experimental conditions and acted as their own controls. The order of intervention was randomized for each participant to reduce the effect of researcher and order bias (Altman, 1991; Winter et al., 1991; Sims and Wright, 2000).The success of subject blinding to the interventions and purpose of the study was investigated via a post-trial questionnaire to ensure that subjects were naı¨ ve to the testing procedure.

2.3. Research method Subjects were positioned in a chair in a standardized position and were instructed to look at a marked spot on the wall. At each recording session, the researcher explained the experimental procedure and whether head rotation to the right (
3) was required. If it was, subjects were told that they should turn at a speed and distance that was comfortable to them, and that this should be pain free. This procedure was chosen to best reflect the clinical environment. Subjects were also informed that whilst turning their heads to the right, the researcher may or may not place their hands their neck. Subjects were advised to inform the researcher if they were uncomfortable at any time. The skin on the palmar surfaces of the subject’s first, second and third digits of the left and right hands were cleaned with an Alcowipe prior to the application of the SC and ST probes (Millington and Wilkinson, 1983; Vicenzino et al., 1994; Chiu and Wright, 1996). The intervertebral joint level of C5/6 was marked on the subject’s neck, to ensure rapid location of this level during the experimental procedure. Previous experimental work suggests that experienced manual therapists have acceptable intra tester reliability for the correct location of spinal levels (Jull et al., 1997; McKenzie and Taylor, 1997), suggesting that C5/6 would be consistently located during each experimental procedure. Following this an 8-min period elapsed to allow for stabilization of recording electrodes (Venables and Christie, 1973; Nance and Hoy, 1996; Biopac Systems Inc). After this period, a 2 min baseline measure of SC and ST was made. Following this, the researcher approached the subject from behind and administered one of the three interventions explained below. Once completed the subject then remained in the start position and ST and SC recordings were taken for another 2 min. It was not possible to blind the researcher to the specific intervention applied, although the recording monitor was not visible to the researcher or subject during the application of the intervention in order to minimize potential feedback.

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2.3.1. Treatment intervention For the treatment intervention, a cervical SNAG was administered to the subject’s C5/6 intervertebral joint whilst the subject simultaneously turned their head to the right from a standardized neutral position (Mulligan, 1999). This procedure was repeated a total of three times in accordance with Mulligan’s ‘rule of three’, which suggests that only three spinal techniques should be used in the first encounter between therapist and patient (Mulligan, 1999). The researcher maintained contact with the C5/6 intervertebral joint between the application of each SNAG technique to ensure consistency of manual contact. The direction of the SNAG technique was parallel to the plane of the joint (Mulligan, 1999; Exelby, 2002). 2.3.2. Placebo intervention For the placebo intervention, the researcher followed the same procedure as the treatment intervention and applied manual contact to the same points on the cervical spine, but did not apply the accessory glide which would constitute an SNAG technique. The subject was instructed to turn their head to the right from a standardized neutral position whilst the researcher maintained skin contact between her thumbs and the C5/6 intervertebral joint. This procedure was repeated a total of three times.

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there is increased sweating of the palmar surfaces of the feet and hands in order to facilitate grasping/grip for escape and to play a role in thermoregulation (Darrow, 1933; Edelberg, 1973; Janig, 1990; Andreassai, 1995). As a result of this sympathoexcitatory response, SC and ST are commonly used to measure sudomotor and vasomotor activity, respectively, and are accepted as an indirect measure of SNS activity (Edelberg, 1971; Kornberg and McCarthy, 1992; Andreassai, 1995; Nance and Hoy, 1996; Genno et al., 1997). Continuous recording of subject ST was achieved with the use of non-invasive probes (Biopac TSD102D series temperature transducer) placed on the palmar surface of the distal phalanx of the subjects left and right ring finger (Darrow, 1933; Uematsu et al., 1988; Scerbo et al., 1992; Nance and Hoy, 1996). Continuous SC measurements were also recorded with non-invasive probes (Biopac TSD103A electrodermal activity transducer), placed on the palmar surfaces of the distal phalanx of the left and right first and second digits (Scerbo et al., 1992; Sterling et al., 2001). A computerized data acquisition system (Acknowledge, version 3.7.1) was employed to sample the analogue data at a rate of 50 Hz. An external foot trigger was used to record the beginning and end of each experimental procedure. All recording units were calibrated prior to experimental use. 3.1. Laboratory

2.3.3. Control intervention For the control intervention the subject remained seated and looking forward during the whole recording time in a standardized neutral position. The researcher remained behind the subject, as in the placebo and treatment conditions, but made no contact with the subject.

3. Instrumentation and measurement It has been suggested that stimulation of the SNS results in vasoconstriction of the artero-venous anastomoses within the skin that, in turn, results in a decrease of cutaneous blood flow, leading to a decrease in ST (Darrow, 1933; Venables and Christie, 1973; Harris and Wagnon, 1987; Uncini et al., 1988; Lovick, 1991; Kornberg and McCarthy, 1992; Chiu and Wright, 1996; Nance and Hoy, 1996). Stimulation of the SNS may also result in an increase in sudomotor activity, via the influence of cholinergic sympathetic fibres, which results in an increase in sweat gland activity and a subsequent decrease in skin resistance and associated increase in SC (Edelberg, 1971; Uncini et al., 1988; Andressai, 1995). This sympathoexcitatory response may be a result of the primitive ‘fight or flight’ mechanism whereby blood flow is redirected away from the cutaneous surface to aid muscle contraction, and

Recordings of temperature and humidity were taken before and after each experimental procedure to monitor consistency of these readings. Noise and discussion was kept to a minimum. 3.2. Data analysis All 16 subjects completed the study. Data was divided into three periods for subsequent data analysis: preintervention, during intervention and post-intervention. The mean for each section was determined using data analysis software (Acknowledge version 3.7.1). Data was analysed using the SPSS statistical package (version 11.0). For the experimental study the mean differences of the dependent variables between the intervention period compared with the pre-intervention period (Diff A) and also post-intervention compared with the pre-intervention period (Diff B) were calculated. The data was descriptively explored in order to investigate the assumptions required to use an analysis of variance (ANOVA) statistical test. Normal distribution was confirmed with the use of the Shapiro–Wilk test. Homogeneity of the data was confirmed with use of the Greenhouse Geisser epsilon and Huynh–Feldt epsilon tests of sphericity (Atkinson, 2001). Subsequently a two-way ANOVA with repeated measures and post hoc Bonferroni correction was used to analyse the

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statistical significance of Diff A and Diff B between the independent variables. The factors for the ANOVA were intervention condition (i.e. control, placebo, treatment) and side (left, right). Significance levels were set at Pp0.05 (Altman, 1991; Polgar and Thomas, 2000).

for all experiments and humidity varied by a maximum of 2%. These levels were consistent with guidelines established in previous trials (Uematsu et al., 1988; Kornberg and McCarthy, 1992; Chiu and Wright, 1996). 4.2. Left and right differences

4. Results The results of the data analysis are discussed in the following paragraphs and presented in Tables 1–3 and Figs. 1–4.

There were no statistically significant differences for the dependant variables (ST and SC) between left and right upper limbs for treatment, placebo or control conditions at any phase of the intervention (see Table 1, Figs. 1 and 2).

4.1. Laboratory conditions 4.3. Skin temperature Measures of laboratory temperature and humidity demonstrated consistent readings throughout all experimental conditions. The temperature remained constant

Data analysis indicated a trend suggestive of a decrease in ST for the treatment and placebo conditions

Table 1 Analysis of variance for skin temperature and skin conductance for left and right upper limbs for Diff A and Diff B

Skin temperature Diff A (intervention period compared with pre-intervention period) Diff B (post-intervention period compared with pre-intervention period) Skin conductance Diff A (intervention period compared with pre-intervention period) Diff B (post-intervention period compared with pre-intervention period)

F values

Df

P value

Significant (S) or nonsignificant (NS)

0.217

1

0.648

NS

0.465

1

0.506

NS

3.771

1

0.071

NS

0.855

1

0.370

NS

Significance set at Pp0.05. Table 2 95% confidence intervals (CI) for mean of ST and SC for Diff A and Diff B for each intervention factor Condition

Skin temperature Diff A (intervention period compared with pre-intervention period) Diff B (post-intervention period compared with pre-intervention period) Skin conductance Diff A (intervention period compared with pre-intervention period) Diff B (post-intervention period compared with pre-intervention period)

Mean

SEM

95% CI (lower bound/ upper bound)

Control Placebo Treatment

0.302 0.147 0.107

0.114 0.071 0.072

0.059/0.545 0.004/0.298 0.048/0.261

Control Placebo Treatment

0.587 0.145 0.140

0.244 0.086 0.090

0.068/1.107 0.038/0.329 0.053/0.332

Control Placebo Treatment

0.044 0.080 0.175

0.015 0.052 0.037

0.077/-0.011 0.029/0.190 0.095/0.254

Control Placebo Treatment

0.050 0.032 0.140

0.034 0.011 0.037

0.123/0.022 0.008/0.056 0.061/0.220

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Table 3 ANOVA and post hoc data for ST and SC for Diff A and Diff B for each intervention factor F value

df

2.454 1.261 0.171

1 1 1

0.138 0.279 0.685

NS NS NS

Diff B (post-intervention period compared with pre-intervention period) Treatment versus control 3.333 Placebo versus control 2.751 Treatment versus placebo 0.002

1 1 1

0.088 0.118 0.962

NS NS NS

Skin conductance Diff A (intervention period compared with pre-intervention period) Treatment versus control 30.147 Placebo versus control 7.617 Treatment versus placebo 2.017

1 1 1

o0.0005 0.015 0.176

S S NS

Diff B (post-intervention period compared with pre-intervention period) Treatment versus control 17.887 Placebo versus control 8.415 Treatment versus placebo 8.543

1 1 1

0.001 0.011 0.010

Skin temperature Diff A (intervention period compared with pre-intervention period) Treatment versus control Placebo versus control Treatment versus placebo

P value

Significant (S) or non-significant (NS)

S S S

Significance set at Pp0.05.

compared with the control condition (see Table 2 and Figs. 1 and 3). This trend appeared greatest for the treatment condition and was apparent for both Diff A (intervention phase compared to pre-intervention phase), and Diff B (post-intervention phase compared to pre-intervention phase). However, the decreases in ST did not reach statistically significant levels between independent variables (see Table 3 and Fig. 3). 4.4. Skin conductance Analysis indicated that there was a statistically significant increase in SC for both treatment and placebo conditions when compared with the control group (see Table 3 and Fig. 4). This was significant for Diff A (intervention phase compared to pre-intervention), and Diff B (post-intervention phase compared with pre-intervention). There was also a statistically significant increase in SC for the treatment intervention compared to the placebo condition. However, this was only true for Diff B data, although there also appeared to be a trend suggestive of a greater increase for SC for the treatment condition compared with the placebo condition for Diff A (see Tables 2, 3 and Figs. 2 and 4). 4.5. Post-trial questionnaire Of the 16 subjects surveyed post-experimental procedure, 13 correctly guessed that the SNAG technique was the treatment condition. No subject correctly guessed

the purpose of the study. This corroborated naivety of the subjects to the purpose of the study.

5. Discussion The results of this study appear to have some correlation with similar studies investigating SNS activity and SMT, and appear to have demonstrated that cervical SNAGs performed on the C5/6 intervertebral joint with active right rotation elicited a pattern of generalized sympathoexcitation in the upper limbs which was not specific to side despite the subject rotating their head only to the right. Specifically, there was a statistically significant increase in SC measures for the treatment and placebo conditions when compared to control, both during and after intervention was applied. The treatment condition demonstrated significantly greater increases in SC compared to the placebo condition once the treatment was finished. There also appeared to be a trend for greater increases in SC for the SNAG technique compared to the placebo whilst the SNAG was performed, although this did not reach statistically significant levels. The study also demonstrated a trend for a decrease in ST in placebo and treatment conditions when compared to control, which was not side dependant, however, this did not reach statistically significant levels. In this study, there were no apparent left to right differences. This is consistent with previous research which has, overall, found there to be a generalized

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1

32 31.5 31 30.5 R

L

30 pre

during

post

Skin conductance (µmho)

Skin temperature (degrees Celsius)

220

0.6 0.4 0.2 L

32

31 30.5

pre

Skin temperature (degrees Celsius)

(b)

during

post

Time period (placebo conditions)

0.8 0.6 0.4 0.2 L

31 30.5 R

L

30 during

post

Time period (treatment conditions)

Fig. 1. Mean ST for 16 subjects for both left and right upper limbs and for each intervention. Note: The close relationship of left and right sides throughout all time periods for each intervention. Also, note the downward trend for ST in both placebo and treatment conditions compared with control condition: (a) control condition, (b) placebo condition and (c) treatment condition.

sympathoexcitatory response to SMT which is not side specific. It can be speculated that the generalized sympathoexcitatory response to the SNAG technique found in the current study may indicate that SNAGs contribute to manipulation-induced analgesia via a centrally mediated phenomenon, rather than a local mechanism (Vicenzino et al., 1994; Willett and Toppenberg, 2001; Toppenberg and Simpson, 2001; Sterling et al., 2001), although this needs to be considered in light of the asymptomatic population tested. Studies which have found left to right differences have used unilateral techniques such as an AP mobilization on the glenohumeral joint (Simon et al., 1997) and a unilateral PA on the lumbar spine (Perry, 2002). In the current study,

plac during

plac post

Time period (placebo conditions) 1 0.8 0.6 0.4 0.2 L

R

0 treat pre

(c)

R

0

(b)

31.5

cont post

1

plac pre 32

pre (c)

R

30

Skin conductance (µmho)

31.5

cont during

Time period (control conditions)

(a)

Skin conductance (µmho)

Skin temperature (degrees Celsius)

cont pre

L

R

0

Time period (control conditions)

(a)

0.8

treat during

treat post

Time period (treatment condition)

Fig. 2. Mean SC for 16 subjects for both left and right upper limbs and for each treatment condition. Note: The close relationship of left and right sides throughout all time periods for each intervention. Also note the upward trend for SC, during intervention, in both placebo and treatment conditions compared with control conditions: (a) control condition, (b) placebo condition and (c) treatment condition.

it could be postulated that as the subjects were instructed to rotate their heads to the right a side difference might have occurred. This was not the case. This may be explained by the fact that a central technique was performed. It is possible to speculate that a unilateral SNAG may have yielded different results, and highlights an area for future research. This study’s results are consistent with previous research in that there was a greater response of SC to interventions compared with ST. A number of researchers have identified that ST response to SMT is often of a smaller magnitude and demonstrates inconsistency

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Difference Diff A Diff B

Change in Skin Temperature (degree C)

2.0

1.0

0.0

-1.0 Control

Placebo

Treatment

Condition Fig. 3. Box plots representing change in skin temperature (1C) for Diff A and Diff B for each intervention.

Difference Diff A Diff B

Change in Skin Conductance (µmho)

0.4

0.2

0.0

-0.2

-0.4

Control

Placebo Condition

Treatment

Fig. 4. Box plots representing change in skin conductance (mmho) for Diff A and Diff B for each intervention.

compared to SC (Peterson et al., 1993; Vicenzino et al., 1995; Chiu and Wright, 1996; Sterling et al., 2001). At this point, it is relevant to consider the construct validity of using SC and ST as measures of SNS activity in experiments of this nature, and to review this in light

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of proposed mechanisms of manipulation-induced analgesia. It would appear from the literature that ST is a more sensitive and reliable measure of SNS activity (Kornberg and McCarthy, 1992; Nance and Hoy, 1996; Watson, 2004), whereas SC is prone to variability as it can be affected by psychological and personality factors (Edelberg, 1973; Millington and Wilkinson, 1983; Barabasz, 1985; Borgeat and Boissonneault, 1989; Uncini et al., 1988; Scerbo et al., 1992). Thacker and Gifford (2002) state that SC, on the palms of the hands, is solely controlled by the psycho-emotional centres and may represent only a measure of psycho-emotional drive. Several authors have cautioned the use of SC as a measure of SNS function as it is influenced by numerous control centres within the central nervous system (Edelberg, 1973; Janig, 1990; Holstege, 1991; Scerbo et al., 1992; Andreassai, 1995). This suggests a far more complex response than has been proposed by Wright (1995, 2002) whereby SMT stimulate the dlPAG and descending pain inhibitory pathways, and are reflected in physiological sympathoexcitatory changes of SC and ST. Additionally, there has also been some dispute over spinal connections with the dlPAG. Bandler et al. (2000) suggest that the dlPAG receives no direct spinal or trigeminocervical nucleus input, implying that the dlPAG may be driven by forces other than physical stressors. The implications of this are that there appears to be no direct pathway linking the physical contact involved in SMT and the dlPAG. It can be speculated that if the dlPAG is involved with response to SMT, it may be as a result of the patient/subjects personal interpretation of the situation and the neurophysiological sequalea this may evoke. In light of the current study’s significant results related to SC it is interesting to speculate that SNAGs may have a profound psychological effect on subjects. This concept is not new and there is much published literature on the relationship between psychological factors and musculoskeletal dysfunction (Hoehler and Tobis, 1983; Flor, 1990; Helliwell et al., 1992; Jensen et al., 1994; Gamsa, 1994; Klaber Moffett and Richardson, 1995; Kendall et al., 1997; Vlaeyen and Crombez, 1999; Turk et al., 2000). In relation to ST, although there have been some questions as to the validity of using ST as a measure of the SNS function (Thacker and Gifford, 2002), it would appear that this is a more reliable and valid measure of vasomotor function (Kornberg and McCarthy, 1992; Nance and Hoy, 1996; Watson, 2004). In view of this it is difficult to explain the lack of significant ST changes found in this and other similar studies as it would appear that this outcome is a more valid measure of sympathoexcitation. This may potentially compromise proposed theories relating to sympathoexcitation, SMT and manipulation induced analgesia. However, measures of SC and ST should not be considered in isolation and additional studies utilizing

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measures of mechanical and thermal pain thresholds in addition to SC and ST may reveal more conclusive results. Further to this recent animal studies have begun to shed supplementary light on the complex nature of manipulation induced analgesia and lend support to proposed theories that joint manipulation may produce a non-opioid form of analgesia, mediated by spinal serotonergic and noradrenergic receptors utilizing descending inhibitory pathways, which may involve the PAG and the SNS (Sluka and Wright, 2001; Malisza et al., 2003; Skyba and Wright 2003). The validity of extrapolating this work to human subjects with all their innate complexities is problematic given the sensory and emotional aspects of the pain experience (Merskey et al., 1979; Zusman, 2004). It may be that such a bottom up, positivist approach to research in this area can only provide a limited account of the underlying mechanisms of SMT (Stephenson, 2004). There were some differences between this current study and previous-related research. This study demonstrated no significant difference between placebo and treatment conditions for SC in Diff A period (intervention compared with pre-intervention phases). However, a significant difference for Diff B (post-intervention compared with the pre-intervention phase) was demonstrated. This is in contrast to similar studies which have investigated cervical spine SMT and found consistent SC differences between treatment and placebo across all time periods (Peterson et al., 1993; Vicenzino et al., 1995, 1998a; Sterling et al., 2001; Perry, 2002). The contrasting research findings are interesting to consider in light of a number of factors. In the current study only three SNAGS were performed during the treatment phase for each subject, which is consistent with the standard established by Mulligan for the first time use of the technique (Mulligan, 1999). This resulted in a mean time for technique performance of 22 s (SD ¼ 3.6 s), which was a considerably shorter treatment period than other studies investigating SNS response to cervical SMT (Peterson et al., 1993; Vicenzino et al., 1995, 1998a; Chiu and Wright, 1996; Sterling et al., 2001). Interestingly, several studies have investigated the relationship between ‘dose’ of SMT treatment and SNS activity over time (Vicenzino et al., 1994; Chiu and Wright, 1996; Souvlis et al., 2001). Results suggest that frequency and duration of treatment time has a significant impact on the response of SC and ST. It may be that if more SNAGs had been performed a greater difference between placebo and treatment conditions would have been found across the time phases. In support of this it is important to highlight the apparent trend which was demonstrated during the intervention application suggesting a greater increase in SC for the SNAG group when compared to placebo, although this was not at a significant level (see Fig. 2). This is an area for further research specifically in light of

the fact that there is no experimental evidence indicating the optimum number of Mulligan techniques to be performed in treatment sessions. A second factor that potentially explains the apparent similarity between placebo and treatment conditions may be that the statistical analysis used in this study was not directly comparable to analysis completed by other authors. Previous studies have used data analysis using the maximum SC, minimum ST and area under the curve (AUC) values expressed as percentages of baseline means to illustrate results (Vicenzino et al., 1998a, 1995; Peterson et al., 1993; Chiu and Wright, 1996; Sterling et al., 2001). Unfortunately, this process has been methodologically questioned (Vickers, 2001) and so was not used in this instance. The significant increase in SC over time (i.e. positive for Diff B but not Diff A) for the SNAG intervention, when compared to placebo, suggests that SNAGs may illicit a significant sympathoexcitatory response after the treatment technique has been completed. This is an unexpected finding when viewed alongside one of the main premises of SNAG techniques in the patient population: that they should be immediately pain relieving. If the underlying mechanism of SNAGs was connected with the dlPAG and descending inhibitory pain pathways it is expected that there would have been an immediate sympathoexcitatory response which was greater than placebo. This was not the case and may indicate that there is a multimodal mechanism underlying the mechanism of SNAGs. It is interesting to speculate that SNAGs may illicit their effects via a mixture of psycho-emotional pathways, such as patient interpretation of the treatment procedure and effect on factors such as fear avoidance as well as physiological pathways such as the primitive ‘fight or flight’ response. It may be that the ‘laying on of hands’ (as in the placebo and SNAG intervention) is sufficient to illicit a sympathoexcitatory response greater than control conditions, as this current study demonstrated. However, the movement element of the SNAG technique may be essential to produce a greater increase in this response over time and this may or may not affect the analgesia induced by the technique. However, as the current study was done on asymptomatic subjects the results cannot be extrapolated to the patient population.

6. Conclusion The results of this study add further data to the body of evidence already completed on SMT and their effects on the SNS. The study investigated a technique which has not previously been evaluated and its results suggest that cervical SNAG techniques, performed on naı¨ ve asymptomatic subjects, have a sympathoexcitatory effect as measured indirectly by changes in the SC and

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ST. Similar studies suggest that this response is consistent with the fight or flight response and may be linked with midbrain stimulation and endogenous analgesia. The study has highlighted some of the underlying assumptions used in this theory of manipulation-induced analgesia and questions aspects of its validity. From the current study it is difficult to suggest the precise neurophysiological or psycho-emotional pathway by which SNAGs exhibit their clinical effect. However, it has been demonstrated that SNAGs, in an asymptomatic population, do illicit a sympathoexcitatory response and it can be speculated that this may play a role in their underlying pain relieving mechanism. Further research should extend this work by investigating the effect of a longer treatment time, the response of the SNS to unilateral SNAG techniques as well as investigating a patient population.

References Abbott JH. Effect of mobilization with movement on shoulder impairment and functional limitation: a case report. The Journal of Manual and Manipulative Therapy 1998;6(2):208. Abbott JH. The initial effects of an elbow mobilization with movement technique on grip strength in subjects with lateral epicondylalgia. Manual Therapy 2001;6(3):163–9. Altman DG. Practical statistics for medical research. London: Chapman & Hall; 1991 [Chapters 4, 8, 12 and 15]. Andreassai JL. Psychophysiology: human behaviour and physiological response. 3rd ed. London: Erlbaum; 1995. p. 166–370. [Chapters 9–16]. Atkinson G. Analysis of repeated measurements in physical therapy research. Physical Therapy in Sport 2001;2:194–208. Bandler R, Carrive P, Depaulis A. Emerging principles of organization of the midbrain periaqueductal gray matter. In: Depaulis A, Bandler R, editors. The midbrain periaqueductal gray matter. New York: Plenum Press; 1991. p. 1–8. Bandler R, Keary K, Floyd N, Price J. Central circuits mediating patterned autonomic activity during active versus passive emotional coping. Brain Research Bulletin 2000;53(1):95–104. Barabasz AF. Enhancement of military pilot reliability by hypnosis and psychophysiological monitoring: preliminary in-flight and simulator data. Aviation Space Environment Medicine 1985;56(3):248–50. Borgeat F, Boissonneault J. Psychophysiological responses to subliminal auditory suggestions for activation. Perception Motor Skills 1989;69(3, Part 1):947–53. Chiu TW, Wright A. To compare the effects of different rates of application of a cervical mobilisation technique on sympathetic outflow to the upper limb in normal subjects. Manual Therapy 1996;1(4):198–203. Darrow C. The functional significance of the galvanic skin reflex and perspiration on the backs and palms of hands. Psychological Bulletin 1933;30:712. Edelberg R. Electrical properties of skin. In: Elden HR, editor. Biophysical properties of the skin: a treatise of skin, vol. 1. New York: Wiley-Interscience; 1971. p. 513–50 [Chapter 15]. Edelberg R. Mechanisms for electrodermal adaptations for locomotion, manipulation or defence. Physiological Psychology 1973;5:155–209. Exelby L. The mulligan concept: its application in the management of spinal conditions. Manual Therapy 2002;6(3):178–82.

223

Flor H, Birbaumer N, Turk D. The psychobiology of chronic pain. Advanced Behavioural Research 1990;12:47–84. Folk B. Traumatic thumb injury management using mobilization with movement. Manual Therapy 2001;6(3):178–82. Gamsa A. The role of psychological factors in chronic pain: a half century of study. Pain 1994;57:5–15. Genno H, Ishikawa K, Kambara O, Kikumoto M, Fujiwara Y, Suzuki R, et al. Using facial skin temperature, to objectively evaluate sensation. International Journal of Industrial Ergonomics 1997;19:161–71. Grieve G. Contra-indications to spinal manipulation and allied treatments. Physiotherapy 1989;75(8):445–53. Harris W, Wagnon RJ. The effects of chiropractic adjustments on distal skin temperature. Journal of Manipulative and Physical Therapy 1987;10(2):57–60. Hearn A, Rivett DA. Cervical SNAGs: a biomechanical analysis. Manual Therapy 2002;7(2):71–9. Helliwell PS, Mumford DB, Smeathers JE, Wright V. Work related upper limb disorder: the relationship between pain, cumulative load, disability, and psychological factors. Annuals of the Rheumatic Diseases 1992;51:1325–9. Hoehler FK, Tobis JS. Psychological factors in the treatment of back pain by spinal manipulation. British Journal of Rheumatology 1983;22:206–12. Holstege G. Descending pathways from the periaqueductal gray and adjacent areas. In: Depaulis A, Bandler R, editors. The midbrain periaqueductal gray matter. New York: Plenum Press; 1991. p. 239–65. Horton SJ. Acute locked thoracic spine: treatment with a SNAG. Manual Therapy 2002;7(2):103–7. Hsieh CY, Vicenzino B, Yang CH, Hu MH, Yang C. Mulligan’s mobilization with movement for the thumb: a single case report using magnetic resonance imaging to evaluate the positional fault hypothesis. Manual Therapy 2002;7(1):44–9. Janig W. The sympathetic nervous system in pain: physiology and pathophysiology. In: Stanton Hicks M, editor. Current management of pain. Boston: Kluwer Academic Press; 1990 [Chapter 2]. Jensen MP, Turner JA, Romano JM, Lawler BK. Relationship of pain-specific beliefs to chronic pain adjustment. Pain 1994;5:301–9. Jull G, Bogduk N, Marshland A. The accuracy of manual diagnosis for the cervical zygoapophyseal joint pain syndrome. The Medical Journal of Australia 1997;148(7):233–6. Kendall NAS, Linton SJ, Main CJ. Guide to assessing psychosocial flags in acute low back pain: risk factors for long term disability and work loss. Accident Rehabilitation and Compensation Insurance Corporation of New Zealand and the National Health Committee, Wellington, New Zealand, 1997. Klaber Moffett JA, Richardson PH. The influence of psychological variables on the development and perception of musculoskeletal pain. Physiotherapy Theory and Practice 1995;11:1–11. Kochar M, Dogra A. Effectiveness of a specific physiotherapy regimen on patients with tennis elbow. Physiotherapy 2002;88(6):333–41. Konstantinou K, Foster N, Rushton A, Baxter D. The use and reported effects on mobilization with movement techniques in low back pain management; a cross sectional descriptive survey of physiotherapists. Manual Therapy 2002;7(4):206–14. Kornberg C, McCarthy T. The effect of neural stretching technique on sympathetic outflow to the lower limbs. Journal of Orthopaedic and Sports Physical Therapy 1992;16(6):269–74. Lovick T. Interactions between descending pathways from the dorsal and ventrolateral periaqueductal gray matter in the rat. In: Depaulis A, Bandler R, editors. The midbrain periaqueductal gray matter. New York: Plenum Press; 1991. p. 101–20. Malisza KL, Gregorash L, Turner A, Foniok T, Stroman PW, Allman A, et al. Functional MRI involving painful stimulation of the ankle

ARTICLE IN PRESS 224

A. Moulson, T. Watson / Manual Therapy 11 (2006) 214–224

and the effect of physiotherapy joint mobilization. Magnetic Resonance Imaging 2003;21:489–96. McGuiness J, Vicenzino B, Wright A. Influence of a cervical mobilisation technique on respiratory and cardiovascular function. Manual Therapy 1997;2(4):216–20. McKenzie AM, Taylor NF. Can physiotherapists locate lumbar spinal levels by palpation. Australian Journal of Physiotherapy 1997;83(5):235–8. Merskey R, Albe-Fessard DG, Bonica JJ. Pain terms: a list with definitions and notes on usage. Pain 1979;6:249–52. Millington PF, Wilkinson R. Skin. Cambridge: Cambridge University Press; 1983. p. 127–42 [Chapter 5]. Mulligan BR. Manual therapy, NAGS, SNAGS, MWMs etc. 4th ed. Wellington: Hutcheson Bowman and Stewart Ltd; 1999. p. 13–6, 44. Nance PW, Hoy CSG. Assessment of the autonomic nervous system. Physical Medicine and Rehabilitation: State of the Art Reviews 1996;10(1):15–35. Paungmali A, O’Leary S, Souvlis T, Vicenzino B. Hypoalgesic and sympathoexcitatory effects of mobilization with movement for lateral epicondylalgia. Physical Therapy 2003;83(4):374–83. Perry J. Effects of unilaterally applied lumbar mobilisation technique on peripheral sympathetic activity in the lower limbs. Physiotherapy 2002;88(7):436. Peterson N, Vicenzino B, Wright A. The effects of a cervical mobilisation technique on sympathetic outflow to the upper limb in normal subjects. Physiotherapy Theory and Practice 1993;9:149–56. Polgar S, Thomas SA. Introduction to Research in the Health sciences. 4th ed. Edinburgh: Churchill Livingstone; 2000. p. 225–39 [Chapter 18]. Scerbo AS, Freedman LW, Raine A, Dawson ME. A major effect of recording site on measurement of electrodermal activity. Psychophysiology 1992;29(2):241–6. Simon R, Vicenzino B, Wright A. The influence of an anteroposterior accessory glide of the glenohumeral joint on measures of peripheral sympathetic nervous system function in the upper limb. Manual Therapy 1997;2(1):18–23. Sims J, Wright C. Research in healthcare. Cheltenham: Stanley Thomas; 2000. Skyba DA, Radhakrishnan R, Rohling JJ, Wright A, Sluka KA. Joint manipulation reduces hyperalgesia by activation of monoamine receptors but not opioid or GABA receptors in the spinal cord. Pain 2003;106:159–68. Slater H, Wright A. An investigation of the physiological effects of the sympathetic slump on peripheral sympathetic function in patients with frozen shoulder. In: Shacklock MO, editor. Moving in on pain. Sydney: Butterworth-Heinemann; 1995. p. 174–84. Sluka KA, Wright A. Knee joint mobilization reduces secondary mechanical hyperalgesia induced by capsaicin injection into the ankle joint. European Journal of Pain 2001;5:81–7. Souvlis T, Vicenzino B, Wright A. Dose of spinal manual therapy influences changes in sympathetic nervous system function. Twelfth Biennial Conference of Musculoskeletal Physiotherapy, Adelaide, Australia, 2001. p. 35. Stephenson R. Discussion paper: attending to pain: ‘mechanisms of musculoskeletal physiotherapy’. Physical Therapy Reviews 2004;9:65–7. Sterling M, Jull G, Wright A. Cervical mobilisation: concurrent effects on pain, sympathetic nervous system activity and motor activity. Manual Therapy 2001;6(2):72–81. Thacker M, Gifford, L. A review of physiotherapy management of complex regional pain syndrome. In: Gifford, L, editor. Topical issues in pain, vol. 3. Falmouth: CNS Press; 2002. p. 119–41 [Chapter 5]. Toppenberg RMK, Simpson G. A comparison of sympathoexcitation and hypoalgesia produced by two cervical mobilisation techniques

at C5/6. Twelfth Biennial Conference of Musculoskeletal Physiotherapy, Adelaide, Australia, 2001. p. 37. Turk DC, Okifuji A, Sherman JJ. Psychologic aspects of back pain: implications for physical therapists. In: Twomey LT, Taylor JR, editors. Physical therapy of the low back. 3rd ed. Philadelphia: Churchill Livingstone; 2000. [Chapter 13]. Uematsu S, Edwin DH, Jankel WR, Kozokowski J, Trattner M. Quantification of thermal symmetry: part 1: normal values and reproducibility. Journal of Neurosurgery 1988;69:552–5. Uncini A, Pulman SL, Lovelace RE, Gambi D. The sympathetic skin response: normal values, elucidation of afferent components and application limits. Journal of Neurological Science 1988;87:299– 306. Venables P, Christie M. Mechanism, instrumentation, recording techniques and quantification of responses. In: Prokasy WF, Raskin DC, editors. Electrodermal activity in psychological research. New York: Academic Press; 1973. p. 2–6. Vicenzino B, Collins D, Wright A. Sudomotor changes induced by neural mobilisation techniques in asymptomatic subjects. The Journal of Manual and Manipulative Therapy 1994;2(2):66–74. Vicenzino B, Gutschlag F, Collins D, Wright A. An investigation of the effects of spinal manual therapy on forequarter pressure and thermal pain thresholds and sympathetic nervous system activity in asymptomatic subjects: a preliminary report. In: Shacklock MO, editor. Moving in on pain. Sydney: Butterworth-Heinemann; 1995. p. 185–93. Vicenzino B, Collin D, Benson H, Wright A. An investigation of the interrelationship between manipulative therapy-induced hypoalgesia and sympathoexcitation. Journal of Manipulative and Physiological Therapeutics 1998a;21(7):448–53. Vicenzino B, Cartwright T, Collins D, Wright A. Cardiovascular and respiratory changes produced by lateral glide mobilization of the cervical spine. Manual Therapy 1998b;3(2):67–71. Vicenzino B, Paungmali A, Buratowski S, Wright A. Specific manipulative therapy treatment for chronic lateral epicondylalgia produces uniquely characteristic hypoalgesia. Manual Therapy 2001;6(4):205–12. Vickers AJ. The use of percentage change from baseline as an outcome in a controlled trial is statistically inefficient: a simulation study. Medical Research Methodology 2001;1(1):6–12. Vlaeyen JWS, Crombez G. Fear of movement/(re)injury, avoidance and pain disability in chronic low back pain patients. Manual Therapy 1999;4(4):187–95. Watson T. Personal communication, 2004. Willett KA, Toppenberg RMK. Effects of lumbar mobilisation on sympathetic outflow to the lower limbs. MPA 12th Biennial Conference of Musculoskeletal Physiotherapy, Adelaide, Australia, 2001. p. 41. Wilson E. Mobilisation with movement and adverse neural tension: an exploration of possible links. Manipulative Association of Chartered Physiotherapists Journal 1995;27(1):40–6. Winter BT, Brown DR, Michels KM. Statistical principles in experimental design. 3rd ed. New York: McGraw-Hill; 1991. [Chapter 4]. Wright A. Hypoalgesia post-manipulative therapy: a review of a potential neurophysiological mechanism. Manual Therapy 1995;1:11–6. Wright A, Vicenzino B. Cervical mobilisation techniques, sympathetic nervous system effects and their relationship to analgesia. In: Shacklock MO, editor. Moving in on pain. Sydney: ButterworthHeinemann; 1995. p. 164–73. Wright A. Pain relieving effects of cervical manual therapy. In: Grant R, editor. Physical therapy of the cervical and thoracic spine. New York: Churchill Livingstone; 2002. p. 217–38 [Chapter 12]. Zusman M. Mechanisms of musculoskeletal physiotherapy. Physical Therapy Reviews 2004;9:39–49.

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Manual Therapy 11 (2006) 225–230 www.elsevier.com/locate/math

Original article

Myofascial trigger points in the suboccipital muscles in episodic tension-type headache Ce´sar Ferna´ndez-de-las-Pen˜asa,b,, Cristina Alonso-Blancoa, Maria Luz Cuadradob,c, Juan A. Parejab,c a

Department of Physical Therapy, Occupational Therapy, Physical Medicine and Rehabilitation of Universidad Rey Juan Carlos, Alcorco´n, Madrid, Spain b Esthesiology Laboratory of Universidad Rey Juan Carlos, Alcorco´n, Madrid, Spain c Department of Neurology of Fundacio´n Hospital Alcorco´n and Universidad Rey Juan Carlos, Alcorco´n, Madrid, Spain

Abstract Referred pain evoked by suboccipital muscle trigger points (TrPs) spreads to the side of the head over the occipital and temporal bones and is usually perceived as bilateral headache. This paper describes the presence of referred pain from suboccipital muscle TrPs in subjects with episodic tension-type headache (ETTH) and in healthy controls. Ten patients presenting with ETTH and 10 matched controls without headache were examined by a blinded assessor for the presence of suboccipital muscle TrPs. Diagnostic criteria described by Simons and Gerwin were adapted to diagnose TrPs, i.e. presence of tenderness in the suboccipital region, referred pain evoked by maintained pressure for 10 s, and increased referred pain on muscle contraction. Six ETTH patients (60%) had active TrPs and 4 had latent TrPs (40%). On the other hand, 2 control subjects also had latent TrPs. Differences in the presence of suboccipital muscle TrPs between both groups were significant for active TrPs (Po0:001), but not for latent TrPs. Active TrPs were only present in ETTH patients, although TrP activity was not related to any clinical variable concerning the intensity and the temporal profile of headache. Myofascial TrPs in the suboccipital muscles might contribute to the origin and/or maintenance of headache, but a comprehensive knowledge of the role of these muscles in tension-type headache awaits further research. r 2006 Elsevier Ltd. All rights reserved. Keywords: Tension-type headache; Myofascial trigger points; Suboccipital muscles; Referred pain

1. Background Headache disorders are one of the most common problems seen in medical practice. Among the many types of headache disorders, tension-type headache (TTH) is the most frequent in adults. Population-based studies suggest 1-year prevalence rates of 38.3% for episodic TTH, and 2.2% for chronic TTH (Schwartz et al., 1998). TTH is considered to be the prototype of headache with myofascial tissues playing an important Corresponding author. Facultad de Ciencias de la Salud, Universidad Rey Juan Carlos, Avenida de Atenas s/n, 28922 Alcorco´n, Madrid, Spain. Tel.: +34 91 488 88 84; fax: +34 91 488 89 57. E-mail addresses: [email protected], [email protected] (C. Ferna´ndez-de-las-Pen˜as).

1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.07.003

role (Jensen and Olesen, 1996). Gerwin (2005) and Jensen (1999) have claimed that pain from pericranial head; neck and shoulder muscles might be referred to the head, and be experienced as headache. Simons et al. (1999) described the referred pain patterns from different myofascial trigger points (TrPs) in head and neck muscles, which produced pain features that are usually found in subjects presenting with TTH. Simons et al. (1999) define a TrP as a hyperirritable spot associated with a taut band of a skeletal muscle that is painful on compression, palpation and/or stretch, and that usually gives rise to a typical referred pain pattern. Active TrPs are cause of clinical symptoms, i.e. spontaneous referred pain and restricted motion of the affected tissues, whereas latent TrPs may not be an immediate source of pain, but might produce other muscle dysfunctions such as fatigue

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and restricted range of motion (Simons et al., 1999). This clinical distinction has been strongly substantiated by histochemical findings, since higher levels of concentration of bradykinin, calcitonin gene-related peptide, substance P, tumour necrosis factor-a, interleukin-1b, serotonin and norepinephrine have been recently found in active TrPs (Shah et al., 2005). TTH is characterized by bilateral, pressing and tightening head pain, of mild-to-moderate intensity, that is not aggravated during routine physical activity. In the episodic form, patients suffer from headache less than 15 days per month, whereas in the chronic form patients experience headache at least 15 days per month (IHS, 2004). Some characteristics of TTH, such as pressure or band-like tightness (IHS, 1988, 2004), and increased tenderness on palpation of neck and shoulder muscles (Jensen and Olesen, 1996; Lipchik et al. 1997), resemble the descriptions of referred pain originating in TrPs (Simons et al. 1999). Marcus et al. (1999) found that subjects suffering from TTH showed a greater number of either active or latent TrPs in different muscles than healthy subjects. On the other hand, we have already found that TTH subjects, either chronic or episodic, show a greater number of TrPs in the superior oblique muscle than controls (Ferna´ndez-de-las-Pen˜as et al., 2005). Therefore, it seems plausible that TrPs might play an important role in the genesis of TTH. Within the cervical musculature, suboccipital muscles can develop TrPs, accounting for a referred pain pattern that spreads to the side of the head over the occipital and temporal bones (Fig. 1). This referred pain extends to both sides, thus being perceived as bilateral headache (Simons et al., 1999). In a series of patients with chronic TTH (CTTH), our research group recently demonstrated that this disorder was associated with suboccipital active TrPs and forward head posture, and that those CTTH subjects with active TrPs had greater headache intensity and frequency than those with latent TrPs (Ferna´ndez-de-lasPen˜as et al., 2006). Moreover, we have previously found that the management of suboccipital muscle TrPs may produce significant pain relief in subjects presenting with episodic TTH (ETTH) (Ferna´ndez-de-las-Pen˜as et al., 2004). After such early observations, we have extended our former study in CTTH subjects (Ferna´ndez-de-las-Pen˜as et al., 2006) to subjects suffering from ETTH. This paper describes the presence of referred pain stemming from suboccipital muscle TrPs in subjects with ETTH and in healthy control subjects.

Fig. 1. Referred pain from myofascial trigger points in the suboccipital muscles (rectus capitis posterior minor and major muscles). Adapted from Simons DG, Travell JG, Simons LS. Travell and Simons’ Myofascial Pain and dysfunction: The trigger point manual. Volume 1: upper half of the body. (2nd edition) Ed Baltimore: Williams & Wilkins, 1999. Fig. 17.1 (p. 473).

2. Material and methods

subjects without headache during the previous year participated in this study from June to November of 2004. Patients were recruited from the Neurology Department of Fundacio´n Hospital Alcorco´n, whereas controls were recruited from the hospital staff. Patients with ETTH were diagnosed according to the criteria of the International Headache Society (IHS) by an experienced neurologist (IHS, 2004). ETTH patients had to have headache less than 15 days per month. A headache diary was kept for 4 weeks in order to substantiate the diagnosis (Russell et al., 1992). The health status of all participants was clinically stable, without current symptoms of any other concomitant disease. This study was supervised by the Departments of Physical Therapy and Neurology of Rey Juan Carlos University and Fundacio´n Hospital Alcorco´n, and it was also approved by the local human research Committee. All subjects signed an informed consent prior to their inclusion.

2.1. Subjects

2.2. Myofascial trigger point examination

Ten patients presenting with episodic tension-type headache (ETTH) and 10 healthy age- and sex-matched

TrPs were sought in the suboccipital muscles by an assessor who had more than 4 years’ experience in TrPs

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diagnosis, and who was also blinded to the subjects’ condition. Diagnostic criteria as described by Simons et al. (1999) and by Gerwin et al. (1997) were adapted for the suboccipital muscles and used to diagnose TrPs. These modified criteria have been employed in previous studies (Ferna´ndez-de-las-Pen˜as et al., 2005, 2006). Specifically, the TrP diagnosis was made when there was tenderness in the suboccipital region; referred pain evoked by maintained pressure for 10 s (Fig. 1), and increased referred pain on muscle contraction, i.e. active extension of the upper cervical spine. The suboccipital muscles that extend the neck at the occipital–atlas junction (rectus capitis posterior major and minor, and the oblique capitis superior) are not directly palpable. To evaluate the effect of muscle contraction on referred pain intensity, subjects lay supine with the cervical spine in a neutral position. The assessor palpated the suboccipital region, that is, the anatomical projection of the rectus capitis posterior major and minor muscles between the posterior arch of the atlas and the occiput bone (Fig. 2), for 10 s. If referred pain was evoked upon compression, subjects were asked to extend the neck. This movement produced a palpable contraction of the most superficial posterior cervical muscles, and conceivably a contraction of the suboccipital muscles, that are not directly palpable. Subjects were asked to keep the neck straight and only extend at the cervical– occipital junction, to focus the contraction on both rectus capitis posterior muscles. The assumption that the suboccipital muscles were involved during the exploration was based on the characteristic referred pain pattern of these muscles (Fig. 1), in contrast to the referred pain patterns characteristic of other posterior cervical muscles. TrPs were considered active if the subject recognized the evoked referred pain as familiar, i.e. if it reproduced the pain that he or she perceived during spontaneous headache attacks; conversely, TrPs were considered latent if the subject did not recognize the evoked referred pain as a familiar pain (Simons et al., 1999; Gerwin et al., 1997). Since referred pain from suboccipital muscle TrPs is elicited bilaterally (Simons et al., 1999), we did not classify TrPs as either right or left. Then, we considered the presence of a unique TrP if manual palpation of suboccipital muscles evoked bilateral referred pain (Simons et al., 1999; Gerwin, 2005; Ferna´ndez-de-las-Pen˜as et al., 2006). 2.3. Study protocol All subjects had to be headache-free on the day of the examination. A first assessor gave a headache diary to ETTH patients. Patients had to register on this diary the daily headache intensity, on a 10-cm horizontal visual analogue scale (VAS; range: 0 ¼ no pain, to 10 ¼ maximum pain) (Jensen et al., 1999), the headache

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Fig. 2. Topography of the rectus capitis posterior minor (RCPmin) and major (RCPmaj) muscles.

duration (in hours per day), and the days with headache. This headache diary was kept for 4 weeks. This assessor also informed control subjects about physical therapy and headache (health education), but did not give them a headache diary. A second assessor, blinded to the subjects’ condition, examined the suboccipital muscles for the presence of TrPs. Four weeks later, ETTH subjects returned the headache diary to the first assessor, who calculated the following variables: 1, headache intensity, which was calculated from the mean of the VAS of the days with headache; 2, headache frequency, which was calculated dividing the number of days with headache by 4 weeks (days per week); and 3, headache duration, which was calculated dividing the sum of the total hours of headache by the number of days with headache (hours per day). 2.4. Statistical analysis Data were analysed with the SPSS statistical package (12.0 Version). The Kolmogorov–Smirnov test showed a

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normal distribution of the quantitative outcomes. The chi-square (w2) test was used to compare the presence of either latent or active TrPs between both study groups. The unpaired t-test was used to analyse the differences in the clinical variables relating to headache (headache intensity, frequency and/or duration) between ETTH subjects with either latent or active TrPs. The statistical analysis was conducted at a 95% confidence level. A Pvalue less than 0.05 was considered statistically significant.

4. Discussion All patients presenting with ETTH in this series had suboccipital muscle TrPs, either active or latent. The referred pain evoked by suboccipital TrPs reproduced usual headache in 6 (60%) of them, which was consistent with active TrPs, while the remaining 4 (40%) had latent TrPs. Within the control group, no one had active TrPs, but 2 healthy subjects (20%) had latent TrPs. Therefore, both groups had latent TrPs, while active TrPs were only present in the ETTH group. Our results are in agreement with Chaiamnuay et al. (1998), who also observed some latent TrPs in healthy subjects. On the other hand, current findings in ETTH subjects complete our previous findings for subjects with the chronic form of TTH (CTTH), in whom, suboccipital muscle TrPs were also more common than in healthy controls (Ferna´ndez-de-las-Pen˜as et al., 2006). However, in CTTH patients the presence of active TrPs was related to greater headache intensity and greater headache frequency than the presence of latent TrPs. These latter results have not been replicated in this study, since none of the clinical variables concerning the intensity and the temporal profile of headache differed with TrP activity in our group of ETTH patients (Table 2). Previous (Ferna´ndez-de-las-Pen˜as et al., 2006) and current findings support the hypothesis that suboccipital muscle TrPs might play an important role in the genesis of TTH, either episodic or chronic. Bendtsen (2000) reported that both peripheral mechanisms, i.e.

3. Results A total of 10 ETTH patients, 2 men and 8 women, aged 18–66 years old, and 10 healthy volunteers, 3 men and 7 women, aged 18–66 years old, were studied. No significant differences were found for gender or age between both study groups. ETTH subjects were headache-free on the day of the evaluation. Demographic and clinical data of each group are given in Table 1. All ETTH patients showed TrPs in the suboccipital muscles. Six of them (60%) had active TrPs, whereas the remaining 4 (40%) had latent TrPs. On the other hand, 2 (20%) control subjects had latent TrPs. Differences in the presence of suboccipital muscle TrPs between both groups were significant for active TrPs (Po0:001), but not for latent TrPs. Within the ETTH group, headache intensity, frequency and duration outcomes did not differ depending on TrP activity, whether the TrPs were active or latent (Table 2).

Table 1 Demographic and clinical data of both groups

Gender (male/female) Age (years) Length of headache history (years) Headache intensity (VAS) Headache frequency (days/week) Headache duration (hours per headache day)

ETTH (n ¼ 10)

Controls (n ¼ 10)

P-value

2/8 35715 5.573.5 4.371.5 2.970.5 572.7

3/7 34713 — — — —

NS NS — — — —

Values are expressed as mean7SD. ETTH ¼ episodic tension-type headache. VAS ¼ Visual Analogue Scale (0–10). NS ¼ Non-significant.

Table 2 Headache intensity, frequency and duration depending on the activity of suboccipital muscle trigger points

Active TrPs (n ¼ 6) Latent TrPs (n ¼ 4)

Headache intensity (VAS)

Headache frequency (days/week)

Headache duration (hours/day)

4.871.4 3.671.4

2.970.5 370.5

4.273.4 6.370.4

Values are expressed as mean7SD. VAS ¼ Visual Analogue Scale (0–10). TrPs ¼ Myofascial trigger points.  Non-significant in comparison with the latent TrP subgroup (unpaired t-test, Po0:05).

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myofascial tenderness of pericranial structures, and central mechanisms, i.e. sensitization of supraspinal neurones and decreased anti-nociceptive activity from supraspinal structures, might be involved in the pathogenesis of TTH. These phenomena could be interconnected, since continuous or prolonged nociceptive inputs from myofascial tissues may contribute to the central sensitization in CTTH (Jensen, 1999). Nociceptive inputs from suboccipital muscle TrPs may produce a continuous afferent bombardment to the trigeminal nerve nucleus caudalis. Such repeated nociceptive activation of the nucleus caudalis could produce central sensitization in CTTH (Bendtsen, 2000). If there were a lesser degree of central sensitization in ETTH, because of the intermittent nature of this condition, one would expect fewer active and more latent TrPs in ETTH subjects than in CTTH subjects. Our findings do not support this hypothesis, as suboccipital active TrPs were present in a similar proportion in both ETTH subjects (60%) and CTTH subjects (65%). However, headache intensity and frequency were related to TrPs activity in CTTH (Ferna´ndez-de-las-Pen˜as et al., 2006), but not in ETTH. Since TrPs are responsible for the liberation of nociceptive mediators (Shah et al., 2005), it seems plausible that TrP activity originated in the suboccipital muscles might be a triggering factor for central sensitization seen in chronic headaches. In such way, the presence of TrPs could contribute to the evolution of the episodic form to the chronic form of TTH. There are some limitations to our studies. First, only subjects with TTH have been evaluated. Hence, our results cannot be extrapolated to other headache disorders. It would be interesting to repeat the same procedure with patients suffering from other disorders in order to explore the relevance of suboccipital muscle TrPs in headache. The second limitation was the sample size. To our knowledge, our studies are the first ones to analyse the relationship between suboccipital muscle TrPs and clinical features in TTH. However, it would be necessary to repeat the same procedure with a greater number of subjects so as to confirm our findings in both ETTH and CTTH patients. Third, it is possible that other structures of the upper cervical region, e.g. atlanto-axial joint or C2 nerve trunk, could be palpated during the exploration and then responsible for the perceived referred pain. However, our palpation was done next to the occipital bone (Fig. 2), so the possibility to palpate these structures was minimal. Moreover, since muscle contraction increased referred pain in all patients, it is most likely that the elicited referred pain was originated in the muscle tissue, that is, in the suboccipital muscles. 5. Conclusions Active myofascial TrPs in the suboccipital muscles were more common in ETTH subjects than in healthy

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controls, although TrP activity was not related to any clinical variable concerning the intensity and the temporal profile of headache. Suboccipital TrPs might contribute to the origin and/or maintenance of headache, but a comprehensive knowledge of the role of these muscles in TTH awaits further research.

Acknowledgements We would like to thank Dr. David Simons and Dr. Robert D. Gerwin for their kind encouragement and support.

References Bendtsen L. Central sensitization in tension-type headache: possible patho-physiological mechanisms. Cephalalgia 2000;29: 486–508. Chaiamnuay P, Darmawan J, Muirden KD, Assawatanabodee P. Epidemiology of rheumatic disease in rural Thailand: a WHOILAR COPCORD study. Community Oriented Programme for the Control of the Rheumatic Disease. Journal of Rheumatology 1998;25:1382–7. Ferna´ndez-de-las-Pen˜as C, Alonso-Blanco C, Cuadrado ML, Pareja JA, Barriga FJ, Miangolarra JC. Adverse tension in cranial dura mater and Myofascial trigger points in suboccipital muscles in patients with episodic tension type headache. Journal of Musculoskeletal Pain 2004;12(Suppl 9):75 (abstract). Ferna´ndez-de-las-Pen˜as C, Cuadrado ML, Gerwin RD, Pareja JA. Referred pain from the trochlear region in tension-type headache: a Myofascial trigger point from the superior oblique muscle. Headache 2005;45:731–7. Ferna´ndez-de-las-Pen˜as C, Alonso-Blanco C, Cuadrado ML, Gerwin RD, Pareja JA. Trigger points in the suboccipital muscles and forward head posture in chronic tension type headache. Headache 2006;46:454–60. Gerwin R. Headache. In: Ferguson L, Gerwin R, editors. Clinical mastery in the treatment of myofascial pain. Philadelphia: Lippincott Williams & Wilkins; 2005. p. 1–24. Gerwin RD, Shanon S, Hong CZ, Hubbard D, Gevirtz R. Interrater reliability in myofascial trigger point examination. Pain 1997;69: 65–73. IHS: Headache Classification Committee of the International Headache Society. Classification and diagnostic criteria for headache disorders, cranial neuralgias and facial pain—1st edition. Cephalalgia 1988;8(Suppl 7):29–34. IHS: Headache Classification Subcommittee of the International Headache Society. The International Classification of Headache Disorders–2nd edition. Cephalalgia 2004;24(Suppl 1):9–160. Jensen R. Pathophysiological mechanism of tension-type headache: a review of epidemiological and experimental studies. Cephalalgia 1999;19:602–21. Jensen R, Olesen J. Initiating mechanism of experimentally induced tension-type headache. Cephalalgia 1996;16:175–82. Jensen MP, Turbner JA, Romano JM, Fisher L. Comparative reliability and validity of chronic pain intensity measures. Pain 1999;83:157–62. Lipchik GL, Holroyd KA, Talbot F, Greer M. Pericranial muscle tenderness and exteroceptive suppression of temporalis muscle activity: a blind study of chronic tension-type headache. Headache 1997;37:368–76.

ARTICLE IN PRESS 230

C. Ferna´ndez-de-las-Pen˜as et al. / Manual Therapy 11 (2006) 225–230

Marcus DA, Scharff L, Mercer S, Turk DC. Musculoskeletal abnormalities in chronic headache: a controlled comparison of headache diagnostic groups. Headache 1999;39:21–7. Russell MB, Rasmussen BK, Brennum J, Iversen HK, Jensen RA, Olesen J. Presentation of a new instrument: the diagnostic headache diary. Cephalalgia 1992;12:369–74. Schwartz BS, Stewart WF, Simon D, et al. Epidemiology of tensiontype headache. Journal of the American Medical Association 1998;279:381–3.

Shah JP, Phillips TM, Danoff JV, Gerber LH. An in vitro microanalytical technique for measuring the local biochemical milieu of human skeletal muscle. Journal of Applied Physiology 2005;99:1977–84. Simons DG, Travell J, Simons LS. Myofascial pain and dysfunction: the trigger point manual: vol. 1. 2nd ed. Baltimore: Williams & Wilkins; 1999.

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Manual Therapy 11 (2006) 231–237 www.elsevier.com/locate/math

Original article

Pathological muscle activation patterns in patients with massive rotator cuff tears, with and without subacromial anaesthetics F. Steenbrinka,b,, J.H. de Grootc, H.E.J. Veegerb, C.G.M. Meskersc, M.A.J. van de Sandea, P.M. Rozinga a Department of Orthopaedics, Leiden University Medical Centre, The Netherlands Department of Human Movement Sciences, Vrije Universiteit Amsterdam, The Netherlands c Department of Rehabilitation Medicine, Leiden University Medical Centre, The Netherlands b

Received 4 November 2005; received in revised form 25 May 2006; accepted 3 July 2006

Abstract A mechanical deficit due to a massive rotator cuff tear is generally concurrent to a pain-induced decrease of maximum arm elevation and peak elevation torque. The purpose of this study was to measure shoulder muscle coordination in patients with massive cuff tears, including the effect of subacromial pain suppression. Ten patients, with MRI-proven cuff tears, performed an isometric force task in which they were asked to exert a force in 24 equidistant intervals in a plane perpendicular to the humerus. By means of bi-polar surface electromyography (EMG) the direction of the maximal muscle activation or principal action of six muscles, as well as the external force, were identified prior to, and after subacromial pain suppression. Subacromial lidocaine injection led to a significant reduction of pain and a significant increase in exerted arm force. Prior to the pain suppression, we observed an activation pattern of the arm adductors (pectoralis major pars clavicularis and/or latissimus dorsi and/or teres major) during abduction force delivery in eight patients. In these eight patients, adductor activation was different from the normal adductor activation pattern. Five out of these eight restored this aberrant activity (partly) in one or more adductor muscles after subacromial lidocaine injection. Absence of glenoid directed forces of the supraspinate muscle and compensation for the lost supraspinate abduction torque by the deltoideus leads to destabilizating forces in the glenohumeral joint, with subsequent upward translation of the humeral head and pain. In order to reduce the superior translation force, arm adductors will be co-activated at the cost of arm force and abduction torque. Pain seems to be the key factor in this (avoidance) mechanism, explaining the observed limitations in arm force and limitations in maximum arm elevation in patients suffering subacromial pathologies. Masking this pain may further deteriorate the subacromial tissues as a result of proximal migration of the humeral head and subsequent impingement of subacromial tissues. r 2006 Elsevier Ltd. All rights reserved. Keywords: Shoulder; Muscle; Coordination; Rotator cuff; Tear; Electromyography; Principal action; Pain

1. Introduction Muscle activation patterns (coordination) are bound to change after mechanical deficits like massive rotator cuff tears. Subacromial injection with lidocaine reduces Corresponding author. Department of Orthopaedics, Leiden University Medical Centre, The Netherlands. E-mail address: [email protected] (F. Steenbrink).

1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2006.07.004

pain and has been shown to coincide with an increase in active forward flexion and muscle strength in patients with specific subacromial disorders like impingement (Ben Yishay et al., 1994). In a comparable intervention it was found that patients with massive rotator cuff tears were well capable of arm abduction despite the absence of supraspinatus force, but were actively hampered to do so due to pain (van de Sande et al., 2006; de Groot

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et al., 2006). Their findings also showed that supraspinatus muscle force was not per se required to produce the necessary glenohumeral abduction torque. Both series used active and isometric loading by a constant force in a direction rotating perpendicular around the longitudinal axis of the humerus. This socalled principal action method made it possible to define the direction of maximum muscle activation, in combination with the additional compensating muscle activity needed to produce force in exactly that direction (Flanders and Soechting, 1990; Arwert et al., 1997; de Groot et al., 2004; Meskers et al., 2004). The principal action method quantifies shoulder muscle contributions during an isometric force task and facilitates the analysis of the activation patterns of shoulder muscles. This study was set up to analyse shoulder muscle coordination using the principal action method in patients with massive cuff tears. We analysed activation patterns prior to and after subacromial anaesthetics. In addition to de Groot et al. (2006) we addressed more muscles in order to explain the observed enhancement of external arm force, viz.; the deltoideus (three parts), the latissimus dorsi, the pectoralis major pars clavicularis and the teres major.

2. Methods 2.1. Subjects Six male and four female patients (Table 1) with an average age of 61 years (SD ¼ 8) with MRI-proven massive rotator cuff tears were included in the study. All patients were informed and signed informed consent. 2.2. Procedure The principal muscle activation patterns of six muscles were recorded as described by de Groot et al. (2004), and Meskers et al. (2004). Patients were seated with their injured arm in a splint with the humerus

positioned in 301 of forward rotation relative to the frontal plane, about 451 elevation and the elbow in 901 flexion (Fig. 1a). The forearm was positioned in about 451 pronation. The splint was connected to a six degrees-of-freedom force transducer (AMTI-300, Advanced Mechanical Technology Inc., Wavertown MA, USA), which was placed in line with the longitudinal axis of the humerus. Since the force transducer was mounted on a low friction rail aligned with the longitudinal axis of the humerus, forward and backward translations along the longitudinal humerus axis were free. A low-friction balland-socket joint was mounted between arm splint and force transducer, which left all rotations of the arm splint relative to the transducer free. The resulting set-up thus only allowed forces in directions perpendicular to the low-friction rail, and thus the longitudinal axis of the humerus (Fig. 1b). To compensate for gravitational effects, the arm was fully supported in rest by means of a weight-and-pulley system. Force range could be varied from 10–50 N, with steps of 10 N. The external force was primarily set at the highest possible level. If the patient showed signs of serious discomfort, the external force was lowered with steps of 10 N until the patient could exert this force in all 24 directions perpendicular to the humerus. Force magnitude was controlled by a moving cursor on a display, which responded to the force task. The task incorporated a repeated exertion of two consecutive, opposite directions of force exertion; in order to ‘‘re-set’’ the neuro-muscular system to make sure the patients choose their optimal subset of muscle activation and to debar from to much synergistic activation. The patients had to maintain the force for 3 s in each of the 24 directions while simultaneously EMG data were collected (Fig. 1c). Two different conditions were measured: (1) without anaesthetics; (2) 10 min after subacromial injection of a 101 cc lidocaine 1% solution. Patients were asked to score their experienced pain during both tasks on a 10-point visual analogue scale (VAS).

Table 1 Patients’ characteristics Patient

Age

Gender

Tear

Origin

Duration (years)

1 2 3 4 5 6 7 8 9 10

69 54 57 50 72 60 61 67 50 66

Male Female Male Male Female Female Male Male Female Male

Supra-/and infraspinatus Supraspinatus Supraspinatus Supra-/and infraspinatus Supraspinatus Supra-/ and infraspinatus Supraspinatus Supra-/and infraspinatus Supraspinatus Supraspinatus

Chronic Chronic Traumatic Traumatic Chronic Chronic Traumatic Traumatic Traumatic Traumatic

2 1.5 1 2 0.5 1 1 1.5 2 1

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Fig. 1. Principal action method (deltoideus posterior right arm). Patients ðn ¼ 10Þ were seated with their injured arm in a splint (a). During an isometric force task in 24 different directions (b) isometrical and isotonic force sections were selected (end trajectory of the circle for every direction) and simultaneously recorded EMG’s were identified (black) based on these force selections (c). The rectified and intergrated (d) EMG was subsequently avaraged (e). The EMG-force vectors were plotted in polar coordinates and a curve was estimated through the data points resulting in one direction of maximum muscle activation, the principal action (PA) (f).

2.3. Electromyography acquisition and parameterization EMGs were recorded from the deltoideus (three parts), latissimus dorsi, pectoralis major (pars clavicularis) and teres major using bipolar surface electrodes. Electrodes were placed according to Table 2 (interelectrode distance 21 mm, maximum skin resistance 10 kO, Bandwidth 20–500 Hz, CMRR 86 dB). For each of the 24 force directions, the rectified (Fig. 1d), averaged EMG over 3 s was determined (Fig. 1e). The magnitudes were normalised between minimum (rest level) and maximum EMG. Force signal and EMG signal were recorded simultaneously. Isometric sections of the force trajectory were identified and simultaneously recorded raw EMG signals were selected (Fig. 1c, black sections) and subsequently rectified (Fig. 1d). An average rectified signal was thus obtained for each of the 24 force directions (Fig. 1e). This signal was reduced by the minimum (assumed rest) level EMG and subsequently normalised relative to the maximum

Table 2 Electrode position for EMG collection Muscle

Surface electrode placement

Deltoideus anterior Deltoideus medialis Deltoideus posterior Latissimus dorsi

Middle of the muscle belly Middle of the muscle belly Middle of the muscle belly About 6 cm below the angulus inferior Middle of the muscle belly of the clavicular part Middle of the muscle belly

Pectoralis major (pars clavicularis) Teres major

observed EMG. Thus, we obtained the muscle activation level in all directions perpendicular to the longitudinal axis of the humerus. Through the force direction related activation levels ðn ¼ 24Þ a function was fitted in a least squares sense based on three directional and two amplitude parameters (de Groot et al., 2004). The directional

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parameters are expressed by positive values between 01 and 3601 ( ¼ 01). The force direction related angle of maximum muscle activation is referred to as principal action (Fig. 1f). Estimated principal actions were compared with normative values obtained from healthy subjects by Meskers et al. (2004).

3. Results Subacromial lidocaine injection led to an average significant reduction on the VAS scale ðp ¼ 0:05Þ, from 7.7 (SD 1.2) to 0.9 (SD 1.6), indicating a strong reduction in pain, although some patients still experienced pain after treatment (Fig. 2a). The exerted arm force during the task could significantly be increased by factor 1.6 ðp ¼ 0:05Þ after pain reduction, from 10.4 N (SD 5.7) to 15.7 N (SD 7.4) (Fig. 2b). Patient no. 7 did not respond to the lidocaine injection on any of the three outcome parameters pain, arm force and principal action. Patient no. 3 reported a decrease in pain and an increase in arm force, without any change in principal action. Compared to a normal activation pattern (Meskers et al., 2004), eight out of ten patients showed a pathological muscle activation pattern in which one or more of the adductor muscles showed a

2.4. Statistics The magnitude of applied force and the VAS prior to and after subacromial lidocaine injection were compared by means of the paired Student’s t-test. Changes in PA were tested by means of an ANOVA for repeated measurements and lidocaine treatment as fixed factor. For individual analysis a principal action change over 901 in one or more muscles was considered a change in activation pattern.

(a) 0

1

2

3

4

5

6

7

8

9

10

(b)

Fig. 2. Effects of lidocaine on pain and arm force: (a) pain scored on visual analogue scale; pain experience decreased significantly after subacromial lidocaine injection ðp ¼ 0:00Þ, : pre-lidocaine, : post-lidocaine and (b) arm force perpendicular to the humerus; exerted arm force increased significantly after subacromial lidocaine injection ðp ¼ 0:00Þ.

Table 3 Principal action (1) before and 10 min after subacromial lidocaine. Mean and SD are calculated (after clustering around zero) Patient

Principal action (1) Delt. ant.

Delt. med.

Delt. post.

Lat. dors.

Pect. maj.

Teres maj.

Pre

Post

Pre

Post

Pre

Post

Pre

Post

Pre

Post

Pre

Post

1 2 3 4 5 6 7 8 9 10

346 11 345 56 314 17 4 333 341 360

355 27 349 73 314 34 23 352 323 18

22 23 10 52 323 81 36 343 0 22

355 27 349 73 314 34 23 352 322 18

41 68 88 64 128 98 90 59 93 36

26 78 81 93 166 75 238 50 100 42

21 210 162 53 168 37 320 147 334 44

160 29 165 131 157 44 41 60 152 46

325 353 311 37 304 34 45 318 290 312

306 319 306 156 280 257 49 324 306 309

34 29 182 351 142 39 289 306 47 5

29 7 200 345 137 39 315 349 140 234

Mean SD

357 28

7 35

19 34

7 36

77 28

95 63

78 87

99 59

340 43

297 63

34 78

288 101

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principal action in the upward/abduction direction, and thus counteracting with the intended mechanical effect as seen in controls. Of these eight patients with pathological adductor activity, five patients restored this aberrant activity (partly) in one or more adductor muscles; which is in accordance with the intended mechanical effect. For the whole patient group, after lidocaine injection none of the muscles showed significant changes in principal actions. Principal actions prior to and after lidocaine injection are presented in Table 3. Because of the circular nature of the principal action data (01 is equal to 3601) the angles are clustered around zero (negative values are introduced), in order to calculate standard deviations.

4. Discussion As reported earlier (van de Sande et al., 2006; de Groot et al., 2006) and in agreement with impingement (Ben Yishay et al., 1994), external forces increased significantly after subacromial lidocaine injection in patients with massive rotator cuff tears, despite the (partially) absent supraspinatus forces. The lidocaine intervention did lead to large changes in principal action, but not consistent for all subjects and therefore not significant for the whole patient group. No statistical difference could therefore be identified in the activation patterns of the shoulder muscles before and after subacromial lidocaine injection. Based on the activation of the major (remaining) abductor and adductor muscles we looked for a general coordination change that could explain these observations. Fig. 3 illustrates the mean principal actions (7SD) for the six muscle (part)s. In eight patients, a pathological adductor pattern could be discerned (upward principal action). On average, the effect of lidocaine appeared to result in a partial normalization of the principal action of the adductor muscles (one or more) of more than 301. Since major differences existed between patients, this effect could not be statistically demonstrated. Single patient analysis on the deltoideus (three parts) showed that none of the patients changed their PA direction more than 451, implying relatively little change in muscle activation of the major glenohumeral abductor muscles. For the adductor muscles, a variety of adaptations after lidocaine injection were observed between patients and between muscles. For every adductor muscle one of the following observations, as illustrated for the teres major in Fig. 3, was seen: (1) no change: the patient’s principal action was equal to the normal PA and no change was observed after lidocaine injection. The increase in force exertion

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Fig. 3. Coordination of the patients illustrated by the average estimated principal actions for each of the six muscle activation patterns for ten patients relative to the normal activation (Meskers et al., 2004). : The grey surface represents the 99% confidence interval for young healthy subjects according to Meskers et al. (2004). The black line represents the average maximum activation (PA) of 10 patients prior to lidocaine intervention (7SD, dashed). The grey line represents the average maximum activation (PA) after lidocaine intervention (7SD, dashed). For the teres major, the single patient results are added to illustrate three conditions: no change (o): principal action was equal to the normal PA and no change was observed after lidocaine injection. Return to normal (*): a deviating principal action of 4901 when compared to normal, which changed to normal after lidocaine injection. Persistent deviation (x): a deviating principal action deviating of 4901 persisting after lidocaine injection.

could be the result of an equal increase of all muscle forces. (2) return to normal: a deviating principal action over 901 was observed when compared to normal, which changed to normal after lidocaine injection. These patients were indeed able to change their activation pattern within 10 min in response to pain reduction. (3) persistent deviation: a deviating principal action over 901, persisting after lidocaine injection. Either these patients were still sensitive for the upward glenohumeral translation after pain suppression, or they were not able to restore their activation pattern within short time. The reason for the persistent deviation could be the duration of the tear and the persistent pathological coordination pattern, which results in a ‘‘hard-wired’’ coordinative adaptation. So far our data do not indicate any relation with duration of the cuff tear. The observation that firstly the maximum activation direction of the deltoideus hardly changed and that secondly the adductor muscles show a pathological pattern that partly returned to normal after reduction of pain can be explained mechanically, taking the necessary compromise between abduction mobility and required glenohumeral stability into account;

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Fig. 4. Schematic representation of muscle contribution and resulting glenohumeral reaction forces in healthy subjects and patients suffering massive cuff tears. (a) Arm elevation in healthy subjects requires an abduction moment along with, glenohumeral force equilibrium, provided by the deltoideus muscles and the supraspinatus. The resultant force (summation of both force vectors; dotted lines) can fully be compensated by the glenoid resulting in a statically stable condition. (b) Compensation of the lost supraspinatus joint torque by the deltoideus is accompanied with an increased upward force, which can only partially be compensated by the glenoid. Without compensation for the remaining force vector, a (painful) upward glenohumeral translation (subluxation) is expected. (c) The upward directed pathological luxating force component prior to the lidocaine intervention can be compensated for by depressor/adductor muscles, e.g. teres major, latissimus dorsi and pectoralis major at the cost of reduction of nett abduction torque.

Arm elevation in healthy patients requires an abduction moment along with glenohumeral force equilibrium (Fig. 4a). Patients suffering from a massive cuff tear have lost the contribution of the supraspinatus and can only compensate this loss of adduction torque by using their deltoid muscles. Relative to the supraspinatus, the deltoideus potentially generate a greater abduction torque. However, the muscle line of action or muscle force vector is more cranial (upward) directed. When activated, the deltoideus therefore generated a greater upward ‘luxating’ force component relative to the suprasinatus. Compensation of the lost supraspinatus joint torque by the deltoideus is therefore accompanied with an increased upward force (Fig. 4b). Without compensation for this force, there would be a tendency towards (painful) upward glenohumeral subluxation (Fig. 4b). Magermans et al. (2004) indeed illustrated, by model simulation, a glenohumeral reaction force in the superior part of the glenoid in patients with a torn supraspinatus, possibly causing a proximal migration of the humeral head. Compared to healthy patients, eight out of ten patients showed compensation for the pathological supreriorly luxating force component prior to the lidocaine intervention by several depressor/ adductor muscles, e.g. latissimus dorsi, pectoralis major and teres major (Fig. 4c). The observed principal action changes imply a change in muscle function, by means of a shift from generating adduction torque, towards generating humeral head depression (stabilization) force. This counterbalance for a threatening upward glenohumeral luxation reduces the overall abduction torque because of the substantial adduction torque function of the adductor muscles. This could explain the

observed functional abduction impairment in patients (de Groot et al., 2006). After lidocaine injection, patients no longer ‘sense’ the pain due to upward GH subluxation. Adductor muscles are no longer required to reduce pain by pulling the humeral head down. Arm force and arm elevation increase, at the expense of glenohumeral stability and further deterioration of the subacromial tissues. Limitations of this study, like the small sample size, may influence outcome. The severity of the rotator cuff tears, duration and origin of the cuff tear (acute trauma, chronic) may influence the different patterns of muscle activation and their changes. So far, our data do not reveal such influences. This study did not focus on the interdependency of the different muscle forces in the used measurement, but treated muscle activities as (relatively) independent phenomena. This simplification could lead to unjustified interpretations at the level of the isolated muscle and to unjustified insignificant changes in principal actions. To include interdependencies, a musculoskeletal model (van der Helm, 1994; Magermans et al., 2004) will be required to evaluate the mechanical effect of muscle deficiency in a single muscle on all muscles involved. Our results are coherent with earlier results presented by De Ben Yishay et al. (1994), van de Sande et al. (2006), de Groot et al. (2006). We also found that external forces increased significantly after subacromial lidocaine injection in patients with massive rotator cuff tears, despite the (partially) absent supraspinatus forces. In order to reduce a painful superior translation of the humeral head, arm adductors are co-activated resulting in a reduced maximum arm elevation. Masking this pain

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may further deteriorate the subacromial tissues as a result of proximal migration of the humeral head and subsequent impingement of subacromial tissues.

References Arwert HJ, de Groot JH, Van Woensel WW, Rozing PM. Electromyography of shoulder muscles in relation to force direction. Journal of Shoulder and Elbow Surgery 1997(6):360–70. Ben Yishay A, Zuckerman JD, Gallagher M, Cuomo F. Pain inhibition of shoulder strength in patients with impingement syndrome. Orthopedics 1994(17):685–8. de Groot JH, Rozendaal LA, Meskers CGM, Arwert HJ. Isometric shoulder muscle activation patterns for 3-D planar forces: a methodology for musculo-skeletal model validation. Clinical Biomechanics 2004(19):790–800. de Groot JH, van de Sande MAJ, Meskers CGM, Rozing PM. Pathological Teres Major activation in patients with massive rotator cuff tears alters with pain relief and/or salvage surgery

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transfer. Clinical Biomechanics (Bristol, Avon) 2006;21 (Suppl 1):S27–32. Flanders M, Soechting J F. Arm muscle activation for static forces in three-dimensional space. Journal of Neurophysiology 1990(64): 1818–37. Magermans DJ, Chadwick EK, Veeger HEJ, van der Helm FCT, Rozing PM. Biomechanical analysis of tendon transfers for massive rotator cuff tears. Clinical Biomechanics (Bristol, Avon) 2004(19):350–7. Meskers CGM, de Groot JH, Arwert HJ, Rozendaal LA, Rozing PM. Reliability of force direction dependent EMG parameters of shoulder muscles for clinical measurements. Clinical Biomechanics 2004(19):913–20. van de Sande MAJ, de Groot JH, Meskers CGM, Rozing PM. Functional and biomechanical assessment of Teres Major tendon transfer as primary treatment of massive rotator cuff tear. Surgery of the shoulder and elbow: an international perspective. In: Proceedings book 9th international congress on surgery of the shoulder, May 2–5, 2004, Washington DC, USA, 2006, in press. van der Helm FCT. A finite element musculoskeletal model of the shoulder mechanism. Journal of Biomechanics 1994(27):551–69.

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Manual Therapy 11 (2006) 238–239 www.elsevier.com/locate/math

Announcement 2nd International Conference on Movement Dysfunction

Elsevier Sponsored Awards—Best Oral and Best Poster Presentation The winners of the awards at the conference were

Best Oral Presentation a

M. Smith Somervillea,*, A. Russellb, P.W. Hodgesa

University of Queensland, Division of Physiotherapy, Australia University of Queensland, School of Population Health, Australia

b

Is back pain more common during pregnancy?

Abstract Purpose: To determine prevalence of back pain (BP) in women during pregnancy compared to those who are not pregnant, to compare prevalence of BP in parous and nulliparous women, and to establish the association between BP and urinary incontinence in pregnant women. Relevance: Previous research suggests that BP is more common in pregnant women, but studies have either not included a control group of non-pregnant women, or included a non-random sample. Urinary incontinence is common during pregnancy; however, its relationship with BP has not been questioned despite the contribution of pelvic floor muscles to continence and spinal control. Subjects: Young and mid-age women from the Australian Longitudinal Study on Women’s Health (ALSWH) were randomly selected from the 1996 Medicare database. The analysis involved 517 pregnant women, and 28 035 women who were not currently pregnant. Methods: We conducted a cross-sectional analysis of self-report, postal survey data from the ALSWH. Analysis: Associations between BP, pregnancy and parity were assessed using w2 analysis. Multinomial logistic regression was used to model the odds of BP. Results: In the young age cohort, BP was more frequent among pregnant women than those who were not pregnant (po0.001), and for parous women compared to nulliparous women (po0.001). However, no associations were seen in the mid-age cohort. In multivariate analysis, women with urinary incontinence had odds ratios for ‘‘often’’ having BP of 8.5, and ‘‘rarely or sometimes’’ having BP of 3.8. Discussion: Unlike young women, BP was not more common in mid-age pregnant women than those who were not pregnant, and BP was not more common in parous women. Taken together this suggests that pregnancy may lead to the earlier development of BP without effecting long-term prevalence. Urinary incontinence and BP may be related in pregnant women due to diverse functions of the pelvic floor muscles. Keywords: Pregnancy; Back pain; Urinary incontinence; Parity

1356-689X/$ - see front matter doi:10.1016/j.math.2006.07.001

ARTICLE IN PRESS Announcement / Manual Therapy 11 (2006) 238–239

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Best Poster Presentation M. Gorelicka,, M. Brownb, H. Groellerb a

Schulthess Clinic, Switzerland University of Wollongong, Australia

b

Whole muscle activation indicates eccentric muscle fatigue and damage Abstract Purpose: The purpose of this study was to measure the reliability and sensitivity of a new non-invasive approach in quantifying muscle morphological changes, utilizing whole muscle belly mechanomyography (MMG), attributed to an aggressive bout of eccentric exercise. Relevance: Continued and intense eccentric muscle activation is typically associated with muscle injury, commonly termed delayed onset of muscle soreness (DOMS). Currently, there are few objective tools to monitor muscle fatigue or associated muscle damage non-invasively. Methods: Twelve (6 males/6 females) healthy athletic university students aged 20–24 years old volunteered to participate in the study. The MMG response of each subject’s dominant (D) and non-Dominant (ND) arm was tested on six consecutive days. However, only the ND arm was subjected to the eccentric fatigue protocol, initiated on Day 2 of testing. Analysis: Two-way repeated measures ANOVA was used to determine the effects of the four parameters—maximal displacement (Dmax), contraction time (Tc), relaxation time (Tr) and half-relaxation time (½Tr). If significance was reached (po0.05) in any parameter a pair-wise multiple comparison procedure (Tukey Post- Hoc) was performed to determine which days attributed to the significant results. Results: The MMG results confirmed the lasting effects of the eccentric exercise fatigue of the ND arm. Dmax, Tc, Tr and ½Tr all showed significant differences on Day 2 and Day 3 when D and ND arms were compared (average change ¼ 26.1% SD 7.2%). Additionally, Tr and ½Tr continued to show differences on Day 4 (average change ¼ 8.4% SD 10.1%). All curve calculation parameters had recovered by Day 5 and continued to show little variation on Day 6. Discussion: The physiological impairments of eccentric exercise induced biceps fatigue can be monitored using whole muscle belly MMG. This was characterized by significant decreases in maximal displacement, a slowing of contraction time and relaxation time until their recovery 2–3 days later. Keywords: Mechanomyography; Eccentric; Muscle; Damage Full poster available online at www.sciencedirect.com.

Mark Gorelick and Michelle Smith Somerville, centre, receive their prizes from Mindy Cairns, Chair of the Scientific Committee (left) and Melanie Burton, Publisher, Elsevier (right).

Manual Therapy (2006) 11(3), 240

Diary of events

The Belgian Scientific organisation of Manual Therapy (B.W.M.T.) presents ‘‘ECT 2006’’ ‘‘State of the art Managing Upper Limb Joint and Soft Tissue Disorders’’ A masterclass by Karim Kahn, Bill Vincenzino, Rachel Leary, JL Gielen, Ann Cools and Jean-Pierre Baeyens. 21, 22 & 23 September 2006 Venue: Provinciehuis, Antwerp, Belgium Information & registration: www.bwmt.be or Tel./Fax: 0032 3 775 88 96

Prof Gordon Waddell Full details are availabel at www.sbpr.info Abstracts should be submitted to [email protected] Deadline for abstract submission is 4 August 2006 Janet G. Travell, MD Seminar Series, Bethesda, USA For information, contact: Myopain Seminars, 7830 Old Georgetown Road, Suite C-15, Bethesda, MD 20814-2432, USA. Tel.: +1 301 656 0220; Fax: +1 301 654 0333; website: www.painpoints.com/seminars.htm; E-mail: [email protected]

The Society for Back pain Research Annual General Meeting 2006 2–3 November 2006 Gisborough Hall, Guisborough, North Yorkshire The Theme of the meeting will be ‘Fitness for Work’ Guest Speakers: Prof Mansel Aylward, Dr Leena Niemisto, Dr kaija Paustjarvi and

If you wish to advertise a course/conference, please contact: Karen Beeton, Department of Physiotherapy, University of Hertfordshire, College Lane, Hatfield, Herts AL10 9AB, UK. There is no charge for this service.

240

Whole Muscle Activation Indicates Eccentric Muscle Fatigue and Damage M. Gorelick1*, M. Brown2, H. Groeller2 1Schulthess

Clinic, Switzerland; 2University of Wollongong, Australia

Purpose

Results

The purpose of this study was to measure the reliability and sensitivity of a novel non-invasive approach, mechanomyography (MMG), to quantify changes in muscle contractile properties due to eccentric exercise.

The results confirmed the deleterious effects of eccentric fatigue on the contractile properties of BB (Fig. 3). Dmax, Tc, Tr and ½Tr were all significantly (p<0.05) longer on Days 2 and 3 (treatment vs control arm) (average change=26.1% SD 7.2%) with Tr and ½Tr continuing to be prolonged until Day 4 (average change=8.4% SD 10.1%). All MMG variables had recovered to baseline by Day 5. Changes in MMG variables, due to fatigue, were correlated to subject self-reports of pain and discomfort (VAS) following the fatigue protocol over the 6-day test period

Relevance Intense eccentric muscle activation is typically associated with a reduction in active tension, injury and a delayed onset of muscle soreness (DOMS). Currently, there are few non-invasive clinical tools to detect muscle fatigue in vivo.

Methods Twelve (6 males/6 females) healthy athletic University students, aged 2024 years old, volunteered to participate in the study. Biceps Brachii (BB) contractile properties (treatment and control arm) were measured on six consecutive days (Fig. 1 & 2) both before (Day 1) and after (Days 2-6) an eccentric fatigue protocol (treatment arm only).

Fig. 2. Analysis of the MMG waveform. Dmax = maximal displacement; Tc = contraction time; Td = delay time; Ts = sustain time; Tr = relaxation time; PNS = percutaneous neuromuscular stimulation. ½ Tr not shown on figure. Figures relate to percentage of maximal displacement.

Dmax ) m m ( t n e m e c al p si D d e sil a m r o N

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Fig. 3. Depicts the normalised (with respects to changes from day 1) mean data from day 1 to 6. Note the significant (p<0.05) change from base-line on days 2 and 3 (Dmax & Tc) as well as day 4 (Tr & ½ Tr) * Significant (p<0.05) difference between Control and Treatment Arm. ∆ Significant (P<0.05) difference from Day 1.

Applications

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Fig. 1. Displays the laser-based whole muscle MMG setup, comprised of (1) two percutaneous neuromuscular stimulating pads (PNS), (2) distance calibration rod, and (3) the laser-sensor head.

Physiological impairments due to eccentric BB fatigue can be reliably monitored by a non-invasive MMG technique. The MMG technique has utility for the in-clinic assessment of eccentric muscle fatigue in musculoskeletal rehabilitation and sport.

0

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There are two main areas of application for the MMG to measure muscle fatigue: (1) improving the effectiveness of rehabilitation treatments and follow-up, and (2) preventative injury management for athletes and potential talent identification through non-invasive and repeated fibre type composition analysis.