Manual Therapy Journal - Volume 14, Issue 6, Pages 585-716 (December 2009)

VOLUME 14 NUMBER 6 PAGES 585–716 December 2009

Editors 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 Gwendolen Jull PhD, MPhty, Grad Dip ManTher, FACP Department of Physiotherapy University of Queensland Brisbane QLD 4072, Australia

Associate Editor’s Deborah Falla PhD, BPhty(Hons) Department of Health Science and Technology Aalborg University, Fredrik BajersVej 7, D-3, DK-9220 Aalborg Denmark Email:[email protected] Tim McClune D.O. Spinal Research Unit. University of Huddersfield 30 Queen Street Huddersfield HD12SP, UK E-mail: [email protected]

Editorial Committee Timothy W Flynn PhD, PT, OCS, FAAOMPT RHSHP-Department of Physical Therapy Regis University Denver, CO 80221-1099 USA Email: [email protected] Masterclass Editor Karen Beeton PhD, MPhty, BSc(Hons), MCSP MACP ex officio member Associate Head of School (Professional Development) School of Health and Emergency Professions University of Hertfordshire College Lane Hatfield AL10 9AB, UK E-mail: [email protected] Case Reports & Professional Issues Editor Jeffrey D. Boyling MSc, BPhty, GradDipAdvManTher, MCSP, MErgS Jeffrey Boyling Associates Broadway Chambers Hammersmith Broadway London W6 7AF, UK E-mail:[email protected] Book Review Editor Raymond Swinkels PhD, PT, MT Ulenpas 80 5655 JD Eindoven The Netherlands E-mail: [email protected]

International Advisory Board K. Bennell (Melbourne, Australia) K. Burton (Huddersfield, UK) B. Carstensen (Frederiksberg, Denmark) T. Chiu (Kowloon, Hong Kong) J. Cleland (Concord, NH, USA) M. Coppieters (Brisbane, Australia) E. Cruz (Setubal, Portugal) L. Danneels (Maríakerke, Belgium) I. Diener (Stellenbosch, South Africa) S. Durrell (London, UK) S. Edmondston (Perth, Australia) L. Exelby (Biggleswade, UK) J. Greening (London, UK) A. Gross (Hamilton, Canada) T. Hall (Perth, Australia) W. Hing (Auckland, New Zealand) M. Jones (Adelaide, Australia) B.W. Koes (Amsterdam, The Netherlands) J. Langendoen (Kempten, Germany) D. Lawrence (Davenport, IA, USA) D. Lee (Delta, Canada) R. Lee (London, UK) C. Liebenson (Los Angeles, CA, USA) L. Maffey-Ward (Calgary, Canada) E. Maheu (Quebec, Canada) C. McCarthy (Coventry, UK) J. McConnell (Northbridge, Australia) S. Mercer (Brisbane, Australia) P. Michaelson (Luleå, Sweden) D. Newham (London, UK) J. Ng (Hung Hom, Hong Kong) S. O’Leary (Brisbane, Australia) 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) E. Rasmussen Barr (Stockholm, Sweden) D. Reid (Auckland, New Zealand) D.A. Rivett (Callaghan, Australia) A. Rushton (Birmingham, UK) M. A. Schmitt (Amersfoort, The Netherlands) M. Shacklock (Adelaide, Australia) D. Shirley (Sydney, Australia) C. Snijders (Rotterdam, The Netherlands) P. Spencer (Barnstaple, UK) M. Sterling (Brisbane, Australia) M. Stokes (Southampton, UK) P. Tehan (Melbourne, Australia) M. Testa (Alassio, Italy) P. van der Wurff (Doorn, The Netherlands) P. van Roy (Brussels, Belgium) O. Vasseljen (Trondheim, Norway) B.Vicenzino (Brisbane, Australia) M. Wessely (Paris, France) A. Wright (Perth, Australia) M. Zusman (Perth, Australia)

Visit the journal website at http://www.elsevier.com/math doi:10.1016/S1356-689X(09)00161-1

Manual Therapy 14 (2009) 585

Contents lists available at ScienceDirect

Manual Therapy journal homepage: www.elsevier.com/math

Editorial

World Congress of Physical Therapy 2011 and IFOMT 2012

As January 2010 approaches the build-up to two significant conference events is in flow. These events are the World Congress of Physical Therapy to be held June 20th to June 23rd 2011 in Amsterdam in Holland, and IFOMT 2012 which will be held between 30th September and 5th October in Quebec, Canada. Both these events will showcase research and developments in practice, but tend to attract different audiences who attend for different reasons and purposes. Whilst IFOMT attracts physical therapists, osteopaths and chiropractors specialising or wishing to specialise in musculoskeletal therapy and sets increasingly high standards in terms of research rigour and endeavour, the World Confederation of Physical Therapy as an organisation, is committed to taking forward physical therapy as a profession and its contribution to global health. The Confederation promotes and encourages high standards of physical therapy research, education and practice. Globally, physical therapy is in very different stages of development, for example, in several countries, physical therapists act as first contact practitioners, some are holding consultant posts in hospital settings and working almost autonomously, whilst other physiotherapists in some parts of the world are struggling to achieve degree status and first contact rights. Wherever physical therapists are based we all face issues and challenges in day to day practice and in professional status and development. Some physical therapists face incredible personal and professional challenges when working, for example, in areas of conflict and severe hardship, dealing with patients who are mal-nourished and who are also suffering other consequences of living in poverty-stricken areas. Many of us working in western societies are perhaps lulled into our own senses of security and are not exposed to the difficulties that some of our colleagues face in different parts of the world. Research in physical therapy and standards of education and practice are at different levels of maturity in different parts of the world. Anything that can be done as a profession to reduce this diversity can only help strengthen the profession globally. I was very honoured to be elected to be Chair of the International Scientific Committee for the World Congress of Physical Therapy 2011. I am highly committed, as is the rest of the International Scientific Committee, to provide a conference in 2011 which celebrates physical therapy as a whole global community which, whilst recognising specialism and distinct areas of practice, also recognises the importance of sharing ideas, new knowledge, new approaches to practice, education and research. The committee is also aiming to construct a conference which works towards enabling all those attending to cross specialisation boundaries, cross international divides and enables the

1356-689X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2009.10.004

whole of the physical therapy worldwide community to grow intellectually. For some this will be via the sheer exposure to new research findings and for some it will be by gaining insights into other specialities, other ways of working, but also by recognising what obstacles physical therapists in some countries face and how they are dealing with these obstacles. The conference should be a learning experience for everyone, whether you come as a top international researcher, or a new graduate physical therapist from a country where physiotherapy is still in its early developmental stages. There is something at WCPT for everyone. The World Confederation of Physical Therapy represents over 300,000 physical therapists worldwide and has 101 member organisations. The World Congress is expected to attract around 3500 delegates, providing a rich and vibrant forum for networking and debate and the opportunity to contribute to other physical therapists’ knowledge base development. WCPT 2011 will be held at the Rai Exhibition and Conference Centre in Amsterdam and the Royal Dutch Society for Physical Therapy (KNGF) is hosting the conference. Please visit the WCPT website for ongoing information. Importantly, the call for abstract submissions for the 2011 conference will be open in January 2010, so think now about submitting an abstract for a platform, poster or interactive poster presentation. Additionally, other sessions will be available at WCPT 2011, for example focused symposia and satellite programmes which will have a strong international focus as will debating sessions, workshops and of course a range of networking and social activities. Put WCPT 2011 in your calendar now! If you have not attended a WCPT congress before, it will be a new experience and one hopefully not to forget. The International Scientific Committee members will be doing its very best to provide a memorable conference for everyone and we will look forward to seeing you there. And whilst you are getting your diaries out to put in the WCPT 2011 dates, please also put the dates in your diary for IFOMT 2012. In the meantime, Seasons Greetings to All. Ann Moore, Executive Editor, Chair of the International Scientific Committee, WCPT 2011* Director Clinical Research Centre for Health Professions, Aldro Building, 49, Darley Road, Eastbourne BN20 7UR, United Kingdom  Tel.: þ44 1273 643 766; fax: þ44 1273 643 944. E-mail address: [email protected]

Manual Therapy 14 (2009) 586–595

Contents lists available at ScienceDirect

Manual Therapy journal homepage: www.elsevier.com/math

Masterclass

Thoracic outlet syndrome part 1: Clinical manifestations, differentiation and treatment pathways L.A. Watson a, b, T. Pizzari b, *, S. Balster a a b

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

a r t i c l e i n f o

a b s t r a c t

Article history: Received 12 January 2009 Received in revised form 7 July 2009 Accepted 10 August 2009

Thoracic outlet syndrome (TOS) is a challenging condition to diagnose correctly and manage appropriately. This is the result of a number of factors including the multifaceted contribution to the syndrome, the limitations of current clinical diagnostic tests, the insufficient recognition of the sub-types of TOS and the dearth of research into the optimal treatment approach. This masterclass identifies the subtypes of TOS, highlights the possible factors that contribute to the condition and outlines the clinical examination required to diagnose the presence of TOS. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Thoracic outlet syndrome Entrapment neuropathy Classification Diagnosis

1. Introduction

2. Definition

Opinions in the literature about thoracic outlet syndrome (TOS) vary in the extreme, swaying from the belief that it is the most underrated, overlooked and misdiagnosed peripheral nerve compression in the upper extremity (Shukla and Carlton, 1996; Sheth and Belzberg, 2001) to questioning whether it exists (Wilbourn, 1990). These varying beliefs highlight the need for the clinician to be rigorous in their clinical assessment so that patients are not misdiagnosed and are appropriately managed. Unfortunately the diagnosis of TOS remains essentially clinical and is often one of exclusion with no investigation being a specific predictor. This may be attributed, in part, to the fact that TOS is considered to be a collection of quite diverse syndromes rather than a single entity (Yanaka et al., 2004). Consequently, this also results in TOS being one of the most difficult upper limb conditions to manage. The aim of this paper (Part 1) is to clarify the nomenclature, classification, varying clinical presentations and assessment techniques so that the reader may attempt to assess and differentially diagnose patients presenting with TOS. The second paper (Part 2) will outline specific rehabilitation approaches used by the authors to treat one sub-type of TOS.

A broad definition of TOS is a symptom complex characterized by pain, paresthesia, weakness and discomfort in the upper limb which is aggravated by elevation of the arms or by exaggerated movements of the head and neck (Lindgren and Oksala, 1995).

* Corresponding author. Tel.: þ61 3 94795872. E-mail address: [email protected] (T. Pizzari). 1356-689X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2009.08.007

3. Anatomical considerations The pain and discomfort of TOS are generally attributed to the compression of the subclavian vein, subclavian artery and the lower trunk of the brachial plexus as they pass through the thoracic outlet (Cooke, 2003; Samarasam et al., 2004; Barkhordarian, 2007). Three sites of compression of the vessels and nerves are possible (Fig. 1). The lower roots of the brachial plexus may be compressed as they exit from the thoracic cavity and rise up over the first rib (or a cervical rib or band when present) and pass between the anterior and middle scalene muscles (or even sometimes through the anterior scalene muscle). The upper roots of the brachial plexus can also be compressed between the scalene muscles but actually exit the cervical spine not the thorax, and should technically be referred to as cervical outlet syndrome (Ranney, 1996). The second potential site of entrapment is beneath the clavicle in the costoclavicular space, where the neural elements are already outside the thorax. The third potential site is more distal in the sub-coracoid tunnel (beneath the tendon of the pectoralis minor) where the plexus may be stretched by shoulder abduction (Ranney, 1996; Rayan, 1998; Demondion et al., 2003; Wright and Jennings, 2005).

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595

587

The classifications for vTOS, tnTOS, and sTOS can be seen in Table 1. 5. Incidence

Fig. 1. Thoracic outlet anatomy. Three possible site of compression and structures compressed; A: Subclavian artery and lower roots of the brachial plexus may be compressed as they exit from the thoracic cavity and rise up over the first rib and pass between the anterior and middle scalene muscles. B: Subclavian artery and vein and/or lower trunk of the brachial plexus beneath the clavicle in the costoclavicular space. C: The axillary artery and/or vein and/or one of the cords of the brachial plexus in the sub-coracoid tunnel.

Very rarely is this clarified in the literature and the reader should be aware that many authors utilize the global term of TOS with little attempt to differentiate which sub-type of TOS they are treating. This may well account for the enormous variation in treatment outcomes described. We believe it is essential that the clinician carefully consider and at least attempt to clinically differentiate, where possible, exactly which component of the neurovascular complex is being affected and precisely where it is being compressed. This will direct not only what further investigations are required, but may well impact on what is the most appropriate treatment strategy. In reality this is often easier said than done. 4. Classification and pathophysiology TOS is often categorized into two specific clinical entities: Vascular TOS (vTOS) and Neurological TOS (nTOS) (Atasoy, 1996; Rayan, 1998; Sharp et al., 2001). vTOS can be divided into arterial and venous TOS syndromes due to compression or angulation of either the subclavian or axillary artery or vein (Rayan, 1998; Davidovic et al., 2003). Usually it is caused by a structural lesion, either a cervical rib or another bony anomaly (Rayan, 1998). Arterial involvement is more common than venous involvement (Davidovic et al., 2003; Singh, 2006) and vTOS is generally easier to define, diagnose and treat than nTOS (Sharp et al., 2001). The subset of patients with bony abnormalities such as cervical ribs, are generally accepted as ‘‘true cases’’ of TOS and this commonly occurs in vTOS and true neurological TOS (tnTOS) (Roos, 1982; Samarasam et al., 2004). tnTOS is caused by irritation, compression or traction of the brachial plexus. The remaining larger group of patients with no radiological or electro-physical abnormalities are usually labeled as ‘‘disputed TOS’’ (Cherington, 1989) or ‘‘non-specific nTOS’’ (Sobey et al., 1993) or ‘‘symptomatic TOS’’ sTOS (Rayan, 1998). sTOS remains the most controversial form of TOS. There has been some suggestion that this may be an early or mild form of vTOS or nTOS and hence may mimic the symptoms with no definitive evidence for either (Rayan, 1998; Seror, 2005; Lee et al., 2006). In some cases patients may present with ‘‘combined TOS,’’ the simultaneous compression of vascular and neurological structures. This may be mixture of arterial and venous or arterial/venous and neurological or all three.

The incidence of TOS is reported to be approximately 8% of the population (Davidovic et al., 2003), is extremely rare in children (Cagli et al., 2006), and affects females more than males (between 4:1 and 2:1 ratios) (Gockel et al., 1994; Davidovic et al., 2003; Demondion et al., 2003; Degeorges et al., 2004). In particular, tnTOS is typically found in young women (van Es, 2001). According to Davidovic et al. (2003), 98% of all patients with TOS fall into the nTOS category and only 2% have vTOS. However this figure is clouded by the fact there is no distinction between tnTOS and sTOS (Urschel et al., 1994; Urschel and Razzuk, 1997; Goff et al., 1998). While neurological symptoms appear more prominently, the majority of these will fall into the sTOS classification (Wilbourn, 1990; Rayan, 1998; Davidovic et al., 2003). 6. Etiology Bony pathology or soft tissue alterations are commonly attributed to the etiology of TOS. Numerous causes have been cited in the literature ranging from congenital abnormalities (anomalies of the transverse process of seventh cervical vertebra, cervical rib, first rib, enlarged scalene tubercle, scalene muscles, costoclavicular ligaments, subclavius or pectoralis minor) to traumatic in origin (such as a motor vehicle accident or sporting incident) (Gruber, 1952; Makhoul and Machleder, 1992; Rockwood et al., 1997; Athanassiadi et al., 2001; Jain et al., 2002; Barkhordarian, 2007). Cervical ribs and other anatomic variations are not prerequisites for the diagnosis of TOS but may be implicated in some cases. Traumatic bony lesions include bone remodeling after fractures of the clavicle or first rib or posterior subluxation of the acromioclavicular joint. Soft tissue pathologies such as anterior scalene muscle hypertrophy, muscle fibre type adaptive transformation, spasm and excessive contraction particularly post cervical trauma have all been implicated in TOS (Roos, 1982; Machleder et al., 1986; Mackinnon, 1994; Schwartzman and Maleki, 1999; Kai et al., 2001; Pascarelli and Hsu, 2001; Davidovic et al., 2003). Less commonly, upper lung tumors have been implicated in the etiology (Machleder et al., 1986; Makhoul and Machleder, 1992; Barkhordarian, 2007). Postural or occupational stressors with repetitive overuse and associated soft tissue adaptations such as hypertrophy in some muscles and atrophy in others, have been implicated in all forms of TOS. Poor posture, especially in patients with large amounts of breast tissue or swelling due to trauma in the area, may predispose to TOS. Compression occurs when the size and the shape of the thoracic outlet is altered. This is commonly caused by poor posture, such as lowering the anterior chest wall with drooping shoulders and holding the head in a forward position (Aligne and Barral, 1992; Novak et al., 1995; Ranney, 1996; Rayan, 1998; Skandalakis and Mirilas, 2001; Barkhordarian, 2007). 7. Diagnosis Diagnosis of TOS is clinical and based on a detailed history, subjective and objective examination of neurovascular and musculoskeletal systems of the neck, shoulder, arm and hands (Roos, 1982; Novak et al., 1995). Frequently a multitude of further investigations are required, many of which in the case of sTOS may indeed prove to be negative (Barkhordarian, 2007). The literature laments that there is no one test or investigation that consistently proves the diagnosis of TOS. Given that TOS really is a ‘‘collection’’ of symptom complexes, often multifaceted, it is unreasonable to

588

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595

Table 1 Classifications, pathophysiology and investigations. Classification

Sub-type

Pathology

Signs & Symptoms

Vascular TOS (vTOS)

1. Arterial TOS (aTOS)

Compression of the subclavian artery that produces any combination of stenosis, poststenotic dilatation, intimal injury, formation of aneurysms and mural thrombosis.

2. Venous TOS (venTOS)

Unilateral arm swelling without thrombosis, when not caused by lymphatic obstruction may be due to subclavian vein compression.

1. True Neurological TOS (tnTOS)

Irritation, compression or traction of the brachial plexus creating compromised nerve function. Compression usually occurs via a bony or soft tissue anomaly present congenitally, created by either repetitive or significant trauma and often influenced by postural, occupational or sporting factors.

2. Symptomatic TOS (sTOS)

Usually no bony or soft tissue anomaly can be demonstrated. Intermittent compression of the neurovascular complex due to repetitive postural, occupational or sporting forces that create temporary compression at varying sites in the cervical or thoracic outlet

Upper limb ischaemia Multiple upper limb arterial embolization Acute hand ischaemia Claudication Vasomotor phenomena Digital gangrene Absent or decreased arterial pulse Swelling, feeling of stiffness/heaviness, fatigability, coldness, pain of muscle cramp in the upper limb or hand Paresthesia (due to ischaemia) Asymmetrical upper extremity oedema (bilateral oedema can occur) Pain, cyanosis, fatigability and a feeling of stiffness or heaviness of the upper extremity Venous engorgement with collateralization of peripheral vessels Axillary or subclavian vein thrombosis Pulmonary embolism Paresthesia Upper plexus syndrome – C5/6/7 pattern: Sensory changes in the first three fingers þ/ numbness in cheek, earlobe, back of shoulder, or lateral arm Weakness in deltoid, biceps, triceps, scapula muscles and forearm extensors Pain in anterior neck, chest, supraclavicular region, triceps, deltoids, parascapular muscle, outer arm to the extensor muscles of the forearm þ/ pain in the neck, pectoral region (pseudoangina), face, mandible, temple and ear with occipital headaches þ/ dizziness, vertigo and blurred vision Lower plexus syndrome – C7/8/T1 pattern: Sensory changes in the fourth and fifth fingers, sensory loss above medial elbow Pain and paresthesia over the medial aspect of the arm, forearm, ulnar 1½ digits Hand weakness, loss of dexterity and wasting (lateral thenar muscles, profundi of the little and ring fingers, the ulna intrinsics and the hypothenar muscles and extend into the forearm) Predominantly neurological, intermittent and transient in nature Paresthesia in digits (variable distribution) on awakening Distal symptoms range from pain, aching ‘‘spasm’’ to tingling, numbness and tightness Feelings of weakness and fatigue either in the hand or entire upper limb (especially when it is used overhead) Feeling of tenderness, swelling or loss of motor control Pain in forearm, hands and wrist þ/ Pain in lower neck and shoulder, elbow and upper back, especially over pectoralis minor, lateral humerus, suprascapular and medial scapula regions þ/ Concurrent cervical pain and headache Pain aggravated by repetitive, suspensory, or sustained overhead forward elevation of the shoulder and activities that depress the shoulder girdle Pain at rest and night pain

Neurological TOS (nTOS)

assume that any one test or one investigation can always accurately examine the whole spectrum of pathology. Diagnosis of sTOS is dependent on a systematic, comprehensive upper-body examination and several authors highlight that postural exacerbation of symptoms is an essential component of the diagnosis (Roos and Owens, 1966; Novak et al., 1995). Lindgren (1997) first tried to systemize the diagnosis of sTOS by describing a clinical index (Fig. 2). While this index is a good initial guideline, there are other criteria that need to be added to ensure that the sTOS diagnosis is not missed in patients.

monitored as well as any changes in skin temperature, color, texture, blotching, hair growth, swelling, stiffness or loss of motor control. Less commonly seen are symptoms of tachycardia or pseudoangina, occipital headache, vertigo, dizziness, and tinnitus (Malas and Ozcakar, 2006). Behaviour of the symptoms should be noted including, morning and/or night pain and any specific

Patients should have at least three of the following four symptoms or signs. 1. a history of aggravation of symptoms with the arm in an elevated position

7.1. Subjective examination A detailed global body chart must be completed looking for total distribution of pain, neurological and vascular symptoms not only in the upper limb but in the head, neck, chest and the other side. In particular the type, nature and intensity of symptoms should be

2. a history of paraesthesia originating from the spinal segments C8/T1. 3. supraclavicular tenderness over the brachial plexus 4. a positive hands up abduction/external rotation or stress test. Fig. 2. Clinical index for diagnosis of sTOS (Lindgren, 1997).

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595

589

Table 2 Differential diagnosis. Differential

Signs in common with TOS

Differing signs

Investigations/Tests

Carpal tunnel syndrome

Paresthesia of the hand (can be the entire hand) Proximal pain Night pain Hand pain aggravated by use Pain over lateral wrist and thumb

Loss of wrist range of motion (predominantly extension)

Wrist range of motion Tinel’s sign Phalen’s and reverse Phalen’s Tethered median nerve stress test (Pascarlei) EMG and nerve conduction

Local tenderness and swelling Pain – resisted thumb extension Pain – passive thumb flexion Pain and point tenderness lateral epicondyle Pain – resisted wrist extension, gripping and morning stiffness Pain and point tenderness medial epicondyle Pain – resisted wrist flexion and wringing activities Changes in the color and temperature of the skin over the affected limb, skin sensitivity, sweating, swelling and changes in nail and hair growth. Ptosis of the eye and a constricted pupil

Finkelstein’s test

deQuervain’s tenosynovitis Lateral epicondylitis

Pain in lateral forearm

Medial epicondylitis

Pain in medial forearm

Complex regional pain syndrome (CRPS I or II).

‘‘Burning’’ pain in the upper limb, Motor disability

Horner’s Syndrome

Can co-exist with TOS due to compression affecting nerves as well as stellate ganglion Vasospastic disorder mimic TOS Discolouration fingers and cold sensitivity

Raynaud’s disease

Cervical disease (especially disc)

May present with pain in cervical spine, radiating in to the upper limb and medial scapula

Brachial plexus trauma Systemic disorders: inflammatory disease, esophageal or cardiac disease Upper extremity deep venous thrombosis (UEDVT), Paget– Schroetter syndrome

Varying from a neuropraxia to a neurotmesis Upper limb pain þ/ chest pain

Tightness or ‘‘heaviness’’ in affected biceps muscle, shoulder, neck, upper back and axilla Provocation tests are positive

Rotator cuff pathology

Restricted and painful shoulder range of motion Weakness in shoulder muscles

Glenohumeral joint instability

History of repeated overuse in the overhead position or trauma ‘‘Dead arm’’ symptoms or transient neurological symptoms

Discolouration also of toes (occasionally other extremities) in a characteristic pattern in time: white, blue and red Symptoms aggravated by cervical movements rather than arm motion. Ease factor may be elevation of the arm whilst this is an aggravating position in TOS

Hand, upper arm, posterolateral shoulder can be swollen and red with increased tissue temperature over the shoulder Painful limitation of internal and external rotation active motion may be present as well as positive rotator cuff tests Ecchymosis and non-edematous swelling of the shoulder, arm and hand, functional impairment, discolouration and mottled skin and distention of the cutaneous veins of the involved upper extremity Positive rotator cuff testing

Positive glenohumeral instability testing

Ultrasound scan

Ultrasound scan

Investigation autonomic nervous system

Radiological, autonomic and neurological investigation to differentiate. May need to be excluded from vTOS by an angiogram Allen’s test Cervical range of motion Neurological examination (decreased reflex in severe disc pathology) Cervical compression and distraction tests Spurling’s maneuver MRI Brachial Plexus Traction test Nerve conduction tests Blood tests (inflammation) Stress electrocardiography (cardiac disease)

This condition can cause a potentially dangerous or even fatal complication.

Clinical tests: - Neer and Hawkins impingement tests - Jobe (supraspinatus) test - Speed’s test (biceps) - External rotation test (infraspinatus) - Lift off & press belly test (subscapularis). Clinical tests: - Apprehension test, - Anterior and posterior draw tests in the adducted & abducted shoulder - The sulcus test - Dynamic anterior & posterior stability tests

590

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595

aggravating factors especially; sustained shoulder elevation, suspensory holding activities, lying on the arm, carrying a back pack, carrying articles by the side, prolonged postures (especially sitting), repetitive use of the upper limb and hand dexterity. A detailed history should include the past history of prior traumatic insult to the surrounding neck, shoulder and arm areas that may indicate co-existence of cervical, glenohumeral (especially instability), acromioclavicular or sternoclavicular joint pathology that may confound, confuse or contribute to the clinical presentation (Barkhordarian, 2007). Loss or gain of weight or muscle mass (especially scalenes or pectoralis minor region) should be noted as should a history of use of growth hormone or steroids (Simovitch et al., 2006). 7.2. Physical examination The physical examination of TOS is frequently long and complex as the clinician needs to examine the entire upper limb and cervical spine. Not only is a neurological examination required, but frequently peripheral nerve entrapment tests also need to be performed. 7.2.1. Postural alignment Postural malalignment should be examined. The physique of classic TOS patients is that of a long neck with sloping shoulders (Kai et al., 2001). Many other variations of scapula malpositioning or ‘‘poor posture’’ may also occur in TOS (Pascarelli and Hsu, 2001). If sTOS is suspected then specific attention should be made to scapula position both at rest, motion and on loading (Refer to Part 2). 7.2.1.1. Palpation. Upper limb pain or symptom reproduction after digital palpation and palpation tenderness (mechanical alodynia) (Schwartzman and Maleki, 1999), especially in the supra and infraclavicular fossae, are considered to be useful in the diagnosis of nTOS. Morley test or the brachial plexus compression test (compression of the brachial plexus in the supraclavicular region) is considered ‘‘positive’’ if there is reproduction of an aching

sensation and typical localized paresthesia and not just mere tenderness of the area (Hasan and Romeo, 2001). This test is reported to be positive in up to 68% of patients with nTOS (Seror, 2005). In some cases fullness or even a palpable hard mass may be present in the supraclavicular region (Cagli et al., 2006). This may be an indicator of a true structural lesion potentially creating either vTOS or tnTOS but the mass itself must also be examined (chest xray and ultrasound) to make sure it is not of a more significant nature (Ozguclu and Ozcakar, 2006). Palpation distally may also be required if local joint pathology or peripheral nerve entrapment needs to be excluded. 7.2.1.2. Active/passive motion. Active and passive motions of the cervical spine, cervicothoracic junction, shoulder, elbow, wrist and hands should be performed looking for; joint hyperlaxity, limitation of motion, dyskinesia or abnormal compensatory motions or symptom reproduction (Pascarelli and Hsu, 2001). At a minimum, cervical and shoulder range of motion should be objectively documented using a goniometer or inclinometer at initial assessment. Restriction of glenohumeral joint range of motion has been noted by several authors in sTOS (Sucher, 1990; Aligne and Barral, 1992; Rayan, 1998). This restriction may be due to the increased anterior tilt of the scapula. Any shoulder, scapula, elbow, wrist or hand muscle weakness should also be objectively assessed preferably using an objective assessment device (such as a dynamometer) or at the very least by using the standard 0–5 classification (Kendall et al., 1971). 7.2.1.3. Rotator cuff tests and glenohumeral joint instability tests. Rotator cuff tests are examined for pain, weakness, and symptom reproduction to assess rotator cuff pathology (Table 2). If there is a history of repeated overuse in the overhead position (throwing athlete) or trauma, then the glenohumeral joint should be examined for instability (Table 2). 7.2.1.4. Neurological examination. A thorough neurological examination of the upper extremities, including motor, sensory and deep tendon reflexes is essential. Sensation can be measured to light

Fig. 3. Adson’s maneuver. A. Patient seated upright. Arms remain supported in patient’s lap and the patient performs cervical spine rotation and extension to the tested side. This is followed by a deep inspirational breath, which is held for up to 30 s, as the examiner palpates for any changes in the radial pulse. B. Modification – perform in 15 shoulder abduction and maintain the head in the tested position for 1 min while the subject breathes normally.

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595

touch and pin prick at a minimum but if possible by Semmes– Weinstein monofilament testing (Gillenson et al., 1998). Attention should be given to; skin temperature, presence of tremor, atrophy and swelling (Pascarelli and Hsu, 2001). A decrease in sensation and strength in the absence of any aberrance of the deep tendon reflexes may indicate tnTOS. Any change in deep tendon reflexes (regardless of any change in sensation and motor control) may indicate a more proximal or central neurological pathology and needs to be referred on for further investigation. Muscle weakness will be manifested in either C5,6 muscle groups (upper plexus) or C8, T1 muscle groups (lower plexus) reflected by poor grip strength. This is not common and largely presents in tnTOS (Athanassiadi et al., 2001). 7.2.1.5. Peripheral nerve tests. There are many peripheral examination tests that can be performed. Carpal tunnel syndrome (CTS) is the most commonly cited peripheral nerve entrapment that may be

591

confused with TOS and therefore should be assessed as part of the standard physical examination (Seror, 2004, 2005). Further tests may be required as part of differential diagnosis (Table 2). 7.2.1.6. Cervical spine. In addition to active/passive range of motion, scalene muscle tightness should be examined. Restriction of cervical range and scalene muscle tightness is more likely associated with upper plexus entrapment (Skandalakis and Mirilas, 2001). Cervical nerve root compression caused by cervical disc disease should be excluded (Table 2) using a test such as Spurling’s test (Spurling and Bradford, 1939; Bradford and Spurling, 1942). Thoracic spine kyphosis or scoliosis should be noted and any compensatory lordosis (Sucher, 1990). 7.2.1.7. Provocation testing. The provocation tests most commonly described in the literature to diagnose TOS are presented in Figs. 3–6. These tests are purported to help delineate the possible level of compression of the neurovascular structures in either the

Fig. 4. a – Costoclavicular maneuver. Patient sitting, therapist assists the patient in performing scapula retraction (A), depression (B), elevation (C) and protraction (D), holding each position for up to 30 s. Subject rests his or her forearms on thighs while the examiner simultaneously monitors a change in pulse and symptom onset, note which positions exacerbates/eases symptoms. Recommended modification: performed with both arms by the side, holding each position for 1 min. b – Modified to the military brace position – exaggerates backward and downward bracing of the shoulders. This movement obliterates the pulses most readily.

592

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595

Fig. 5. Wright’s test – Hyperabduction maneuver. The test is performed in two steps. The patient sits in a comfortable position, head forward, while the arm is passively brought into abduction and external rotation to 90 without tilting the head. The elbow is flexed no more than 45 . The arm is then held for 1 min (Rayan and Jensen, 1995). The tester monitors the patient’s symptom onset and the quality of the radial pulse. The test is repeated with extremity in hyperabduction (end range of abduction).

scalene, costoclavicular or axillary (sub-coracoid) intervals. Given the numerous possible causes and symptoms associated with TOS, no single test can unequivocally establish the presence or absence of the condition, particularly where sTOS is concerned (Roos, 1982; Lindgren, 1997). The classic provocation tests have been reported to be unreliable and frequently positive (up to 90%) for pulse obliteration in healthy patients (Hachulla et al., 1990; Urschel et al., 1994; Rayan and Jensen, 1995; Nannapaneni and Marks, 2003). No study to date has analyzed the specificity, sensitivity and predictability of the provocation tests in relationship to the separate categories of TOS. 7.2.1.7.1. Adson’s maneuver. This test is considered positive if there is an obliteration or diminution of the radial pulse and/or a precipitation of patient’s symptoms (Fig. 3) (Adson and Coffey,

Fig. 6. Roos stress test – EAST test (elevated arm stress test) The patient sits with the head in the neutral position, the arms abducted and externally rotated to 90 and the elbows flexed to 90 . The patient is then requested to flex and extend the fingers for up to 3 min. The examiner watches for any dropping of the extremity during this time, which could indicate fatigue or arterial compromise. The therapist should also observe the color of the distal extremity, comparing left with right and monitor symptoms onset.

1927; Leffert and Perlmutter, 1999). Distribution of pain þ/ paresthesia should be noted and graded as mild, moderate, severe (Rayan and Jensen, 1995). The importance of the obliteration of the pulse has been questioned, especially in nTOS (Gergoudis and Barnes, 1980). This test is thought to stress the scalene triangle but may also stress the contralateral scalene triangle, indirectly bringing on symptoms (Walsh, 1994). 7.2.1.7.2. Costoclavicular maneuver. This maneuver (Fig. 4) is thought to stress the costoclavicular interval where either the subclavian artery, vein or brachial plexus may be entrapped by structures such as subclavius or costocoracoid ligament (Falconer and Weddell, 1943). The test is positive when radial pulse changes and/or patient’s symptoms are provoked. 7.2.1.7.3. Wright’s test – hyperabduction maneuver. The stress hyperabduction test (Fig. 5) is thought to implicate the axillary interval (space posterior to pectoralis minor) in the etiology of TOS (Wright, 1945). The test has two components and a positive result is a decrease in the radial pulse and/or reproduction of the patient’s symptoms. Distribution and severity of symptoms should be recorded (Rayan and Jensen, 1995). The first part of the maneuver could implicate the subclavian vessels and plexus as they are stretched around the coracoid process (pectoralis minor impingement). The second part places the extremity in hyperabduction. A positive test is said to implicate the costoclavicular interval (Walsh, 1994). Other authors have described adding on the effect of cervical spine motion (flexion, extension, left and right rotation) (Seror, 2005). 7.2.1.7.4. Roos stress test – EAST test (elevated arm stress test). Originally described by Roos and Owens (1966) and purported by the developers to be the most sensitive and specific test to detect nTOS (Fig. 6). This test is believed to stress all three intervals (scalene, costoclavicular, axillary) since this position places the arterial, venous and nervous systems in tension. The test is positive when the patient is unable to maintain elevation for the 3-min period or when symptoms are induced (Roos and Owens, 1966; Walsh, 1994). Accuracy of the test is reported to be best at angles of 90 or less (Hachulla et al., 1990). Despite the test being deemed the most sensitive and specific of the provocation tests (Roos and Owens, 1966), a study by Seror (2005) showed that 14% of patients could not complete the 3-min test with their symptomatic upper limb and 58% of patients with confirmed CTS also had positive stress tests. In the same study only 5% of patients with CTS had a positive Adson’s test (Seror, 2005). 7.2.1.7.5. Other considerations. When using provocation tests for cases of vTOS then obliteration of the radial artery pulse, looking for distal ischaemic signs, oedema, and cyanosis of the upper extremity, measuring blood pressure and auscultation for a bruit in both upper extremities with the arms by the side and in provocation positions (Athanassiadi et al., 2001) is required and likely to be significant if found positive (Singh, 2006). In cases of nTOS it would be logical that provocation tests should not only be performed to obliterate the radial artery pulse but also to recreate the patient’s discomfort and symptoms (Konin et al., 1997). Due to the low specificity of these various tests, some authors argue that if these tests are being utilized for a diagnosis of sTOS then two or three tests should be positive in a given patient (Hachulla et al., 1990). 7.2.1.8. Postural and scapula correction. Exacerbation of symptoms during testing by alterations in posture is considered a strong argument for the diagnosis of sTOS (Hachulla et al., 1990; Rayan and Jensen, 1995). Poor posture or malalignment of the shoulder girdle (such as drooping or rounded shoulders) has been cited by many authors as being a potential cause of sTOS due to the alteration of the anatomical position of the shoulder girdle potentially

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595

593

Fig. 7. Correction of scapula position – Elevation/Upward Rotation. Performed in standing with the examiner behind the patient. Patient’s symptoms are provoked either by performing an active motion (such as abduction) or one of the Provocation tests. The point in range or time to onset of symptoms is objectively noted. Examiner then places his/her hand in the patient’s axilla (A). The examiner’s thumb in the posterior axilla, fingers anterior. The scapula is then passively elevated until it is level with the other side (if the patient has unilateral symptoms) or to a level that approximates the normal resting position of the scapula. A small component (10 –15 ) of scapula upward rotation may also be added. Correction is maintained for 1 min as this will allow tractional forces to be relieved off the brachial plexus. Any alterations in the patient’s resting symptoms are noted. The patient then performs the active movement or provocation test whilst the examiner maintains the passive correction force. Any alteration in patient’s symptoms – distribution, intensity, location or type (worsening or improvement) should be noted. A positive correction response is a significant reduction or absence of pain or an increased time duration in the ability to hold provocation positions or perform the stress test before symptom onset.

decreasing the space available in either the scalene triangle, the thoracic outlet, costoclavicular space or sub-coracoid tunnel. Clinically we have found that manual correction of the scapula position is an extremely useful clinical sign to help establish the diagnosis of sTOS and to determine if rehabilitation strategies that focus on strengthening of the scapula stabilizers and altering the scapula position at rest and in motion are likely to be successful (see Figs. 7 and 8). Attempts should be made, where possible, to objectively document the scapula asymmetries observed (Watson et al., 2005). As a general rule, if correction of the scapula improves the patient’s symptoms then the test is positive. If the patient’s symptoms are aggravated or not changed by repositioning then the test is negative. This would indicate that either the wrong correction position for the scapula has been chosen or the patient may not have a form of TOS that will be assisted by rehabilitation strategies for the scapula. This may help establish the diagnosis of either vTOS or nTOS and may indicate greater likelihood that surgical intervention is required. 8. Differential diagnosis The first step in the differential diagnosis of TOS is to separate it from other painful conditions of the upper extremity and neck. Other pathologies may mimic TOS or have some clinical overlap (Table 2). It should be taken into account that co-existence of pathology can occur. Upton and McComas (1973) introduced the ‘double crush’ hypothesis, stating that a proximal level of compression could cause more distal sites along the nerve to be more susceptible to compression (Mackinnon, 1994). This hypothesis is extremely pertinent for the patient with nTOS who may be symptomatic from a combination of multiple levels of nerve compression. Each site in and of itself may not be significant to produce symptoms but the cumulative effect of minor

compression at several sites along the nerve will result in significant symptoms. The most commonly seen clinical picture is the association of carpal and ulnar nerve compression with TOS (Nannapaneni and Marks, 2003) but a similar phenomenon has been reported with cervical spine pathology and TOS (Kai et al., 2001). 9. Treatment Treatment strategies for TOS, particularly with regard to surgical intervention, remain highly controversial. The available literature does not provide strong support either for or against surgery or conservative management (Degeorges et al., 2004). The sub-type of TOS to some extent determines the appropriate treatment pathway. Part 2 of this article will comprehensively outline conservative management. vTOS generally requires surgical treatment and surgery usually involves decompression of the thoracic outlet with removal of the cervical rib (if present) and/or first rib excision together with associated muscles and other soft tissue structures as indicated (Gergoudis and Barnes, 1980; Urschel and Razzuk, 1991; Bondarev et al., 1992; Atasoy, 1996; Pupka et al., 2004). The general consensus is that surgery is usually required for aTOS since there is often a structural lesion demonstrated. The decision to operate for venous symptoms is often more difficult as many patients have no bony structures that can be proven responsible for compression. Initially conservative management may be trialed (thromboembolytic therapy and monitoring) but if symptoms persist or progress then decompression may be required (Jamieson and Chinnick, 1996; Azakie et al., 1998; Sultan et al., 2001). In tnTOS there is a high association with structural anomalies (such as a cervical rib) and objective confirmatory tests are positive, potentially justifying surgical intervention. Despite this, many authors still recommend a trial of conservative treatment and only

594

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595

References

Fig. 8. Scapula correction for posterior tilt. Performed when there is an increased anterior tilt or winging of the scapula. Examiner then places one hand anteriorly over the coracoid process and the other hand posteriorly over the blade of the scapula. The scapula is then passively tilted posteriorly and pressure maintained for 1 min. Any alterations in the patients resting symptoms are noted. The patient then reperforms the active movement or provocation test whilst the examiner maintains the passive correction force. If symptoms are worsened with posterior tilt then the test should be repeated applying correction of elevation as well as posterior tilt.

perform surgery if neurological symptoms such as muscle wasting progress (Dale, 1982; Mingoli et al., 1995; Sanders and Hammond, 2002; Degeorges et al., 2004). In sTOS there is often no obvious structural cause and objective confirmatory testing may be lacking. The optimal approach for both surgical and conservative treatment remains controversial and variable (Lindgren, 1997; Sharp et al., 2001). Conservative management is almost universally accepted as the first step (Sharp et al., 2001). 10. Conclusion To diagnose TOS is a difficult process that requires time and effort. Given that the etiology of TOS is multifactorial and the signs and symptoms so varied, it would appear logical that physical therapy can successfully be employed in the optimal management of TOS patients (both conservative and surgical). There is a need for the development of a systemized approach to conservative management for TOS (refer to Part 2). If a better objective framework can be established this could facilitate communication between the disciplines to improve patient selection for both surgical and conservative treatment and help develop treatment algorithms that do reliably achieve consistently good or excellent objective treatment outcomes that are sustainable.

Adson AW, Coffey JR. Cervical rib: a method of anterior approach for relief of symptoms by division of the scalenus anticus. Annals of Surgery 1927; 85(6):839–57. Aligne C, Barral X. Rehabilitation of patients with thoracic outlet syndrome. Annals of Vascular Surgery 1992;6(4):381–9. Atasoy E. Thoracic outlet compression syndrome. Orthopedic Clinics of North America 1996;27(2):265–303. Athanassiadi K, Kalavrouziotis G, Karydakis K, Bellenis I. Treatment of thoracic outlet syndrome: long-term results. World Journal of Surgery 2001;25(5):553–7. Azakie A, McElhinney DB, Thompson RW, Raven RB, Messina LM, Stoney RJ. Surgical management of subclavian-vein effort thrombosis as a result of thoracic outlet compression. Journal of Vascular Surgery 1998;28(5):777–86. Barkhordarian S. First rib resection in thoracic outlet syndrome. Journal of Hand Surgery 2007;32(4):565–70. Bondarev VI, Kiandarian AK, Ablitsov NP, Baziak AP. New approaches in diagnosis and therapy of the thoracic outlet syndrome. Klinichna Khirurhia 1992;11:43–5. Bradford RK, Spurling RG. The intervertebral disc with special reference to the rupture of the annulous fibrosus with herniation. Journal of Nervous and Mental Disease 1942;95(6):768. Cagli K, Ozcakar L, Beyazit M, Sirmali M. Thoracic outlet syndrome in an adolescent with bilateral bifid ribs. Clinical Anatomy 2006;19(6):558–60. Cherington M. A conservative point of view of the thoracic outlet syndrome. American Journal of Surgery 1989;158(5):394–5. Cooke RA. Thoracic outlet syndrome – aspects of diagnosis in the differential diagnosis of hand-arm vibration syndrome. Occupational Medicine 2003; 53(5):331–6. Dale WA. Thoracic outlet compression syndrome. Critique in 1982. Archives of Surgery 1982;117(11):1437–45. Davidovic LB, Kostic DM, Jakovljevic NS, Kuzmanovic IL, Simic TM. Vascular thoracic outlet syndrome. World Journal of Surgery 2003;27(5):545–50. Degeorges R, Reynaud C, Becquemin JP. Thoracic outlet syndrome surgery: longterm functional results. Annals of Vascular Surgery 2004;18(5):558–65. Demondion X, Bacqueville E, Paul C, Duquesnoy B, Hachulla E, Cotten A. Thoracic outlet: assessment with MR imaging in asymptomatic and symptomatic populations. Radiology 2003;227(2):461–8. Falconer MA, Weddell G. Costoclavicular compression of the subclavian artery and vein. Costoclavicular compression of the subclavian artery and vein. Lancet 1943;2:539–43. Gergoudis R, Barnes RW. Thoracic outlet arterial compression: prevalence in normal persons. Angiology 1980;31(8):538–41. Gillenson SP, Parets N, Bear-Lehman J, Stanton DB. The effect of wrist position on testing light touch sensation using the Semmes–Weinstein pressure aesthesiometer: a preliminary study. Journal of Hand Therapy 1998;11(1):27–31. Gockel M, Vastamaki M, Alaranta H. Long-term results of primary scalenotomy in the treatment of thoracic outlet syndrome. Journal of Hand Surgery [Br] 1994;19(2):229–33. Goff CD, Parent FN, Sato DT, Robinson KD, Gregory RT, Gayle RG, et al. A comparison of surgery for neurogenic thoracic outlet syndrome between laborers and nonlaborers. American Journal of Surgery 1998;176(2):215–8. Gruber E. Cervical rib; report of a case. South African Medical Journal 1952;26(27):551–2. Hachulla E, Camilleri G, Fournier C, Vinckier L. Clinical, flowmetric and radiologic study of the thoracic outlet in 95 healthy subjects: physiologic limitations and practical impact. Revue De Medecine Interne 1990;11(1):19–24. Hasan SS, Romeo AA. Thoracic outlet syndrome secondary to an anomalous subclavius muscle. Orthopedics 2001;24(8):793–4. Jain S, Monbaliu D, Thompson JF. Thoracic outlet syndrome caused by chronic retrosternal dislocation of the clavicle. Successful treatment by transaxillary resection of the first rib. Journal of Bone and Joint Surgery 2002;84B(1):116–8. Jamieson WG, Chinnick B. Thoracic outlet syndrome: fact or fancy? A review of 409 consecutive patients who underwent operation. Canadian Journal of Surgery 1996;39(4):321–6. Kai Y, Oyama M, Kurose S, Inadome T, Oketani Y, Masuda Y. Neurogenic thoracic outlet syndrome in whiplash injury. Journal of Spinal Disorders 2001;14(6):487–93. Kendall HO, Kendall FP, Wadsworth GE. Muscles, testing and function. 2nd ed. Baltimore: Williams and Wilkins; 1971. Konin J, Wiksten D, Isear J. Special tests for orthopedic examination. New Jersey: Slack Incorporated; 1997. Lee AD, Agarwal S, Sadhu D. Doppler Adson’s test: predictor of outcome of surgery in non-specific thoracic outlet syndrome. World Journal of Surgery 2006;30(3):291–2. Leffert RD, Perlmutter GS. Thoracic outlet syndrome. Results of 282 transaxillary first rib resections. Clinical Orthopedics and Related Research 1999; (368): 66–79. Lindgren KA. Conservative treatment of thoracic outlet syndrome: a 2-year followup. Archives of Physical Medicine and Rehabilitation 1997;78(4):373–8. Lindgren KA, Oksala I. Long-term outcome of surgery for thoracic outlet syndrome. American Journal of Surgery 1995;169(3):358–60. Machleder HI, Moll F, Verity MA. The anterior scalene muscle in thoracic outlet compression syndrome. Histochemical and morphometric studies. Archives of Surgery 1986;121(10):1141–4.

L.A. Watson et al. / Manual Therapy 14 (2009) 586–595 Mackinnon SE. Thoracic outlet syndrome. Annals of Thoracic Surgery 1994;58(2):287–9. Makhoul RG, Machleder HI. Developmental anomalies at the thoracic outlet: an analysis of 200 consecutive cases. Journal of Vascular Surgery 1992;16(4):534–42. Malas FU, Ozcakar L. Legends of thoracic outlet syndrome. Rheumatology International 2006;27(1):109–10. Mingoli A, Feldhaus RJ, Farina C, Cavallari N, Sapienza P, di Marzo L, et al. Long-term outcome after transaxillary approach for thoracic outlet syndrome. Surgery 1995;118(5):840–4. Nannapaneni R, Marks SM. Neurogenic thoracic outlet syndrome. British Journal of Neurosurgery 2003;17(2):144–8. Novak CB, Collins ED, Mackinnon SE. Outcome following conservative management of thoracic outlet syndrome. Journal of Hand Surgery 1995;20(4):542–8. Ozguclu E, Ozcakar L. Supraclavicular mass disguising as thoracic outlet syndrome. Rheumatology International 2006;26(8):777–8. Pascarelli EF, Hsu YP. Understanding work-related upper extremity disorders: clinical findings in 485 computer users, musicians, and others. Journal of Occupational Rehabilitation 2001;11(1):1–21. Pupka A, Rucinski A, Skora J, Janczak D, Pawlowski S, Kaluza G, et al. The treatment of subclavian artery compression with the use of ringed polytetrafluoroethylene vascular prostheses. Polimery w Medycynie 2004;34(4):53–61. Ranney D. Thoracic outlet: an anatomical redefinition that makes clinical sense. Clinical Anatomy 1996;9(1):50–2. Rayan GM. Thoracic outlet syndrome. Journal of Shoulder and Elbow Surgery 1998;7(4):440–51. Rayan GM, Jensen C. Thoracic outlet syndrome: provocative examination maneuvers in a typical population. Journal of Shoulder and Elbow Surgery 1995;4(2):113–7. Rockwood Jr CA, Groh GI, Wirth MA, Grassi FA. Resection arthroplasty of the sternoclavicular joint. Journal of Bone and Joint Surgery 1997;79A(3):387–93. Roos DB. The place for scalenectomy and first-rib resection in thoracic outlet syndrome. Surgery 1982;92(6):1077–85. Roos DB, Owens JC. Thoracic outlet syndrome. Archives of Surgery 1966;93(1):71–4. Samarasam I, Sadhu D, Agarwal S, Nayak S. Surgical management of thoracic outlet syndrome: a 10-year experience. ANZ Journal of Surgery 2004;74(6):450–4. Sanders RJ, Hammond SL. Management of cervical ribs and anomalous first ribs causing neurogenic thoracic outlet syndrome. Journal of Vascular Surgery 2002;36(1):51–6. Schwartzman RJ, Maleki J. Postinjury neuropathic pain syndromes. Medical Clinics of North America 1999;83(3):597–626. Seror P. Medial antebrachial cutaneous nerve conduction study, a new tool to demonstrate mild lower brachial plexus lesions. A report of 16 cases. Clinical Neurophysiology 2004;115(10):2316–22. Seror P. Frequency of neurogenic thoracic outlet syndrome in patients with definite carpal tunnel syndrome: an electrophysiological evaluation in 100 women. Clinical Neurophysiology 2005;116(2):259–63. Sharp WJ, Nowak LR, Zamani T, Kresowik TF, Hoballah JJ, Ballinger BA, et al. Longterm follow-up and patient satisfaction after surgery for thoracic outlet syndrome. Annals of Vascular Surgery 2001;15(1):32–6.

595

Sheth RN, Belzberg AJ. Diagnosis and treatment of thoracic outlet syndrome. Neurosurgery Clinics of North America 2001;12(2):295–309. Shukla PC, Carlton Jr FB. Diagnosis of thoracic outlet syndrome in the emergency department. Southern Medical Journal 1996;89(2):212–7. Simovitch RW, Bal GK, Basamania CJ. Thoracic outlet syndrome in a competitive baseball player secondary to the anomalous insertion of an atrophic pectoralis minor muscle: a case report. American Journal of Sports Medicine 2006;34(6): 1016–9. Singh D. Arterial complications of thoracic outlet syndrome. Surgical Practice 2006;10:52–6. Skandalakis JE, Mirilas P. Benign anatomical mistakes: the thoracic outlet syndrome. American Surgeon 2001;67(10):1007–10. Sobey AV, Grewal RP, Hutchison KJ, Urschel JD. Investigation of nonspecific neurogenic thoracic outlet syndrome. Journal of Cardiovascular Surgery 1993;34(4):343–5. Spurling RG, Bradford RK. Neurologic signs in trauma of the brain and spinal cord. Southern Medical Journal 1939;32(1):59–65. Sucher BM. Thoracic outlet syndrome – a myofascial variant: part 2. Treatment. Journal of the American Osteopathic Association 1990;90(9):810–2. 817–823. Sultan S, Evoy D, Eldin AS, Eldeeb M, Elmehairy N. Atraumatic acute upper limb ischemia: a series of 64 patients in a Middle East tertiary vascular center and literature review. Vascular Surgery 2001;35(3):181–97. Upton AR, McComas AJ. The double crush in nerve entrapment syndromes. Lancet 1973;2(7825):359–62. Urschel Jr HC, Razzuk MA. Improved management of the Paget–Schroetter syndrome secondary to thoracic outlet compression. Annals of Thoracic Surgery 1991;52(6):1217–21. Urschel Jr HC, Razzuk MA. Upper plexus thoracic outlet syndrome: optimal therapy. Annals of Thoracic Surgery 1997;63(4):935–9. Urschel JD, Hameed SM, Grewal RP. Neurogenic thoracic outlet syndromes. Postgraduate Medical Journal 1994;70(829):785–9. van Es HW. MRI of the brachial plexus. European Radiology 2001;11(2):325–36. Walsh MT. Therapist management of thoracic outlet syndrome. Journal of Hand Therapy 1994;7(2):131–44. Watson L, Balster SM, Finch C, Dalziel R. Measurement of scapula upward rotation: a reliable clinical procedure. British Journal of Sports Medicine 2005;39(9): 599–603. Wilbourn AJ. The thoracic outlet syndrome is overdiagnosed. Archives of Neurology 1990;47(3):328–30. Wright IS. The neurovascular syndrome produced by hyperabduction of the arms. The immediate change produced in 150 normals and the effects on some persons of prolonged hyperabduction of the arms as in sleeping and in certain occupations. American Heart Journal 1945;29:1–19. Wright D, Jennings PR. Thoracic outlet syndrome. Journal of the American Academy of Physician Assistants 2005;18(5):57–8. Yanaka K, Asakawa H, Matsumaru Y, Kujiraoka Y, Nose T. Diagnosis of vascular compression at the thoracic outlet using magnetic resonance angiography. European Neurology 2004;51(2):122–3.

Manual Therapy 14 (2009) 596–604

Contents lists available at ScienceDirect

Manual Therapy journal homepage: www.elsevier.com/math

Systematic Review

The effect of age on lumbar range of motion: A systematic review Pattariya Intolo a, Stephan Milosavljevic a, *, David G. Baxter a, Allan B. Carman a, Poonam Pal a, Joanne Munn b a b

Centre for Physiotherapy Research, School of Physiotherapy, University of Otago, Dunedin 9015, New Zealand Faculty of Health Sciences, University of Sydney, Cumberland Campus, Australia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 September 2008 Received in revised form 22 July 2009 Accepted 6 August 2009

A systematic review and meta-analysis to determine the effect of age on lumbar range of motion (ROM). Assessment of lumbar ROM is commonly used in spinal clinical examination. Although known to reduce with advancing age, it is unclear how this occurs across different age bands; how this compares between movement planes; and what differences exist between males and females. Ten electronic databases were searched to find studies matching predetermined inclusion criteria. Methodological quality was assessed with a quality assessment tool for quantitative studies. Evidence for effect of age on ROM in all planes was investigated with meta-analyses. Sixteen studies met inclusion criteria with results showing age-related reductions in flexion, extension and lateral flexion particularly from 40 to 50 and after 60 years of age. There was very little age effect on lumbar rotation. There is strong evidence for a non-linear age-related reduction in lumbar sagittal and coronal ROM after 40 years of age that also appears to be asymmetric in the coronal plane. These factors should be considered during the evaluation of spinal ROM in patients who present with lumbar disorders. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Age Lumbar Range of motion Mobility

1. Introduction Low back pain (LBP) is a common and costly health problem (Dagenais et al., 2008). Back injury claims cost the Accident Compensation Corporation (ACC) of New Zealand NZ$233 million in compensation in 2002/2003 (Pal et al., 2006) while they are estimated to be £1632 million per year (Maniadakis and Gray, 2000) in the UK. Back problems have a lifetime prevalence ranging from 52% to 91% across all age groups (Jin et al., 2004; Raspe et al., 2004; Walker et al., 2004), and prevalence increases as age progresses. There is debate regarding lumbar range of motion (ROM) as a predictor of successful rehabilitation in LBP with recent evidence suggesting angular velocity and acceleration may be more sensitive indicators (Marras, 2005). Although such dynamic measures are plausible directions for future research, technological and time restraints limit their use in clinical examinations. Clinical assessment of movement impairment in LBP is still most commonly quantified by ROM, being used to guide treatment and assess the patient’s response. Although lumbar ROM reduces with advancing

age it is still unclear how this reduction occurs across different age categories and clinicians may be uncertain of normative expectations when considering age and sex of a given patient. Thus it may be important to know whether movement reduces with age and whether it does this consistently across different age strata. Assessment of spinal ROM is done with a variety of equipment, procedures and analyses. A number of these studies use variable age categories (Moll and Wright, 1971; Einkauf et al., 1987; Burton and Tillotson, 1988; McGill et al., 1999; Tully et al., 2002), do not address sex differences in ROM (Fitzgerald et al., 1983; Einkauf et al., 1987; Milosavljevic et al., 2005), and do not investigate all planar movements (Einkauf et al., 1987; Russell et al., 1993; McGill et al., 1999; Tully et al., 2002; Milosavljevic et al., 2005). Uncertainty regarding how lumbar ROM reduces across age categories, and how sex may affect such movement is the prime driver for the current review. Our aim is to systematically examine the evidence for effect of age on lumbar ROM in healthy male and female participants. The criteria focused on non-invasive procedures for measuring ROM. 2. Methods

* Corresponding author. Centre for Physiotherapy Research, School of Physiotherapy, University of Otago, PO Box 56, Dunedin 9015, New Zealand. Tel.: þ64 3 479 7193; fax: þ64 3 479 8414. E-mail address: [email protected] (S. Milosavljevic). 1356-689X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2009.08.006

2.1. Literature search Electronic searches included Ovid; Medline; CINAHL; PEDro; ScienceDirect; Scopus; PubMed; ProQuest; EMBASE; and Web of

P. Intolo et al. / Manual Therapy 14 (2009) 596–604

Science. The search strategy used combinations of the terms ‘age’, ‘healthy’, ‘lumbar’, and ‘ROM’. Manual searches of relevant review bibliographies and reference lists of primary studies were undertaken to look for possible studies not captured by the electronic search.

597

2.4. Participants Studies that included healthy male and/or female participants in any age ranges who free of LBP were considered for review. In addition, participants were required to have had no history of serious spinal or hip joint trauma, including surgery; and/or no local or systematic disease likely to affect the spine.

2.2. Experimental design In order to determine initial relevance for inclusion, citation postings were independently screened by two reviewers (PI and PP). Discussion between the reviewers led to a consensus for articles that met the criteria for abstract review. If abstract review indicated that inclusion criteria were met the full article was extracted. Following independent review of these manuscripts the reviewers discussed whether consensus had been met for inclusion criteria (Fig. 1), study design and participant inclusion. Consensus allowed the given study to be included in this review. A lack of consensus would lead to a third reviewer (JM) independently examining the manuscript and a decision made on majority opinion.

2.3. Study design Cross-sectional investigation of studies measuring lumbar ROM in healthy participants.

2.5. Outcomes Studies reporting lumbar ROM in different ages, including female and male participants. Studies reporting non-invasive procedures measuring lumbar ROM (e.g. 3 Space Isotrak) were included.

2.6. Methodological assessment Study quality was assessed with Quality Assessment Tool for Quantitative Studies, developed by the Effective Public Health Practice Project 2003, Canada (Jackson et al., 2005). Two reviewers (PI and PP) separately evaluated all included studies for quality rating. When reviewers could not agree on a quality rating a third reviewer (JM) was asked to review and make judgment on study quality. All studies were rated according to the components in Table 2 including selection and allocation bias, confounders, blinding, data collection methods,

Fig. 1. Selection of studies for inclusion in systematic review.

598

P. Intolo et al. / Manual Therapy 14 (2009) 596–604

withdrawals and drop-outs, and statistical analysis. These ratings were judged as strong, moderate or weak. 2.7. Data extraction Data for means and standard deviations of lumbar ROM for the different age categories and directions of movement in both females and males (from reported values or extrapolated from figures) and study sample size were extracted by PI. Where relevant data were unavailable, additional data were requested from authors of these studies. Extracted data were then checked for accuracy by a second reviewer (PP). Disagreement was resolved by discussion and consensus. 2.8. Data synthesis The mean in degrees and estimated standard deviation for flexion, extension, left and right lateral flexion, and left and right rotation ROM (in degrees) as well as sample sizes for each age group were extracted for all pooled data. Results of individual studies were pooled across age group categories for similar measurement protocols using Meta-analysis Interactive eXplanations-version 1.54 (MIXTM) software employing a random effects model and reported as mean difference (X2–X1, 95%CI) (Egger et al., 1997, 1998). Statistical significance was accepted at p < 0.05. Data were calculated for flexion, extension, right and left lateral flexion, right and left rotation within the relevant age and sex groups. This software requires the use of the mean and standard deviation of ROM, as well as the sample size for each chosen age strata in each sex group, allowing calculation of 95% confidence intervals (CIs) for age band within each sex category in order to estimate the difference between two population means in different age groups. Statistical tests were considered significant at a level of a ¼ 0.05. 3. Results A title review was conducted on 511 extracted articles with 19 relevant manuscripts identified and full papers obtained. Seven were excluded, where five used invasive radiological measures (Pearcy and Tibrewel, 1984; Pearcy et al., 1984; Hayes et al., 1989; Harada et al., 2000; Wong et al., 2004), one did not meet participant selection criteria (Twomey, 1979) and one duplicated previously reported results (Troke et al., 2001, 2005). Four further studies were identified from the reference lists of the remaining articles (Fitzgerald et al., 1983; Einkauf et al., 1987; Hindle et al., 1990; Dvorak et al., 1995). A total of 16 studies were therefore included in this systematic review (Fig. 1, Table 1). Total participants available for meta-analysis included 1323 female and 1001 male participants aged between 8 and 90 years who were described as being in good health. 3.1. Methodological quality Study ratings varied (Table 2) with four not reporting data for height, weight, body mass index (BMI) and recreational activity (Batti’e et al., 1987). All articles described either reliability or validity of measurement devices, three indicated the percentage of participants completing the study. Although the majority provided sample size power calculations (n ¼ 15), substantial differences were noted among all manuscripts for age group descriptions. 3.2. Participants Two studies included participants who reported no back pain within the past year; five included participants who were free of LBP for at least six months; two included those who were free of

LBP within the last three months; and seven described participants with no current LBP and no previous pathology affecting the spine (Table 1). Burton and Tillotson (1988) divided subjects into 20 year age spans (16–34, 35–54 years old) while Vachalathiti et al. (1995) divided subjects into 15 year age ranges. A further 10 studies divided the age of subjects into decades as follows; 20–29 years and 30–39 years. Two studies categorized age of subjects into either 15–24 years or 16–24 years of age. Tully et al. (2002) divided participants into two age groups 8–10 and 18–23 years old. McGill et al. (1999) studied two distinct mean age groups; 21 years (3.4) and 64 years (3.5) (Table 1). Ultimately 7 of the 16 reviewed articles had sufficiently common criteria for inclusion in at least one of the planar meta-analyses. Thus data for 109 females and 154 males were available for meta-analysis. 3.3. Instrumentation Four studies used the 3 Space Isotrak tracking system (McDonnel Douglas Electronics Company, VT, USA); three used the CA-6000 spinal motion analyzer (Orthopedic Systems, Incorporate, Hayward, CA, USA); and three used tape measures or goniometry. The remaining six studies either used a motion analysis system (Motion Analysis CorporationÔ, CA, USA), a fluid-filled inclinometer (MEDesign Ltd., Southport, UK), Flexicurve, a B-200 Lumbar dynamometer (Isotechnologies, North Carolina, USA), a geometric CAD process (Northern Digital Inc, Ontario, Canada), or videorecording (Table 1). Studies with similar methodology and similar age categories included the angular measures of Fitzgerald et al. (1983), Einkauf et al. (1987), Hindle et al. (1990), Russell et al. (1993), McGregor et al. (1995), Herp et al. (2000), Troke et al. (2005), and Milosavljevic et al. (2005) and were included in the data pool for meta-analysis. Flexion was linearly measured by distraction by Fitzgerald et al. (1983) and Einkauf et al. (1987) and thus the flexion results were not included in the meta-analysis. However these authors used goniometry to measure lumbar extension and lateral flexion thus allowing these angular measures to be included in the data pool. Although Dvorak et al. (1995) used a similar angular measurement methodology for all planes of movement the results were not included in the data pool as examiner overpressure in passive end range stance was applied prior to angular measurement. This procedure was not used by the other included authors. 4. Effect of age on lumbar ROM These results use the 20–29 year age band as the primary benchmark comparison for all other age bands in the expectation that this age band will likely demonstrate the greatest ROM against which reductions in motion within other age bands can be compared. 4.1. Females 4.1.1. Sagittal plane Data pooling (n ¼ 88) were used for four flexion (Russell et al., 1993; McGregor et al., 1995; Herp et al., 2000; Troke et al., 2005) and five extension (n ¼ 109) studies (Einkauf et al., 1987; Russell et al., 1993; McGregor et al., 1995; Herp et al., 2000; Troke et al., 2005). Although non-significant there was a trend for a small increase (2.4 ) in flexion for the 30–39 year group in comparison to the 20–29 year age group. There was a significant reduction in flexion (Fig. 2, Table 3) after 40 years of age with a mean difference of 3.5 when comparing the 20–29 to the 40–49 year age groups. A further significant reduction of 9.2 was observed between the

Table 1 Details of included studies. Author, date, country

Participants criteria

Burton and Tillotson, 1988, UK

Instruments/company, city

Position/Motion

Spinal level

Results

268F, 242 M no notable low 10 to >54 years old: 10–12, back trouble 16–34, 35–54, >54

Flexicurve

Sitting, prone lying/static

T12–S2

Dvorak et al., 1995, Switzerland

42F, 62M no history of LBP in 20–70 years old: 20–29, 30– the past year 39, 40–49, >50

Einkauf et al., 1987, USAa

109F no history of LBP in past 3 months

CA-6000 Spinal Motion Analyzer/ Standing/dynamic (Passive ROM) Orthopedic System, Incorporate, Hayward, CA, USA Distraction method, Goniometer Standing/static

Spinal mobility decreases with. advancing age. Males showed a reduction in flexion range in middle year whereas females showed reduced flexion younger, maintained that level through middle-age and have a further decline over 65 years of age. A normative database was established showing significantly decreased motion as age increased.

Fitzgerald et al., 1983, USAa

Gomez et al., 1991, Canada

Hindle et al., 1990, UK

McGill et al., 1999, Canada

McGregor et al., 1995, UKa

Milosavljevic et al., 2005, New Zealand Moll and Wright, 1971, UK

Russell et al., 1993, Australiaa

Sullivan et al., 1994, USA

Troke et al., 2005, UKa

Tully et al., 2002, Australia

Vachalathiti et al., 1995, Australia

20–84 years old: 20–29, 30– 39, 40–49, 50–59, 60–69, 70– 84 4F, 168M no LBP currently 20–82 years old: 20–29, 30– Distraction method Goniometer no history of LBP in past 3 39, 40–49, 50–59, 60–69, 70– 82 months 83F, 85M no history of LBP in 18–68 years old: 50 Carolina, USA back surgery 50F, 50M no history of 20–77 years old: 20–29, 30– 3 Space Isotrak, Polhemus recent LBP 39, 40–49, 50–59, 60þ Navigator Sciences, McDonnel Douglas Electronic Company Colchester, VT, USA 3 Space Isotrak, Polhemus 40F, 40M no history of LBP in 20 to >50 years old: 20–29, Navigation Science, McDonell past 6 months, no history of 30–39, 40–49, >50 Douglas Electronics Company, back surgery Chlchester, VT, USA 21  3.4 years old, 64  35 3 Space Isotrak, Polhemus 7F, 5M no history of low years old Navigation Science, McDonell back injury, or recent Douglas Electronics Company, recurrent pain Chlchester, VT, USA 20–70 years old: 20–29, 30– CA-6000 Spinal Motion Analyzer/ 100F, 103M no LBP Orthopedic System, Incorporate, currently, no history of LBP 39, 40–49, 50–59, 60–70 Hayward, CA, USA in past 6 months 128M no LBP 19–59 years old 20–29, 30–39, Geometric CAD/Northern Digital 40–49, 50–59 Inc, Waterloo, Ontario, Canada Distraction method 118F, 119M no LBP 15 to >75 years old: 15– 24,25–34, 35–44,45–54, 55– 64, 65–74, >75 78 F, 103M no history of LBP 20–69 years old: 20–29, 30– 3 Space Isotrak, Polhemus Navigation Science, McDonnell and any pathology affected 39, 40–49, 50–59, 60–69 Douglas Electronics Company, the spine Colchester, VT, USA 15–65 years old: 16–24, 25– Fluid-filled inclinometer/ 686F, 440M no previous 34, 35–44, 45–65 MEDesign Ltd., Southport, UK experience of LBP during lifetimes 196F, 209M no LBP currently 16–90 years old: 10–20, 21– CA-6000 Spinal Motion Analyzer/ no history of LBP in past 12 30, 31–40,41–50, 51–60, 61– Orthopedic System, Incorporate, Hayward, CA, USA months or pain in previous 6 70, 71–80, 81–90 months 8–10, 18–23 years old Videotape 22 Adults, 22 Children no movement dysfunction, no history of pathology or pain in the hip 20 to >60 years old: 20–35, Motion Analysis System/Motion 54 Female, 46 Male no Analysis CorporationTM Santa history or back or lower limb 36–59, >60 pain for at least 6 months Rosa, California, USA

TL junction–S

L-S

Spinal mobility decreases with advancing age.

Standing/static

L-S

Spinal mobility decreases with advancing age.

Standing/dynamic

L

ROM reduced with advancing age.

Standing/dynamic

T12–S1

A clear trend of reducing motion with age in both males and females

Standing/dynamic

L1–S

A general trend for decreasing mobility with age.

Standing/dynamic

T12–S

The elderly had a reduced ROM in full flexion and lateral bend but not in axial rotation.

Standing/dynamic

TL junction– PSIS/dynamic

Age appeared to have an influence on motion, and a gradual reduction was seen with each decade.

Standing/static

T12–PSIS

Lumbar mobility had decreased in advancing age.

Standing/dynamic

L–S

Standing/dynamic

L1–S1

An initiation increase in mean mobility from 15 to 24 decade to the 25–34 decade was followed by a progressive decrease with advancing age. Lumbar ROM was seen to be affected by age.

Prone lying/static

T12–S2

Total sagittal ROM, flexion angle, and extension angle declined as age increased.

Standing/dynamic

T12–S2

Normative flexion and lateral flexion range declined across age spectrum. Extension declined the greatest. In axial rotation no age-related decline was observed.

Standing/static

T10, L1–PSIS

Lumbar movement in adults group were more than that of in children

Sitting/dynamic

T12–L5

Advancing age, significant reductions in the ranges of forward and side flexion, but not axial rotation were found

599

(F) Female; (M) Male; (LBP) Low Back Pain; (ROM) Range of motion; (TL) Thoracolumbar; (L) Lumbar; (S) Sacrum; (PSIS) Posterior Superior Iliac Spine. a Results of these studies were eligible and pooled for meta-analysis.

P. Intolo et al. / Manual Therapy 14 (2009) 596–604

Herp et al., 2000, UKa

Age: categories

600

P. Intolo et al. / Manual Therapy 14 (2009) 596–604

Table 2 Quality of studies (n ¼ 16) based on the quality assessment tool for quantitative studies. Study

Burton and Tillotson, 1988 Dvorak et al., 1995 Einkauf et al., 1987 Fitzgerald et al., 1983 Gomez et al., 1991 Herp et al., 2000 Hindle et al., 1990 McGill et al., 1999 McGregor et al., 1995 Milosavljevic et al., 2005 Moll and Wright, 1971 Russell et al., 1993 Sullivan et al., 1994 Troke et al., 2005 Tully et al., 2002 Vachalathiti et al., 1995

Summary of component ratings Selection bias

Allocation bias

Confounders

S W M M W M W W W W W M M M W W

W W W W W W W W W M W W W W W W

M M M W M W W W M M M M M M M M

Blinding

NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA NA

Data collection methods

Withdrawals and drop-outs

S S S S S S S S S S S S S S S S

S W W W S W W W W S W W W W W W

Statistical analysis Sample size calculation

Significant difference

Statistic methods appropriate

Y Y Y Y Y Y Y N Y Y Y Y Y Y Y Y

Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y

Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y Y

Integrity intervention

NR NR NR NR NR NR NR NR NR NR NR NR NR NR NR NR

Key: Selection bias –Does the sample represent the target population. Allocation bias –The extent that assessments of exposure and outcome are likely to be independent. Confounders –Is a risk factor associated statistically associated with exposure to the putative cause. Blinding – The purpose of blinding the assessor (who might also be the care providers) is to protect against detection bias. Data collection methods – Reliability and validity can be reported in the study or in a separate study. For example, some standard assessment tolls have known reliability and validity. Withdrawals and drop-outs – It indicates the percentage of participants completing the study. Statistical Analysis – Appropriate statistic significant needs to be determined between groups. Intervention integrity – What percentage of participants received the allocated intervention or exposure of interest? (S) Strong; (M) Moderate; (W) Weak; (NA) Not Applicable; (Y) Yes; (N) No; (NR) Not relevant.

20–29 and the 60–69 year age groups. No differences were observed between the 20–29 and 50–59 year age groups. In comparison to the 30–39 year age group there are significant mean reductions of 5.9 in the 40–49; 6.2 in the 50–59; and 11.7 for the 60–69 year age groups (Fig. 2, Table 3). Compared to the 40–49 year age group flexion did not significantly reduce for the 50–59 age group however there was a comparative reduction of 5.9 for the 60–69

year age group. There was also a significant 5.6 reduction when comparing flexion between the 50–59 and 60–69 year age groups. Extension ROM significantly reduced each decade (Fig. 2, Table 3) for those subjects aged beyond 40 years. There was a mean extension reduction of 7.7 between the 20–29 and 40–49 year age groups; a mean reduction of 10.5 when comparing the 20–29 to 50–59 year age groups, and a 13.9 mean extension reduction when comparing

Fig. 2. The influence of age category on sagittal ROM in females and males. Symbol (A) represents mean pooled effect of age on ROM in degrees; whiskers represent 95% CIs.

P. Intolo et al. / Manual Therapy 14 (2009) 596–604

601

Table 3 Mean and 95%CI difference (degrees) and p-value between two age categories. Age category

Flexion

Left lateral flexion

Female

Male

Female

Left rotation Male

Female

Male

Group1

Group2

X  95%CI

p-Value

X  95%CI

p-Value

X  95%CI

p-Value

X  95%CI

p-Value

X  95%CI

p-Value

X  95%CI

p-Value

20–29

30–39 40–49 50–59 60–69

2.4  3.2 3.5  3.2 2.8  6.3 9.2  3.6

0.13 0.03a 0.39 0.0001a

2.1  10.7 4.0  8.6 7.1  5.4 16.3  4.4

0.7 0.37 0.01a 0.001a

1.8  1.7 4.2  1.7 5.4  2.0 7.4  2.3

0.04a 0.00001a 0.001a 0.0001a

1.7  1.4 5.6  7.1 6.7  7.6 10.8  7.0

0.04a 0.00001a 0.001a 0.0001a

0.7  1.3 0.3  2.2 1.4  1.4 1.8  3.6

0.26 0.78 0.04a 0.31

2.17  1.6 2.0  1.6 1.7  1.6 2.4  1.9

0.01a 0.015a 0.04a 0.01a

30–39

40–49 50–59 60–69

5.9  3.3 6.2  3.4 11.7  2.8

0.0005a 0.0004a 0.00001a

3.1  2.5 5.1  6.0 10.5  5.0

0.02a 0.01a 0.001a

2.4  1.9 2.4  1.9 5.6  1.9

0.01a 0.01a 0.0001a

4.0  6.8 5.2  7.0 9.3  6.3

0.01a 0.01a 0.001a

0.1  2.7 0.7  1.3 1.8  1.6

0.94 0.26 0.5

0.1  1.1 0.4  1.7 0.2  1.4

0.91 0.63 0.74

40–49

50–59 60–69

0.3  5.1 5.9  3.3

0.9 0.004a

3.0  4.7 1.9  5.5

0.21 0.5

0.3  2.1 3.3  2.1

0.82 0.002a

1.4  1.8 5.0  2.0

0.82 0.002a

1.8  1.7 0.8  1.7

0.03 0.33

0.4  1.6 0.2  1.6

0.65 0.76

50–59

60–69

5.6  3.3

0.00001a

7.0  5.1

0.007a

3.6  2.3

0.0018a

3.6  2.2

0.0018a

1.1  1.4

0.11

0.6  1.7

0.47

Age category

Extension

Right lateral flexion

Female

Male

Female

Right rotation Male

Female

Group2

X  95%CI

p-Value

X  95%CI

p-Value

X  95%CI

p-Value

X  95%CI

p-Value

20–29

30–39 40–49 50–59 60–69

2.9  3.9 7.7  3.5 10.5  2.7 13.9  4.0

0.15 0.00001a 0.00001a 0.00001a

7.8  1.7 5.4  1.9 8.5  2.8 8.5  7.6

0.03 0.001 0.001 0.03

2.8  1.8 4.4  1.8 4.8  1.9 7.9  2.3

0.002a 0.0001a 0.001a 0.0001a

1.2  1.2 5.3  4.2 5.7  6.0 9.4  10.4

0.05a 0.01a 0.06 0.08

0.1  1.5 1.9  4.4 1.9  4.1 2.8  6.9

0.96 0.41 0.36 0.42

2.7  3.6 1.8  2.3 1.5  1.6 0.6  3.0

0.15 0.12 0.06 0.68

30–39

40–49 50–59 60–69

4.9  2.7 7.9  3.8 10.8  5.4

0.00003a 0.00001a 0.00001a

3.7  1.7 6.6  3.3 6.5  7.1

0.001 0.001 0.07

1.8  1.9 2.1  2.1 5.3  2.0

0.07 0.05a 0.0001a

3.6  3.4 4.1  5.1 7.8  9.3

0.04a 0.16 0.1

0.2  1.7 0.1  2.2 1.3  5.2

0.78 0.99 0.63

0.5  2.5 0.8  2.8 1.7  3.1

0.69 0.56 0.28

40–49

50–59 60–69

3.0  3.1 6.0  4.6

0.06 0.01a

2.6  2.1 3.6  6.8

0.01 0.3

0.3  2.0 3.6  1.9

0.77 0.0002a

0.2  1.6 3.8  5.1

0.8 0.15

0.1  1.7 0.4  2.6

0.94 0.76

1.2  2.7 1.0  2.0

0.78 0.34

50–59

60–69

3.7  1.8

0.01a

1.6  6.7

0.6

3.4  3.0

0.03a

3.5  4.3

0.11

0.5  2.2

0.63

1.0  2.3

0.4

a

X  95%CI

Male

Group1

p-Value

X  95%CI

p-Value

Significant difference at level 0.05.

the 20–29 and 60–69 year age groups. There were significant reductions in mean extension of 4.9 , 7.9 and 10.8 when comparing the 30–39 to the 40–49, 50–59 and 60–69 age groups, respectively. For the 40–49 age group there was a non-significant 3.0 mean reduction compared to the 50–59 and a significant 6.0 mean reduction compared to the 60–69 year age group. Extension also significantly reduced by 3.7 from 50–59 to 60–69 year age groups. 4.1.2. Coronal plane Data could be pooled for four lateral flexion (n ¼ 93) studies (Einkauf et al., 1987; McGregor et al., 1995; Herp et al., 2000; Troke et al., 2005). Left lateral flexion was found to reduce (Fig. 3, Table 3) by a mean difference of 4.2 when comparing the 20–29 to the 40–49 year age groups; and by 4.5 mean when comparing the 20–29 to the 50–59 year age groups. There were also significant reductions in mean left lateral flexion of 2.4 , 2.4 and 5.6 when comparing the 30–39 to the 40–49, 50–59 and 60–69 year age groups. Although there were no significant comparative differences between the 40–49 and the 50–59 age groups, significant reductions of 3.3 and 3.6 were observed when comparing the 40–49 to the 60–69 as well as the 50–59 to the 60–69 year age groups. There were significant mean reductions in right lateral flexion (Fig. 3, Table 3) of 2.8 between the 20–29 and 30–39 year age groups; 4.4 when comparing the 20–29 to 40–49 year age groups; 4.8 reductions when comparing the 20–29 and 50–59 year age groups, and 7.9 when comparing the 20–29 and 60–69 year age groups. There were significant reductions of 2.1 and 5.3 when comparing the 30–39 to the 50–59 and 60–69 year age groups, respectively. Although there were significant reductions of 3.6 and

3.4 (respectively) when comparing the 40–49 to the 60–69 and the 50–59 to the 60–69 years age groups the difference between the 40–49 and the 50–59 year age groups was not significant. 4.1.3. Transverse plane Data were pooled (n ¼ 72) for three studies (McGregor et al., 1995; Herp et al., 2000; Troke et al., 2005). Although there was a small yet statistically significant difference of 1.4 when comparing rotation between the 20–29 and the 50–59 years age groups (Fig. 4, Table 3), there were no further statistically significant differences in left and right rotations between 20 and 70 years age bands. 4.2. Males 4.2.1. Sagittal plane Data were pooled (n ¼ 133) from five flexion (Russell et al., 1993; McGregor et al., 1995; Herp et al., 2000; Milosavljevic et al., 2005; Troke et al., 2005) and six extension (n ¼ 164) studies (Fitzgerald et al., 1983; Hindle et al., 1990; Russell et al., 1993; Herp et al., 2000; Milosavljevic et al., 2005; Troke et al., 2005). There were statistically significant reductions in flexion with mean differences of 7.0 and 16.3 when comparing the 20–29 to the 50–59 and 60–69 year age groups (Fig. 2, Table 3). In comparison to the 30–39 year age group there are significant mean reductions of 3.1 in the 40–49; 5.1 in the 50–59; and 10.5 for the 60–69 year age groups. There was also a statistically significant difference of 7.0 when comparing flexion between the 50–59 and the 60–69 years age groups. There were significant mean extension reductions of 5.4 , 8.5 , and 8.5 between the 20–29 and the 40–49, 50–59 and 60–69 year

602

P. Intolo et al. / Manual Therapy 14 (2009) 596–604

Fig. 3. The influence of age category on coronal ROM in females and males. Symbol (A) represents mean pooled effect of age on ROM in degrees; whiskers represent 95% CIs.

age groups, respectively (Fig. 2, Table 3). ROM significantly reduced by a mean 3.7 and 6.6 between the 30–39 and the 40–49 year, and the 30–39 and 50–59 age groups respectively. There was also a significant reduction of 2.6 when comparing the 40–49 and 50–59 year age group. There was no significant reduction in extension when comparing the 60–69 age group to the 30–39, 40–49 and 50–59 age groups.

4.2.2. Coronal plane Data pooling from four (n ¼ 90) studies (Fitzgerald et al., 1983; McGregor et al., 1995; Herp et al., 2000; Troke et al., 2005) showed statistically significant 1.7 and 10.8 reductions in left lateral flexion when comparing the 20–29 to the 30–39 and 60–69 year age groups, respectively (Fig. 3, Table 3). There were also significant reductions of 4.0 , 5.2 and 9.3 comparing the 30–39 to 40–49,

Fig. 4. The influence of age category on horizontal ROM in females and males. Symbol (A) represents mean pooled effect of age on ROM in degrees; whiskers represent 95% CIs.

P. Intolo et al. / Manual Therapy 14 (2009) 596–604

50–59 and 60–69 year age groups, respectively. Further significant reductions of 5.0 and 3.6 (respectively) were observed when comparing the 40–49 to the 60–69 year age groups and the 50–59 to the 60–69 year age groups. Right lateral flexion significantly reduced by a mean 1.2 and  5.3 between the 20–29 and 30–39 and the 40–49 year age groups, respectively (Fig. 3, Table 3). While there was a significant mean reduction of 3.6 when comparing the 30–39 to 40–49 year age group there were no differences noted for respective between group comparisons for the 40–49, 50–59 and 60–69 year age groups. 4.2.3. Transverse plane Three studies were eligible (n ¼ 59) for data pooling (McGregor et al., 1995; Herp et al., 2000; Troke et al., 2001) showing small but significant reductions in mean left rotation of 2.1, 2.0 , 1.7 and 2.4 when comparing the 20–29 to the 30–39, 40–49 50–59 and 60–69 year age groups (Fig. 4, Table 3). However there were no statistically significant differences in right rotation from 20 years of age to 70 years old. In summary lumbar ROM appears to reduce most noticeably after 40 years of age for the sagittal and coronal planes of movement in both sexes with only a minimal effect for age on transverse plane movement. 5. Discussion 5.1. Effect of age on lumbar ROM While significant age-related reductions in lumbar flexion, extension, and lateral flexion were generally observed for both females and males the reductions in rotation were minor (Table 3). For females extension reduced by a mean 13.9 from 20 to 70 years whereas flexion reduced by a mean 9.0 . Comparatively for males extension reduced by a mean 8.0 in the same age span whereas flexion reduced by a mean 16.3 . Flexion reduction was more pronounced after 40 and 50 years for females and males, respectively, while extension reduced in each decade after 40 and 30 years of age, respectively. All studies showed a greater reduction in flexion for males to some extent. The reasons for such sex differences are unclear and might be due to a variety of factors that include occupational demands, previous pregnancies and sex differences in traditional daily functional activities (Hagstromer et al., 2007). It will take future research to verify and elucidate the reasons for this finding. Similarly the loss of extension ROM appears to be associated with advancing age and was more obvious in females. As many daily living and work-related activities involve flexed postures it is likely that this helps to maintain ROM compared to extension and perhaps this effect is more pronounced in females for reasons that are yet unknown. For females, lateral flexion reduced in an incremental manner by about 2.0 for each decade beyond 30 years of age. For males the pattern of reduction was less clear, with left and right lateral flexion reducing by less than 2.0 from 20 to 30 years of age and then an asymmetric reduction where left lateral flexion reduced by about 11.0 by 60 years of age, whereas the reduction in right lateral flexion was approximately 5.0 at 40 years with no significant reduction beyond this (Table 3 and Fig. 4). The reason for this occurring more predominantly in males is unknown. Investigations for factors such as hand dominance, structural asymmetry and/or lifestyle activities in sport and occupation will be required. The approximate 5.0 and 3.0 reduction in left rotation (less for right rotation) between 20 and 70 years of age for both females and males, respectively, is a 15 and 11% loss of range respectively over

603

a 50 year age span and it is thus apparent that rotation is not strongly influenced by age – at least when quantifying this movement with a non-invasive measure. 5.2. Limitations A potential weakness of this review and of most systematic reviews is the risk of an incomplete literature search. Although an extensive literature search was conducted it is possible that some relevant published studies were not identified due to either alternative key words or a poorly worded abstract. Although both sexes and similar age categories were included in the meta-analysis the studies used a variety of definitions for an absence of a history of LBP prior to testing including no LBP within the past 3 months; 6 months; the past year; and during participants lifetime. Such variation in symptom-related inclusion/exclusion criteria could lead to measurable differences in ROM. There was also considerable variation in the tools used to measure angular ROM in the pooled manuscripts, including use of the 3 Space Isotrak (Russell et al., 1993; Herp et al., 2000; Troke et al., 2005), CA-6000 Spinal Motion Analyzer (McGregor et al., 1995), Geometric CAD analysis (Milosavljevic et al., 2005), and goniometry (Fitzgerald et al., 1983; Einkauf et al., 1987). Good to excellent levels of either inter-rater and/or intra-observer reliability were reported by all studies while an acceptable (low) system error was only described by Russell et al. (1993) and Herp et al. (2000) for the 3 Space Isotrak – and was based on the work of Pearcy and Hindle (1989). ROM was either measured in static end range positions or alternatively during continual dynamic movement. The use of either static or dynamic tests will likely have varying relationships to limitations of functional movement, and further studies are required to truly test the sensitivity effects of static versus dynamic comparative movement measures. It is also possible that, given the small number of pooled manuscripts, mean values from each study may have a strong influence on the outcome of the meta-analysis, particularly those that are at the lower and higher ends of pooled angular data (e.g. Fitzgerald et al., 1983 and Milosavljevic et al., 2005 respectively). However when the meta-analysis was repeated without the data from these two papers there was very little change ( 0.05).

4. Discussion This study investigated the influence of degenerative hip joint pathology on size of the deep abductor muscles, GMED, GMIN and PIRI.

Table 3 Muscle volumes (cm3) for gluteus medius, gluteus minimus, and piriformis muscles, and percentage difference between sides. Group

Side

Mild (n ¼ 6)

Affected Unaffected % Difference Affected Unaffected % Difference Left Right % Difference

Advanced (n ¼ 6) Control (n ¼ 12)

GMED

GMIN

PIRI

Mean (SD)

Mean (SD)

Mean (SD)

369 (63) 367 (62) 0.4% 317 (94) 361 (71) 12%** 317 (75) 305 (88) 3.7%

87 (23) 95 (32) 7.9% 84 (34) 91 (33) 8.2% 86 (21) 79 (21) 8.3%

28 (10) 29 (14) 2.6% 28 (8) 33 (8) 14.4%* 28 (8) 28 (8) 0.4%

Gluteus medius muscle (GMED); Gluteus minimus muscle (GMIN); Piriformis muscle (PIRI); Standard deviation (SD); * p < 0.05, **p < 0.01.

608

A. Grimaldi et al. / Manual Therapy 14 (2009) 605–610

these muscles on the unaffected side as this side becomes favoured for weight-bearing function. Despite a lack of statistically significant asymmetry in the deepest abductor muscle, GMIN, there was a trend towards asymmetry in the advanced group (mean 8.3% smaller on affected side, p ¼ 0.1). The importance of this trend is further highlighted when the removal of a single subject results in an asymmetry reflecting an average 21.5% smaller GMIN muscle volume on the affected side. The reason for the lack of atrophy around the affected hip in the remaining subject is unclear. This subject did remain very active with an AMI just below the average for normal control subjects, which may provide some explanation for this variation. Without this subject there is a clear pattern of asymmetry, smaller on the affected side, in the majority of the advanced pathology group. Atrophy in this deepest hip abductor muscle would be consistent with atrophy evident in other local muscles involved in joint protection, such as the multifidus muscle in the lumbar spine (Hides et al., 1994), although some concurrent hypertrophy on the unaffected side cannot be excluded. The other consideration in the interpretation of results for the GMIN muscle is the trend towards GMIN asymmetry, larger on the left side, in control subjects (p ¼ 0.076). This asymmetry may be related to leg dominance as all subjects were left stance dominant. The GMIN muscle may be particularly important in weight-bearing function to assist in joint protection and stabilisation of the femoral head in the acetabulum (Beck et al., 2000; Walters et al., 2001). The relevance of this trend towards asymmetry in control group subjects is that for subjects with left sided hip joint pathology, the loss of muscle size may be underestimated. The only other study to date to investigate symmetry of hip abductor muscle size in subjects with OA of the hip showed a 6% smaller CSA of the ‘gluteal muscles’ around the most affected hip in those with unilateral or bilateral OA (Arokoski et al., 2002). Although the general picture is consistent with our findings the combined measure of all hip abductor muscles is difficult to directly compare to that of the present study. 4.2. Differences in muscle volumes between groups

Fig. 1. The gluteus medius muscle ( in web version), gluteus minimus muscle ( in web version), and piriformis muscle ( in web version) in axial images above the hip joint in control group subject (A), and subjects with mild left osteoarthritis (B), and advanced left osteoarthritis (C). White dot indicates left ilium.

4.1. Side to side differences in muscle volumes within groups Although subjects with mild degenerative hip joint pathology were not significantly asymmetrical, those with advanced pathology demonstrated significant asymmetry for the GMED and PIRI muscles with smaller muscle volumes around the affected hip (mean 12%, p < 0.01 and mean 14.4%, p < 0.05 respectively). This is consistent with the changes in gait pattern at this stage of pathology (Krebs et al., 1998). Peak acetabular pressures have been shown to coincide with peak GMED activity rather than peak ground reaction forces (Krebs et al., 1998). The associated increases in lateral trunk flexion over the weight-bearing leg during stance phase of gait was proposed to be a strategy to reduce abductor muscle activity, thereby reducing compressive forces across painful degenerated joint surfaces. This functional disuse would be in line with the muscle atrophy illustrated in the current study. Part of the asymmetry revealed may also be accounted for by hypertrophy of

Differences in muscle volumes between groups were not significant for PIRI and GMIN muscles, consistent with the lack of between group difference (OA and control) reported by Arokoski et al. (2002). A significant difference between control and mild pathology groups for the GMED muscle however, provides some important information for understanding changes occurring in this muscle, and inconsistencies in previous EMG research. For subjects with mild joint pathology, GMED muscle volume of the affected side was on average 16% larger than those of normal control subjects (p < 0.05). This information may indicate that the GMED muscle could be more predisposed to hypertrophy rather than atrophy in the early stages of joint pathology. This could help explain why subjects with early OA of the hip exhibit higher levels of EMG for this muscle (Sims et al., 2002), while patients just prior to arthroplasty exhibit reduced GMED EMG activity (Long et al., 1993). Differing gait patterns may provide some further explanation for the apparent disparity in GMED response across stages of joint pathology. As GMED muscle atrophy appears inherently linked to offloading strategies used in gait during late stage joint pathology (Krebs et al., 1998), GMED muscle hypertrophy may occur in early joint pathology associated with increases in relative hip adduction (Watelain et al., 2001). Kumagai et al. (1997) determined that the GMED muscle provides maximal contribution to abduction force from a position of 20 hip adduction and more specifically, the most superficial, ‘middle’ portion of the GMED muscle is more active in a position of hip adduction than the deeper anterior and posterior

A. Grimaldi et al. / Manual Therapy 14 (2009) 605–610

609

Furthermore in the early stages of pathology motor control changes are likely to preempt changes in muscle size. Future research aimed at quantifying not only size, but ideally concurrent dynamic EMG activity of each member of the abductor synergy, including the functionally separate portions within the GMED muscle, may be able to elucidate the specific functions and exercise requirements for muscles of the abductor synergy. 5. Conclusion

Fig. 2. The three separate portions of the gluteus medius muscle. Anterior (A), Middle (M), Posterior (P).

portions (Fig. 2), and the GMIN muscle, which are favoured in a more neutral hip position. Increasing pelvic tilt or lateral shift to a position of increased adduction may be an inherent compensatory strategy to increase the contribution from the more superficial abductors to lateral pelvic support. This alignment not only creates preferential recruitment in the superficial portion of the GMED muscle, but also pretensions the iliotibial band potentially increasing the effect of the TFL and UGM muscles. As the GMED muscle is composed of 3 fascially distinct portions, anterior and posterior portions sitting deep to the middle portion (Jaegers et al., 1992) (Fig. 2), all with independent nerve supply (Gottschalk et al., 1989), it is possible that while the overall volume of the GMED muscle increased, the deeper anterior and posterior portions may be responding differently to their superficial counterpart. 4.3. Possible clinical implications Information from this and our previous study (Grimaldi et al., in press) together demonstrate that the abductor synergy does not respond homogenously to joint pathology. While the deeper abductor muscles GMED, PIRI and GMIN demonstrate atrophy in subjects with advanced OA, superficial abductor muscles UGM and TFL appear less affected by underlying pathology. Another finding of important clinical significance is that the GMED muscle may hypertrophy in patients with mild joint pathology. In light of the fact that peak acetabular pressures during gait are associated with peaks in GMED muscle activity (Krebs et al., 1998), non specific exercise programmes focusing on generalised abductor strengthening may need to be reassessed. Programmes assessing and retraining specific portions of the abductor synergy, with particular attention to pelvic-femur alignment, may be most effective in both rehabilitation and prevention strategies. Real time ultrasound has been used successfully for assessment and specific rehabilitation of deep trunk musculature (Stokes et al., 1997; Painter et al., 2007). This tool also holds great potential for use in assessment and retraining of deeper members of the hip abductor synergy. 4.4. Limitations and future directions This study provides information from only a small subject population. This may have impacted on our ability to demonstrate significant differences in muscle size in subjects with mild pathology. The other factor that may have resulted in underestimation of muscle loss is the technique of measuring around the circumference of a muscle. This technique does not account for replacement of viable muscle tissue with intramuscular fatty or connective tissue. As fatty atrophy has been shown to be unevenly distributed within the GMED and GMIN muscles (Pfirrmann et al., 2005) however, the use of a volume measurement should provide the most valid estimation of muscle size in comparison to a single CSA.

This study has shown that the deeper members of the hip abductor synergy, the GMED, GMIN, and PIRI muscles are smaller around the affected hip in subjects with advanced unilateral hip joint pathology. This atrophy was not measurable in subjects with mild pathology, however differing processes are likely in place associated with differing functional weight-bearing patterns. In subjects with mild pathology GMED muscle size was significantly larger on the affected side than control group subjects suggesting the GMED muscle may hypertrophy at this stage of pathology. Assessment and rehabilitation strategies should carefully consider stage of pathology and specific changes occurring within the abductor synergy. This more specific approach may improve long term outcomes of conservative intervention in the management of OA of the hip, and may provide a direction for future prevention programmes. References Alkner BA, Tesch PA. Knee extensor and plantar flexor muscle size and function following 90 days of bed rest with or without resistance exercise. European Journal of Applied Physiology 2004;93:294–305. Angielczyk A, Bronarski J. Electromyographic analysis of the gluteus medius muscle in osteoarthritis of the hip. Chirurgia Narzadow Ruchu I Ortopedica Polska 1982;47:201–4. Arokoski MH, Arokoski JPA, Haara M, Kankaanpaa M, Vesterinen M, Niemitukia LH, et al. Hip muscle strength and muscle cross sectional area in men with and without hip osteoarthritis. Journal of Rheumatology 2002;29:2185–95. Beck M, Sledge J, Gautier E, Dora C, Ganz R. The anatomy and function of the gluteus minimus muscle. Journal of Bone and Joint Surgery British 2000;82B(2): 358–63. Byrd JWT, Jones KS. Prospective analysis of hip arthroscopy with 2-year follow up. Arthroscopy 2000;16(6):578–87. Fukunaga T, Roy RR, Shellock FG, Day MK, Lee PL, Kwong-Fu H, et al. Physiological cross-sectional area of human leg muscles based on magnetic resonance imaging. Journal of Orthopedic Research 1992;10(6):926–34. Grimaldi AM, Richardson CA, Hides JA, Donnelly W, Durbridge G. The association between degenerative hip joint pathology and size of the gluteus maximus and tensor fascia lata muscles. Manual Therapy, in press. Gottschalk F, Kourosh S, Leveau B. The functional anatomy of tensor fascia latae and gluteus medius and minimus. Journal of Anatomy 1989;166:179–89. Herneth A, Philip M, Pretterklieber M, Balassy C, Winkelbauer F, Beaulieu C. Asymmetric closure of ischiopubic synchondrosis in pediatric patients: correlation with foot dominance. American Journal of Radiology 2004;182(2):361–5. Hides JA, Richardson CA, Jull GA. Multifidus muscle recovery is not automatic after resolution of acute, first-episode low back pain. Spine 1996;21(23):2763–9. Hides J, Stokes M, Saide M, Jull G, Cooper D. Evidence of lumbar multifidus muscle wasting ipsilateral to symptoms in patients with acute/subacute low back pain. Spine 1994;19:165–72. Hirsch R, Fernandes RJ, Pillemer SR, Hochberg MC, Lane NE, Altman RD, et al. Hip osteoarthritis prevalence estimates by three radiographic scoring systems. Arthritis & Rheumatism 1998;41(2):361–8. Jaegers S, Dantuma R, deJongh H. Three dimensional reconstruction of the hip on the basis of magnetic resonance images. Surgical Radiologic Anatomy 1992;14:241–9. Jandric S. Muscle parameters in coxarthrosis. Medicinski Pregled 1997;50 (7–8):301–4. Kellgren J, Lawrence J. Radiological assessment of osteoarthritis. Annals of the Rheumatic Diseases 1957;16:494–502. Kumagai M, Shiba N, Higuchi F, Nishimura H, Inoue A. Functional evaluation of hip abductor muscles with use of magnetic resonance imaging. Journal of Orthopaedic Research 1997;15:888–93. Krebs DE, Robbins CE, Lavine L, Mann RW. Hip biomechanics during gait. Journal of Orthopedic and Sports Physical Therapy 1998;28(1):51–9. Long W, Dorr L, Healy B, Perry J. Functional recovery of noncemented total hip arthroplasty. Clinical Orthopaedics and Related Research 1993;288:73–7.

610

A. Grimaldi et al. / Manual Therapy 14 (2009) 605–610

March LM, Bagga H. Epidemiology of osteoarthritis in Australia. Medical Journal of Australia 2004;180(Supplement):S6–17. Murray MP, Sepic SB. Maximum isometric torque of hip abductor and adductor muscle. Physical Therapy 1968;48:1327–35. Painter E, Ogle M, Tehyen D. Lumbopelvic dysfunction and stress urinary incontinence: a case report applying rehabilitative ultrasound imaging. Journal of Sport and Physical Therapy 2007;37(8):499–504. Pfirrmann CWA, Notzli HP, Dora C, Hodler J, Zanetti. Abductor tendons and muscle assessed at MR imaging after total hip arthroplasty in asymptomatic and symptomatic patients. Radiology 2005;235:969–76. Sims K, Richardson CA, Brauer SG. Investigation of hip abductor activation in subjects with clinical unilateral osteoarthritis. Annals of the Rheumatic Diseases 2002;61:687–92. Stokes M, Hides J, Nassiri D. Musculoskeletal ultrasound imaging: diagnostic and treatment aid in rehabilitation. Physical Therapy Reviews 1997;2(2): 73–92.

Taylor HL, Jacobs DR, Schucker B, Knudsen J, Leon AS, Debacker G. A questionnaire for the assessment of leisure time activities. Journal of Chronic Diseases 1978;31:741–55. Teshima K. Hip abduction force in osteoarthritis of the hip. Acta Medica Nagasakiensia 1994;39(3):21–30. Watelain E, Dujardin F, Babier F, Dubois D, Allard P. Pelvic and lower limb compensatory actions of subjects in an early stage of hip osteoarthritis. Archives of Physical Medicine and Rehabilitation 2001;82:1705–11. Wallwork TL, Hides JA, Stanton WR. Intrarater and interrater reliability of assessment of lumbar multifidus muscle thickness using rehabilitative ultrasound imaging. Journal of Orthopedic and Sports Physical Therapy 2007;37(10): 608–12. Walters J, Solomons M, Davies J. Gluteus minimus: observations on its insertion. Journal of Anatomy 2001;198:239–42. Williams P, Warwick R, Dyson M, Bannister L. Grays anatomy. 37th ed. Edinburgh: Churchill Livingstone; 1989.

Manual Therapy 14 (2009) 611–617

Contents lists available at ScienceDirect

Manual Therapy journal homepage: www.elsevier.com/math

Original Article

The association between degenerative hip joint pathology and size of the gluteus maximus and tensor fascia lata muscles Alison Grimaldi a, *, Carolyn Richardson a, Gail Durbridge b, William Donnelly c, Ross Darnell a, Julie Hides a, d a

Division of Physiotherapy, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane 4072, Australia Centre for Magnetic Resonance Imaging, Brisbane, Australia Brisbane Orthopaedic Specialist Services, Brisbane, Australia d The UQ/Mater Back Stability Clinic, Mater Health Services, Raymond Terrace, South Brisbane, Queensland 4101, Australia b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 August 2007 Received in revised form 28 October 2008 Accepted 8 November 2008

The aim of this study was to obtain, using Magnetic Resonance Imaging (MRI), muscle volume measurements for the gluteus maximus (upper: UGM and lower: LGM portions) and tensor fascia lata (TFL) muscles in both healthy subjects (n ¼ 12) and those with unilateral osteoarthritis (OA) of the hip (mild: n ¼ 6, and advanced: n ¼ 6). While control group subjects were symmetrical between sides for the muscles measured, subjects with hip joint pathology showed asymmetry in GM muscle volume dependent on stage of pathology. The LGM demonstrated atrophy around the affected hip in subjects with advanced pathology (p < 0.05), however asymmetry of the UGM (p < 0.01) could be attributed largely to hypertrophy on the unaffected side, based on between group comparisons of muscle volume. TFL showed no significant asymmetry, or difference compared to the normal control group. This study highlights the functional separation of UGM and LGM, and the similarities of the UGM and TFL, both superficial abductors appearing to maintain their size around the affected hip. Further research is required to determine the specific changes occurring in the deeper abductor muscles. This information may assist in the development of more targeted and effective exercise programmes in the management of OA of the hip. Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: Hip osteoarthritis Gluteus maximus Tensor fascia lata Magnetic resonance imaging

1. Introduction Therapeutic exercise has been cited as an important approach used in management of osteoarthritis (OA) of the hip (Hochberg et al., 1995; Altman et al., 2000; Smidt et al., 2005; National Collaborating Centre for Chronic Conditions, 2008; Zhang et al., 2008). There is however, a distinct scarcity of literature investigating the effectiveness of therapeutic exercise of the hip. Programmes have often been quite generalised with small to moderate short term effects and poorer long term effects (van Baar et al., 2001; Tak et al., 2005). Outcomes may be improved through the development of more specific programmes based on a greater understanding of muscle function and dysfunction around the hip joint. One of the most consistent findings in subjects with hip dysfunction is an inability to maintain adequate lateral control of the hip and pelvis in single leg stance (Hardcastle and Nade, 1985). Studies assessing hip abductor muscle strength in subjects with OA

* Correspondence to: Alison Grimaldi, PhysioTec Physiotherapy, 23 Weller Road, Tarragindi, Brisbane, Queensland 4121, Australia. Tel./fax: þ61 7 3342 4284. E-mail address: [email protected] (A. Grimaldi). 1356-689X/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2008.11.002

of the hip have found deficits of up to 31% (Murray and Sepic, 1968; Jandric, 1997; Arokoski et al., 2002), while others have found no significant losses in abductor strength (Teshima, 1994; Sims et al., 2002). These apparent inconsistencies may be associated with specific changes occurring within muscles of the abductor synergy, and the association of these changes with stage of pathology. While strength testing provides information on global abductor muscle function, a resultant effect of all synergists, specific changes within the synergy will only become evident by addressing each muscle individually. Muscles of the abductor synergy providing lateral stability of the hip and pelvis could be divided into superficial muscles that provide their effect via insertion into the iliotibial band (ITB), and deeper muscles that act via insertion into the greater trochanter. Muscles of the superficial system include the tensor fascia lata (TFL) muscle and the gluteus maximus (GM) muscle. The deep system would include the gluteus medius (GMED), piriformis (PIRI) and gluteus minimus (GMIN) muscles. This paper will focus on the study of muscles of the superficial system, while the deep muscle system will be addressed in a further publication (Grimaldi et al., unpublished). In clinical rehabilitation settings, the GM muscle has been targeted for strengthening exercises, due to its reported tendency to

612

A. Grimaldi et al. / Manual Therapy 14 (2009) 611–617

weaken and atrophy (Janda, 1983; Sims, 1999; Sahrmann, 2002). In contrast, the TFL muscle has been targeted for lengthening techniques, due to its reported tendency to become excessively active (Janda, 1983; Sims, 1999; Sahrmann, 2002). There has been little attention paid in either research or clinical settings, to the impact of the functional differentiation of the GM muscle on joint mechanics and the prescription of therapeutic exercise. The upper portion of the GM muscle (UGM) arises from the posterior iliac crest, while the lower portion of the GM muscle (LGM) arises from the inferior sacrum and upper lateral coccyx (Williams et al., 1989). Despite a lack of fascial separation in adult humans, studies on morphogenesis of the GM muscle have revealed that it arises from two muscle primordia with a loose connective tissue separation between cranial and caudal portions in the foetus followed by fusion in the prenatal period (Tichy and Grim, 1985). The UGM, acting above the centre of rotation of the hip, has a primary function of hip abduction, and does not have a role in hip extension. While both portions may externally rotate the femur, the lower portion of the GM muscle (LGM), acting below the centre of rotation of the hip, is the primary hip extensor (Stern, 1972; Stern et al., 1980; Lyons et al., 1983; Jaegers et al., 1992) playing an important protective role in absorbing ground reaction forces at heel strike during gait. The role of the hip abductor synergy in joint protection is less clear. While hip abductor strengthening is generally considered as a priority in patients with hip pain, an in vivo study on joint loads during gait revealed that peak joint loads were associated with peaks in hip abductor muscle activity during stance phase rather than solely loads applied from body weight (Krebs et al., 1998). Contrary to common clinical belief, the authors from this study recommended that clinicians aiming to reduce joint load should reduce hip abductor activity. Another important aspect that should be considered in the prescription of therapeutic exercise for patients with OA of the hip is the stage of pathology. While global atrophy of hip muscles may be present in end stage pathology, in the earlier stages of the condition, more specific changes in the muscles of the hip abductor synergy may occur. It has been proposed that these changes can result in alteration of the orientation of the resultant hip joint vector, and ultimately result in joint damage over time (Kummer, 1993; Sims, 1999). Further information pertaining to hip muscle dysfunction at different stages of pathology would be useful as it could be used in the development of more specific and possibly more effective conservative intervention or prevention programmes for those with degenerative hip joint pathology. Imaging studies provide an excellent opportunity to analyse individual muscles of the hip. Only one study has measured muscle size in subjects with OA of the hip. Arokoski et al. (2002) used magnetic resonance imaging (MRI) to measure hip muscle cross sectional area (CSA) in men with and without hip OA. Two axial slices through the pelvis provided a single CSA for LGM and a combined CSA of all hip abductors, including the UGM. This measure unfortunately failed to provide specific information of individual muscles of the abductor synergy. Furthermore, volume measurements rather than single slice CSA measurements, may be more representative of the complex pelvic musculature. One study has reported muscle volume measurements of the hip muscles for

three healthy subjects (Jaegers et al., 1992), but no volume measurements have been reported in subjects with hip OA. The main aim of this study was to investigate size of the muscles of the superficial lateral stability mechanism of the hip, TFL and GM muscles, in subjects with either mild or advanced degenerative pathology of the hip. Subjects with unilateral pathology were selected in order to provide both within and between subject comparisons. The specific aims were to examine i) if there was significant side asymmetry in the superficial muscles across 3 groups (mild degenerative change, advanced degenerative change, matched controls), ii) if there were significant differences in actual muscle size among the pathology and control groups, and iii) if the functionally separate portions of the GM muscle, UGM, and LGM, display similar patterns of change in subjects with hip pathology. This study also examined the association of both stage of pathology, and muscle size, with the factors of age, height, weight, pain, function and activity levels. The hypotheses of the study were that ia) there would be significant asymmetry in size of the UGM, LGM, and TFL in subjects with hip joint pathology, but not in controls, ib) asymmetry would be greater in subjects with advanced pathology, ii) the affected side LGM muscle would be smaller that the comparable side in control subjects, based on clinical expectation (Sims, 1999; Sahrmann, 2002), and iii) changes in the UGM would more closely reflect changes in the TFL muscle based on their close functional relationship. 2. Methods 2.1. Subjects Twenty-four subjects (12 subjects with hip joint pathology and 12 control subjects) were recruited for this study via community advertisement and via contact with medical practitioners. Control subjects were recruited to match each subject with pathology by sex and age. The age of the control subject was required to be within 5 years of the age of the matched subject with hip pathology. There was an equal distribution of males and females in each group. Subject details are listed in Table 1. Subjects with hip joint pathology were included in the study if they had both a medical diagnosis and radiographic evidence of unilateral degenerative hip joint pathology. Radiographic evidence included X-Ray or MRI demonstrating OA or atraumatic, degenerative labral pathology. OA of the hip joint was classified by an experienced radiologist using the Kellgren/Lawrence (K/L) global scoring system (Kellgren and Lawrence, 1957; Hirsch et al., 1998). Six subjects with early joint space narrowing and osteophytes (K/L grades 1–2) were recruited for the ‘Mild Group’ and 6 subjects with moderate to severe joint space narrowing and osteophytes (K/L grades 3–4) were recruited for the ‘Advanced Group’. Seven subjects had left sided pathology and five subjects had right sided pathology. Exclusion criteria for all subjects included any systemic disease affecting the muscular or nervous system, history of congenital or adolescent hip disease, hip trauma or previous surgery, inflammatory joint disease, presence of tumour, any lower limb injuries in the previous 2 years, participation in unilateral sports, use of a walking aid, and factors that would preclude them from MRI

Table 1 Subject characteristics for each group. Group No Sex M:F Age Mean(SD) Weight(kg) Mean(SD) Height(cm) Mean(SD) AMI Mean(SD) Mild Adv Con

6 6 12

3:3 3:3 6:6

46.5(9.5) 57.7 (6.7) 51.8 (9.7)

80.4 (15.1) 78.3 (8.5) 73.5 (13.3)

171.3 (9.7) 172.0 (7.4) 168.2 (10.2)

MHHS(P) Mean(SD) MHHS(F) Mean(SD) MHHS(Total) Mean(SD)

63 667 (23 884) 25 (10.5) 82 890 (75 410) 16.7 (5.2) 123 175 (68 766) –

41.5 (3.0) 36.2 (5.5) –

73.2 *(11.3) 58.1 *(58.7) –

No ¼ Number. BMI ¼ Body Mass Index. AMI ¼ Activity Metabolic Index. MHHS ¼ Modified Harris Hip Score. P ¼ Pain. F ¼ Function. M:F ¼ Male:Female. SD ¼ Standard deviation. Adv ¼ Advanced Pathology. Con ¼ Control. *Significant difference between pathology groups (p < 0.05).

A. Grimaldi et al. / Manual Therapy 14 (2009) 611–617

scanning procedures (eg. pacemaker, metal implants, pregnancy, claustrophobia). Subjects in both groups were also excluded if they had experienced any lower back pain in the previous 2 years or if there had been any significant lifetime history of lower back pain that resulted in a period of immobility, or required further investigation or treatment. Subjects in the control group were excluded if they had any history of hip pain. Information on the study was sent to the subjects prior to admission to the study. Ethical approval was obtained from the institutional review boards and informed consent was obtained from all subjects.

2.2. Procedure 2.2.1. Self-report questionnaires Information on subject activity levels was gathered using a 12 month Leisure Time Physical Activity questionnaire providing an activity metabolic index (AMI) (Taylor et al., 1978; Arokoski et al., 2002). Activities were coded using the intensity code provided (Taylor et al., 1978).The AMI for each activity the subject participated in was calculated with the formula: AMI ¼ Intensity code (mean metabolic units)  average number of times per month  the number of months per year (frequency)  the time the activity was performed per occasion (duration). Total AMI reflects the addition of AMI for all activities (Taylor et al., 1978) and provides a measure of metabolic units used per year. The Modified Harris Hip Score (MHHS) was used to assess pain and function in the subjects with OA of the hip (Byrd and Jones, 2000). The pain section consisted of 44 points, where a score of 44 represents a pain-free state. The function section consisted of 47 points, where a score of 47 points represents full, normal function. The multiplier 1.1 was used to achieve a total score out of a possible 100 (pain-free normal function).

613

2.2.2. Testing of leg dominance Subjects were also tested for leg dominance. Kicking was used as the test function (Herneth et al., 2004). The weight-bearing leg was recorded as ‘‘stance dominant’’ and the kicking leg as the ‘‘skill dominant’’ leg. 2.2.3. MRI assessment Subjects were first screened for contraindications to MRI by a medical practitioner. Subjects were positioned in supine lying with legs extended to a neutral position. Leg rotation was controlled with the use of sand bags. A 1.5 Tesla Siemens Sonata MR system was used. A T2 True Fast Imaging with Steady State Progression (FISP) sequence using 2 series of 28  6 mm contiguous slices from the iliac crest to the most distal extent of the GM muscle was employed (Time to Repetition (TR): 3.78 ms/Echo Time (TE): 1.89 ms/Field of View (FOV): 390 mm). 2.2.4. Measurement procedure An MRI measurement software package (Osiris) was used to measure CSA (cm2) of UGM, LGM and TFL muscles on each image in which the muscle appeared. Muscle volume (cm3) was calculated by multiplying CSA by slice width and then adding the volumes from each slice to determine the total muscle volume (Fukunaga et al., 1992; Alkner and Tesch, 2004) (Fig. 2). The two functionally separate parts of GM were measured (UGM and LGM). The UGM includes that part of the muscle acting above the centre of rotation of the femoral head. These fibres insert almost exclusively into the ITB via a thick laminar tendon (Lieberman et al., 2006). The LGM inserts below the centre of rotation, superficial fibres into the ITB, deep fibres into the gluteal ridge of the femur (Lieberman et al., 2006). This anatomy is depicted in Fig. 1. In this study the largest CSA of the femoral head was used as an anatomical landmark to functionally separate the UGM from the LGM muscle, to approximate the centre of rotation of the femoral head (Stern, 1972). Reliability of the assessor’s measurement technique was tested by retracing all slices of one subject (44 slices) with an interim period of 6 weeks. Intra-tester reliability was tested for each separate measurement on each slice using a two sided bootstrapped interval of intraclass correlation coefficient (ICC2,1). Intrarater reliability was found to be good, with correlation coefficients ranging from 0.87 to 0.99. Standard error of measurement (SEM) was calculated using the formula SEM ¼ pooled SD  (1-ICC)1/2 (Wallwork et al., 2007). Standard deviation of the difference (SDD) was also calculated as the standard deviation of the differences between measurement 1 and 2. SEM for the GM muscle was 0.495 cm2 and the SDD was 3.87 cm2, while for the TFL muscle the SEM was 0.536 cm2 and the SDD was 2.44 cm2. These values represent good measurement stability with low error. 2.3. Statistical analysis

Fig. 1. Diagramatic representation of the portions of the GM muscle. UGM ; ITB .

; LGM

The comparison of muscle volumes among groups and between sides was performed using a mixed linear model describing muscle volume with group as a between-subject factor, and side as a within-subject factor (Dependent variable ¼ muscle volume, Independent variables ¼ sides and groups). Each muscle was analysed separately. Contrasts of means were performed to compare sides within groups. Muscle volumes around the affected and unaffected hips of the subjects with hip joint pathology were compared with muscle volumes of the corresponding sides of their matched control subjects. That is, if the pathological side was left, the left side muscle volume of the matched control subject was used for comparison, and the right compared with the unaffected side value of the pathology group counterpart. Percent differences were calculated using the formula: % Difference ¼ [(larger value  smaller value)/larger value]  100 (Hides et al., 1996).

614

A. Grimaldi et al. / Manual Therapy 14 (2009) 611–617

Fig. 2. Axial MRIs through the pelvis: images A,C & E through ilia showing UGM in the proximal pelvis; Images B, D & F showing LGM and TFL just below the hip joint. A & B: control TFL . subject; C & D: subject with mild left hip OA (right side as viewed in image); E & F: subject with advanced left hip OA. GM

Analyses were also conducted to assess participant characteristics in relation to a) the similarity of the groups and b) the extent of association with muscle size. One way analysis of variance was used to assess group equivalence across each of the dependent measures of age, height, weight, pain, function, and metabolic activity. The association between these patient characteristics and UGM, LGM, or TFL muscle size was assessed using analysis of covariance.

significant. In the group with advanced pathology there were significant between side differences in the GM but not the TFL muscle. The asymmetry was greater in the UGM muscle (mean difference 21%, p < 0.01) than the LGM muscle (mean difference 19.7%, p < 0.05). Means, standard deviations, and percentage difference in muscle volumes are reported for each group in Table 2. Examples of side to side differences are illustrated for each group in Fig. 2.

3. Results 3.2. Differences in muscle volumes between groups 3.1. Side to side differences in muscle volumes within groups There were no significant side to side differences in the control or mild pathology groups. While LGM size was smaller on the affected side in all but one subject in the group with mild joint changes, the asymmetry was not great enough to be statistically

No significant differences in muscle volumes were found between the mild and advanced pathology groups. The UGM muscles were significantly larger on the unaffected side (Mean difference 30.5%) of the subjects in the advanced pathology group when compared with matched controls (p < 0.05, Table 3). No other

A. Grimaldi et al. / Manual Therapy 14 (2009) 611–617 Table 2 Side to side differences in muscle volume (cm3), and percentage differences within groups for UGM, LGM, and TFL muscles. GROUP

SIDE

UGM Mean (SD)

LGM Mean (SD)

TFL Mean (SD)

Mild

Affected Unaffected % Difference Affected Unaffected % Difference Left Right % Difference

405 (70) 421 (60) 3.8% 378 (96) 479 (118) 21.0% 352 (106) 359 (125) 2.0%

508 (118) 539 (120) 5.8% 457 (158) 569 (144) 19.7%* 453 (130) 495 (158) 8.6%

82.5 (20) 73.8 (19) 10.5% 86.2 (38) 89.5 (27) 3.8% 74.3 (24) 80.6 (29) 7.8%

Advanced

Control

615

4. Discussion This study investigated the influence of degenerative hip joint pathology on size of the GM and TFL muscles. 4.1. Side to side differences in muscle volumes within groups

SD ¼ Standard Deviation. UGM ¼ Upper gluteus maximus muscle. LGM ¼ Lower gluteus maximus muscle. TFL ¼ Tensor fascia lata muscle. p < 0.01 * p < 0.05.

comparisons reached statistical significance although LGM volumes were on average 15.2% larger (p ¼ 0.12) on the unaffected side in the group with advanced pathology, compared with controls, statistical analysis did not reveal a significant difference in this relatively small sample size. Means, standard deviations, and percentage difference in muscle volumes around matched hips of the pathology and control groups are reported in Table 3.

3.3. Self-report questionnaires Results of the AMI for all subjects and the MHHS for subjects with OA of the hip are shown in Table 1. Pain and function scores were lower for the group with more advanced radiological changes, reflecting higher pain levels and more functional disability, as measured by the MHHS. These scores considered alone were not significantly different statistically, however when the total score was calculated there was a significant difference between scores in the mild and advanced pathology groups (p < 0.05). There was no statistically significant difference between groups for the AMI.

3.4. Leg dominance All subjects were left stance dominant/right skill dominant.

3.5. Effect of subject characteristics on muscle size Results of the analyses indicated the groups were comparable in terms of age, height, weight, and metabolic activity (all p > 0.05). In addition there was no significant relationship between these patient characteristics, or pain and function, and UGM, LGM or TFL muscle volume (p > 0.05).

The results of this study showed that subjects with demonstrated unilateral hip joint pathology exhibited marked side to side differences in the size of the GM muscle, specific to stage of pathology. While asymmetry in LGM size in subjects with mild joint pathology was not great enough to be statistically significant, in those with advanced joint changes the mean volume of the LGM muscle was on average 19.7% smaller on the affected side (p < 0.05). The only previous study to investigate muscle size in those with OA of the hip/s reported that the mean CSA of the LGM muscle was 9% smaller on the side of the worse hip in those with either unilateral or bilateral OA (Arokoski et al., 2002). The most likely explanations for the smaller percent difference are the inclusion of subjects with bilateral pathology in the latter study which would be expected to reduce the degree of side to side difference demonstrated, and the inclusion of subjects with both mild and advanced joint pathology in the analysis. Some explanation may also be provided by the different measurement techniques. A single CSA measurement may not provide a true reflection of change in total muscle volume. The UGM muscle similarly showed no significant side to side difference in those with mild joint pathology. In the presence of advanced pathology, the UGM was on average 21% smaller on the affected side, representing a significant side to side difference in muscle size (p < 0.01). The TFL muscle was not significantly different between sides in either pathology group, although the mild group was on average 10.5% larger on the affected side. In contrast Arokoski et al. (2002) reported that the CSA of the TFL muscle was 13% smaller on the more affected side in men with OA. This difference is again most likely due to differences in subject selection and/or measurement technique. Another important consideration when interpreting side to side differences in muscle size is that in the absence of longitudinal data, the determination of side to side differences as atrophy or hypertrophy around weight-bearing joints must be approached with caution. Side to side differences could reflect either atrophy or hypertrophy. Decreases in muscle size on the affected side could occur in response to pain (Lund et al., 1991) or reflex inhibition (Stokes and Young, 1984). However, as pain causes an instinctive shift in weight-bearing towards the unaffected side, side to side volume differences may occur due to disuse atrophy around the affected hip and/or overuse hypertrophy of the unaffected side. For this reason, a control group was included for comparison of actual muscle volumes between groups, thereby assisting in the interpretation of side to side differences. 4.2. Differences in muscle volumes between groups

Table 3 Between group differences in muscle volume (cm3) for UGM, LGM, and TFL muscles. SIDE

GROUP

UGM Mean (SD)

LGM Mean (SD)

TFL

Affected

Mild Advanced Controla Mild Advanced Controla

405 378 354 421 479 361

508 457 460 539 569 489

82.5 86.2 74.9 73.8 89.5 75.4

Unaffected

(70) (96) (103) (60) (118)* (119)

(118) (158) (128) (120) (144) (150)

(20) (38) (24) (19) (27) (26)

UGM ¼ Upper gluteus maximus muscle. LGM ¼ Lower gluteus maximus muscle. TFL ¼ Tensor fascia lata muscle. SD ¼ Standard Deviation. Side refers to the named side in the pathology group, and for the control group side is aligned by matched pair dependent on side of pathology; * p < 0.05. a Reference group for significance values.

As with Arokoski et al. (2002) study, the current study was unable to demonstrate any between group difference in LGM size. This may be simply due to the inherent variability within the population and the relatively small sample size. Another consideration is the fact that the measurement of muscle size by tracing around the perimeter of a muscle in the subjects with pathology of the hip joint may underestimate the loss of contractile muscle tissue. Replacement of normal viable muscle tissue with intramuscular fatty or connective tissue has been reported as ‘fatty atrophy’ at the hip in the GMED muscle (Pfirrmann et al., 2005). Differences in tissue quality of the LGM muscle are observable as increased black markings within the muscle on the side of the

616

A. Grimaldi et al. / Manual Therapy 14 (2009) 611–617

affected hip in Fig. 1D and F. This assists in the support of the assumption that side to side differences in the LGM muscle in those with hip pathology are at least in part due to atrophy around the affected hip. It is most likely however that together with atrophy around the affected hip, there may be concurrent hypertrophy of the unaffected side LGM secondary to patterns of antalgic weight shift. The finding that advanced group subjects LGM volumes were 15.2% larger on the unaffected side than matched control subjects (p ¼ 0.12), provides some support for this effect although not reaching statistical significance. Between group differences for the UGM muscle showed that the mean muscle volume of the UGM muscle on the unaffected side in those with advanced pathology was significantly (Mean difference 30.5%) larger than the corresponding muscles in the control group subjects. This finding suggests that the significant asymmetry (Mean difference 21%) observed in subjects with advanced joint pathology may be largely attributable to hypertrophy on the unaffected side. Some degree of atrophy on the affected side however cannot be discounted although fatty atrophy was not commonly observed in the UGM muscle. Around the affected hip neither the UGM muscle, nor the other superficial hip abductor, the TFL muscle, were significantly different in size to a normal population. The other information that was assessed with regard to the subjects of this study was gathered through self-report questionnaires and leg dominance testing. While pain, function and leg dominance had no significant effect on GM or TFL muscle size, the information collected provided 2 important pieces of information. 4.3. Pain, function and radiological change The first of these relate to the association between pain, function, and radiological change. It has been previously noted that there is often no clear relationship between severity of radiological change in an osteoarthritic joint and severity of pain or degree of disability (Hurley, 1999). In studies of subjects with OA of the knee, advanced radiological change may in some people be accompanied by very little pain, while others with only mild degenerative change may experience severe disabling pain (Claessens et al., 1990; McAlindon et al., 1993). Arokoski et al. (2002) in their study of men with OA of the hip were unable to demonstrate a correlation between grade of severity of OA and pain measured on a visual analogue scale. There was however significantly more pain within individuals on the side with the highest radiographic OA score. Similarly the findings of the current study reflect the difficulty in linking a pain score alone to degree of radiographic change. By combining measures of pain and function, the MHHS was able to demonstrate significant differences between subjects with early radiographic change and those with advanced radiographic change. This may suggest that this particular combination of questions may be more sensitive to degree of radiographic change than those available for OA of the knee. 4.4. The influence of leg dominance The second finding of importance relates to the potentially confounding variable of leg dominance. Although there is evidence that dominance has an effect on muscle strength (Balogen and Onigbinde, 1992), particularly in upper limb strength in those involved in unilateral sports (Ducher et al., 2005; Ellenbecker et al., 2006), there is a much weaker link between leg dominance and muscle strength (Hunter et al., 2000; Zakas, 2006), and little evidence to link leg dominance to asymmetry in muscle size. Greater muscle strength of the dominant limb may be associated with improved neuromuscular functioning, rather than muscle size alone. In the current study the exclusion of all subjects involved in unilateral sports sought to avoid the effect of this potentially

confounding variable on muscle symmetry. The results of this study were able to demonstrate that for the normal control subjects tested there was no significant asymmetry in muscle size for the muscles measured. All subjects were left stance dominant which, if this factor were imparting an effect, would favour a larger muscle volume on the left side particularly for the weight-bearing LGM muscle. This was not the case, allowing greater clarity in interpretation of results for the pathology groups. 4.5. Possible clinical implications The balance of muscle activity around a joint may either protect a joint from injury or accelerate destructive joint forces. Both the UGM and LGM muscles are known to be active at heel strike in gait to help absorb ground reaction forces causing lateral pelvic drop and flexion moments at the hip and knee (Stern et al., 1980; Lyons et al., 1983). While reduced activation of the GM muscle may fail to absorb these ground reaction forces, excessive activation in the abductor muscles, may lead to an increase in joint loading (Krebs et al., 1998). So both atrophy of the LGM muscle around the affected hip, and hypertrophy of the UGM muscle around the unaffected hip may have negative effects on their respective underlying joints. Hurley (1999) has suggested that the presence of bilateral muscle dysfunction may help to explain why unilateral OA years later often becomes bilateral OA. The findings of this study imply that the LGM and UGM muscles should be assessed individually, and on both sides, with clinical management directed towards restoring normal symmetrical weight-bearing patterns and muscle bulk. Further, the finding that neither of the superficial hip abductor muscles appear to be affected on the side of pathology, and recommendations to reduce recruitment of the hip abductor muscles in order to reduce peak acetabular pressures during gait (Krebs et al., 1998), the current clinical rationale for generalised hip abductor muscle strengthening could be questioned. While some authors have reported hip abductor muscle strength deficits of up to 31% (Murray and Sepic, 1968; Jandric, 1997; Arokoski et al., 2002), others have reported no significant difference (Teshima, 1994; Sims et al., 2002). These variable findings may be a reflection of the relative degrees of atrophy of individual muscles of the abductor synergy. If both superficial abductor muscles are not significantly affected by pathology, strength changes may possibly reflect weakness in the deeper abductor muscles. Together with the information provided by this study, further information on the response of the deep muscle system to degenerative change of the hip may provide further insight into specific changes within the abductor synergy. Greater specificity in exercise prescription around the hip may allow development of interventions that achieve more significant and longer lasting changes in pain and function scores in patients with OA of the hip. 4.6. Limitations and future directions The main limitation of this study was low subject numbers. Valuable additional information may be gained by subsequent studies with larger subject numbers and the inclusion of a method to measure quality of muscle tissue. Furthermore, this study assessed only two of many hip muscles which may be associated with hip pathology. Further investigation of other muscles, such as the deeper abductor muscles, is required to provide a more complete picture of muscle dysfunction. 5. Conclusion This study has demonstrated that the GM muscle should be considered as 2 functionally separate entities, the UGM a hip abductor and the LGM, a hip extensor, these muscles having

A. Grimaldi et al. / Manual Therapy 14 (2009) 611–617

differing responses to the presence of joint pathology. The UGM muscle like its functional counterpart, the TFL, appears unaffected on the side of joint pathology, while the LGM muscle demonstrates local atrophy. The lack of affect on the superficial hip abductors suggests that muscle weakness demonstrated in subjects with OA of the hip may be related to changes in the deeper hip abductors (GMED, GMIN and PIRI) and require more specific therapeutic exercise intervention. References Alkner BA, Tesch PA. Knee extensor and plantar flexor muscle size and function following 90 days of bed rest with or without resistance exercise. European Journal of Applied Physiology 2004;93:294–305. Altman RD, Hochberg MC, Moskowitz RW, Schnitzer TJ. Recommendations for the medical management of osteoarthritis of the hip and knee:2000 update. Arthritis and Rheumatism 2000;43:1905–15. Arokoski MH, Arokoski JPA, Haara M, Kankaanpaa M, Vesterinen M, Niemitukia LH, et al. Hip muscle strength and muscle cross sectional area in men with and without hip osteoarthritis. The Journal of Rheumatology 2002;29:2185–95. Balogen JA, Onigbinde AT. Hand and leg dominance: do they really affect limb muscle strength? Physiotherapy Theory and Practice 1992;8(2):89–96. Byrd JWT, Jones KS. Prospective analysis of hip arthroscopy with 2-year follow up. Arthroscopy 2000;16(6):578–87. Claessens AA, Schouten JS, van den Ouweland FA, Valkenburg HA. Do clinical findings associate with radiographic osteoarthritis of the knee? Annals of the Rheumatic Diseases 1990;49:771–4. Ducher G, Courteix D, Me´me´ S, Magni C, Viala J, Benhamou C. Bone geometry in response to long-term tennis playing and its relationship with muscle volume: A quantitative magnetic resonance imaging study in tennis players. Bone 2005;37(4):457–66. Ellenbecker TS, Roetert EP, Riewald S. Isokinetic profile of wrist and forearm strength in elite female junior tennis players. British Journal of Sports Medicine 2006;40:411–4. Fukunaga T, Roy RR, Shellock FG, Day MK, Lee PL, Kwong-Fu H, et al. Physiological cross-sectional area of human leg muscles based on magnetic resonance imaging. Journal of Orthopedic Research 1992;10(6):926–34. Grimaldi A, Richardson C, Stanton W, Durbridge G, Donnelly W, Hides J. The association between degenerative hip joint pathology and size of the gluteus medius, gluteus minimus, and piriformis muscles, unpublished. Hardcastle P, Nade S. The significance of the trendelenberg test. The Journal of Bone and Joint Surgery British 1985;67B:741–6. Herneth A, Philip M, Pretterklieber M, Balassy C, Winkelbauer F, Beaulieu C. Asymmetric closure of ischiopubic synchondrosis in pediatric patients: correlation with foot dominance. American Journal of Radiology 2004;182(2):361–5. Hochberg MC, Altman RD, Brandt KD, Clark BM, Dieppe PA, Griffin MR, et al. Guidelines for the medical management of osteoarthritis. Part 1. Osteoarthritis of the hip. Arthritis and Rheumatism 1995;38:1535–40. Hides JA, Richardson CA, Jull GA. Multifidus muscle recovery is not automatic after resolution of acute, first-episode low back pain. Spine 1996;21(23):2763–9. Hirsch R, Fernandes RJ, Pillemer SR, Hochberg MC, Lane NE, Altman RD, et al. Hip osteoarthritis prevalence estimates by three radiographic scoring systems. Arthritis and Rheumatism 1998;41(2):361–8. Hunter SK, Thompson MW, Adams RD. Relationships among age-associated strength changes and physical activity level, limb dominance, and muscle group in women. Journal of Gerentology 2000;55A(6):B246–72. Hurley MV. The role of muscle weakness in the pathogenesis of osteoarthritis. Rheumatic Disease Clinics of North America 1999;25(2):283–98. Jaegers S, Dantuma R, deJongh H. Three dimensional reconstruction of the hip on the basis of magnetic resonance images. Surgical Radiologic Anatomy 1992;14:241–9. Jandric S. Muscle parameters in coxarthrosis. Medicinski Pregled 1997;50(7–8): 301–4. Janda V. Muscle function testing. London, Boston: Butterworths; 1983. Kellgren J, Lawrence J. Radiological assessment of osteoarthritis. Annals of the Rheumatic Diseases 1957;16:494–502.

617

Krebs DE, Robbins CE, Lavine L, Mann RW. Hip biomechanics during gait. Journal of Orthopedic and Sports Physical Therapy 1998;28(1):51–9. Kummer B. Is the Pauwels theory of hip biomechanics still valid? a critical analysis, based on modern methods. Annals of Anatomy 1993;175:203–10. Lieberman D, Raichlen D, Pontzer H, Bramble D, Cutright-Smith E. The human gluteus maximus and its role in running. The Journal of Experimental Biology 2006;209(11):2143–55. Lund JP, Donga R, Widmer CG, Stohler CS. The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Canadian Journal of Physiology and Pharmacology 1991;69(5): 683–94. Lyons K, Perry J, Gronley JK, Barnes L, Antonelli D. Timing and relative intensity of hip extensor and abductor muscle action during level and stair ambulation. Physical Therapy 1983;63(10):1597–605. McAlindon TE, Cooper C, Kirwan JR, Dieppe PA. Determinants of disability in osteoarthritis of the knee. Annals of the Rheumatic Diseases 1993;52: 258–62. Murray MP, Sepic SB. Maximum isometric torque of hip abductor and adductor muscle. Physical Therapy 1968;48:1327–35. National Collaborating Centre for Chronic Conditions. Osteoarthritis: national clinical guideline for care and management in adults. London: Royal College of Physicians; 2008. Pfirrmann CWA, Notzli HP, Dora C, Hodler J, Zanetti. Abductor tendons and muscle assessed at MR imaging after total hip arthroplasty in asymptomatic and symptomatic patients. Radiology 2005;235:969–76. Sahrmann S. Diagnosis and treatment of movement impairment syndromes. St. Louis: Mosby; 2002. Sims K, Richardson CA, Brauer SG. Investigation of hip abductor activation in subjects with clinical unilateral osteoarthritis. Annals of the Rheumatic Diseases 2002;61:687–92. Sims K. The development of hip osteoarthritis: implications for conservative management. Manual Therapy 1999;4:127–35. Smidt N, de Vet HCW, Bouter LM, Dekker J, for the Exercise Therapy Group. Effectiveness of exercise therapy: a best evidence summary of systematic reviews. Australian Journal of Physiotherapy 2005;51:71–83. Stern JT. Anatomical and functional specializations of the human gluteus maximus. American Journal of Physical Anthropology 1972;36:315–40. Stern JT, Pare EB, Schwartz JM. New perspectives on muscle during locomotion. Electromyographic studies of rapid and complex behaviours. Journal of the American Orthopedic Association 1980;80(4):287–91. Stokes M, Young A. The contribution of reflex inhibition to arthrogenous muscle weakness. Clinical Science 1984;67(1):7–14. Tak E, Staats P, van Hespen A, Hopman-Roc M. The effects of an exercise programme for older adults with osteoarthritis of the hip. The Journal of Rheumatology 2005;32:1106–13. Taylor HL, Jacobs DR, Schucker B, Knudsen J, Leon AS, Debacker G. A questionnaire for the assessment of leisure time activities. Journal of Chronic Diseases 1978;31:741–55. Teshima K. Hip abduction force in osteoarthritis of the hip. Acta Medica Nagasakiensia 1994;39(3):21–30. Tichy M, Grim M. Morphogenesis of the human gluteus maximus muscle arising from two muscle primordia. Anatomy and Embrology 1985;173(2): 275–7. van Baar M, Dekker J, Oostendorp R, Bijl D, Voorn T, Bijlsma J. Effectiveness of exercise in patients with osteoarthritis of hip or knee: nine months’ follow up. Annals of the Rheumatic Diseases 2001;60:1123–30. Wallwork TL, Hides JA, Stanton WR. Intrarater and interrater reliability of assessment of lumbar multifidus muscle thickness using rehabilitative ultrasound imaging. Journal of Orthopedic and Sports Physical Therapy 2007;37(10): 608–12. Williams P, Warwick R, Dyson M, Bannister L. Grays anatomy. 37th ed. Edinburgh: Churchill Livingstone; 1989. Zakas A. Bilateral isokinetic peak torque of quadriceps and hamstring muscles in professional soccer players with dominance on one or both two sides. Journal of Sports Medicine and Physical Fitness 2006;46:28–35. Zhang W, Moskowitz RW, Nuki G, Abramson S, Altman RD, Arden N, et al. OARSI recommendations for the management of hip and knee osteoarthritis, Part II: OARSI evidence-based, expert consensus guidelines. Osteoarthritis and Cartilage 2008;16:137–62.

Manual Therapy 14 (2009) 618–622

Contents lists available at ScienceDirect

Manual Therapy journal homepage: www.elsevier.com/math

Original Article

Video based measurement of sagittal range of spinal motion in young and older adultsq Yi-Liang Kuo a, Elizabeth A. Tully b, *, Mary P. Galea b a b

Department of Physical Therapy, Shu Zen College of Medicine and Management, Kaohsiung County 821, Taiwan School of Physiotherapy, Faulty of Medicine, Dentistry and Health Sciences, The University of Melbourne, 200 Berkeley Street, Parkville, Victoria 3010, Australia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 23 May 2008 Received in revised form 20 November 2008 Accepted 3 December 2008

A revised model of skin marker placement with the two-dimensional (2D) PEAK Motus system was used to investigate the effect of aging on sagittal range of spinal motion. Twenty-four healthy young adults and twenty-two healthy older adults were videotaped while performing the movements of flexion and extension in each spinal region d cervical, thoracic and lumbar spine. Alternative movement tests that may allow a greater range of motion (ROM) for thoracic extension and lumbar flexion were also investigated. Older adults demonstrated significantly decreased flexion/extension ranges in the cervical, thoracic and lumbar spine. The movement of cat-stretch in the all-fours position allowed greater thoracic extension, and the movement of toe-touch in standing permitted greater lumbar flexion. This study provides reference data for sagittal ranges of spinal motion in healthy young and older adults as measured by a 2D imaged-based system. The sagittal model of skin marker placement used in this study can have a broader application for ROM measurement in the clinical setting using a digital camera and freely downloadable software. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Spine Measurement Range of motion Aging

1. Introduction Knowledge of the expected range of motion (ROM) in healthy subjects provides the basis for assessment and for establishing appropriate treatment goals in clinical practice. Radiographic methods are considered the ‘gold standard’ for ROM measurement (Portek et al., 1983), however the risk of radiation exposure limits its use. Previous studies agree that increasing age is associated with decreased spinal motion, however the descriptive information provided from simple clinical tools (Loebl, 1967; Moll and Wright, 1971; Kuhlman, 1993) has frequently been jeopardized by measurement issues. For example, the Schober tape measure method (Moll and Wright, 1971) provides an index of lumbar movement (in cm) reported as unreliable (Portek et al., 1983; Miller et al., 1992). Use of a single inclinometer positioned over a specific spinous process (e.g. T12/L1) is gravity referenced, and thus only indicates the orientation of the body segment in space, with the angle being dependent on the position of the more caudal body segments. The dual inclinometer method provides more valid and

q This research was carried out as part of a PhD by Yi-Liang Kuo at The University of Melbourne. * Corresponding author. Tel.: þ61 3 8344 4171; fax: þ61 3 8344 4188. E-mail address: [email protected] (E.A. Tully). 1356-689X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2008.12.006

accurate measurement for lumbar flexion (Loebl, 1967; Saur et al., 1996), however the reliability of measurement for lumbar extension has shown to be low (Merritt et al., 1986; Dillard et al., 1991). In contrast, a motion analysis system that tracks the displacement of reference markers attached to the skin over relevant bony landmarks can provide more reliable and accurate measurement of human movement. However, previous ROM studies have been compromised by problematic models of marker placement. For example, Hu et al. (2006) placed markers over a swimming cap and a sleeveless shirt to measure ROM in the cervical spine. Possible stretch or slide of the cap and clothes as well as skin movement errors likely influenced the validity and reliability of the data. In addition, the cervical spine was measured as a whole without acknowledging the functional differences between the upper and lower cervical regions. Also, in most surface-based studies information regarding ROM has been limited to a single spinal region (Dvorak et al., 1995; McGill et al., 1999; Sforza et al., 2002; Wu et al., 2007), with no attempt to determine the mobility of adjacent regions in this functionally interdependent chain of joints. Another factor influencing the ROM is test movement. The clinical tests for lumbar flexion and extension are often performed in standing, and patients with balance problems may have difficulty achieving full lumbar extension. Similarly patients attempting thoracic extension in sitting tend to lean backwards from the hips so that the full available thoracic movement is not achieved. An

Y.-L. Kuo et al. / Manual Therapy 14 (2009) 618–622

alternative test movement may be provided by the ‘cat-stretch’, a common spinal ROM exercise performed in the all-fours position (Fig. 1). Patients arch their back upward and downward accompanied by coordinated head movement while kneeling on the hands and knees. When patients hollow their back, the end position is achieved by simultaneous extension of the thoracic and lumbar spine. The opposite movement, arching the back toward the ceiling, is comprised of thoracic and lumbar flexion. The movement of catstretch in the all-fours position is stable, allows the normal movement interaction between the spinal regions, may permit a greater range of thoracolumbar motion, and also minimises the trouble of changing test positions. Therefore, the aim of this study was to use our previously developed two-dimensional (2D) model of marker placement (Tully and Stillman, 1997) with the 2D PEAK Motus video analysis system (PEAK Performance Technologies Inc., Englewood, Colorado, USA) to establish reference values for sagittal ROM in all spinal regions, and to investigate the effect of aging on regional mobility. The second aim of this study was to investigate the feasibility of an alternative movement, cat-stretch, for testing ROM in the lumbar and thoracic spine. 2. Material and methods 2.1. Subjects Twenty-four healthy young adults (15 women, 9 men; age: 17– 27 years; weight: 62.6  8.9 kg; height: 170.2  9.1 cm; BMI: 21.5  1.9 kg/m2) and 22 healthy older adults (14 women, 8 men; age: 60–83 years; weight: 69.3  12.1 kg; height: 163.9  8.4 cm;

619

BMI: 25.8  4.0 kg/m2) volunteered for this study. Exclusion criteria were: 1) significant spinal lateral deviation or lower limb deformity; 2) severe pain and/or injury/pathology in spine or lower extremities requiring treatment during the preceding 6 months. This study was approved by the Human Research Ethics Committee of the university. Prior to involvement in this study, subjects were informed of the details of this project and signed a written consent form. 2.2. Experimental protocol Nine spherical reflective markers (B&L Engineering, Tustin, CA, USA) were attached to specific anatomic landmarks of subjects in standing (Fig. 2). For ease of application, one face marker was attached to the centre of the flexible ear hook of a headphone piece (SHS3201/97, Philips, Sydney, NSW, Australia), while the other face marker was attached to the mid point between the right corner of the mouth and the right nasal ala. Details for locating the other skin reference markers have been reported previously (Tully et al., 2002; Kuo et al., 2008). Good test-retest reliability for skin marker placement was established in standing (ICC1, 1 ¼ 0.85–0.92). Subjects were videotaped while performing various ROM tests. They were instructed to move at their own comfortable speed to the maximal available end position and then return to the starting position. Before performing three trials, subjects were given two practice trials to familiarize themselves with the specific movement. The investigator corrected any faulty movement, including out of plane movement, during practice. A brief rest period was given between each trial. Cervical flexion and extension were tested in sitting by looking down toward the chest and up toward the ceiling while maintaining an upright posture. Thoracic and lumbar flexion and extension were tested when subjects performed the cat-stretch in the all-fours position. Thoracic extension was also tested in sitting by instructing subjects to arch their thoracic spine while maintaining their lower back and hips steady. Lumbar flexion was also tested by performing toe touching from upright standing with knees extended. Subjects who could touch their toes stood on a platform, and were instructed to bend downward until their fingers reached the edge of the platform or beyond. 2.3. Data management Fig. 2 illustrates the angle definitions and calculation. Increasing upper and lower cervical spine angles indicate extension, and

Fig. 1. End positions of cat-stretch in the all-fours position.

Fig. 2. Marker placement and angle definition.

620

Y.-L. Kuo et al. / Manual Therapy 14 (2009) 618–622

decreasing thoracic flexion angle indicates extension. Negative lumbar spine angles denote lumbar extension. The videotaped images of the three test movements were automatically digitised using the 2D PEAK software program. The video images were then converted to kinematic data and smoothed using a fourth order Butterworth (high cut-off) filter (Winter, 2005) at an optimum cutoff frequency determined by the software (Jackson, 1979). The average of the three trials was used for statistical analysis. ROM was expressed as the maximal available angle and total flexion/extension range. The maximal available angle was obtained from the end position of the joint/segment during the test movement. The total flexion/extension range was calculated by subtracting the maximal available extension angle from the maximal available flexion angle. Prior to statistical analysis, normal distribution for each numerical variable was examined. Descriptive statistics were summarised for all data accordingly. To determine the group difference in physical characteristics and sagittal spinal ROM, unpaired t-tests (or appropriate non-parametric tests) were used. Two-way repeated measures ANOVA, with group as a betweensubject factor and method as a within-subject factor, were used to determine the statistical significance for measurement of thoracic extension and lumbar flexion. If there was a significant interaction in the repeated measures ANOVA, the simple factor analysis was performed to assess age-related differences at each position and position-related differences within the age group. The statistical significance level was set at P < 0.05. 3. Results The young group was significantly taller (t ¼ 2.44, P ¼ 0.02) and lighter (t ¼ 2.15, P ¼ 0.04) than the older group, and had a lower body mass index (t ¼ 4.50, P < 0.001). 3.1. Upper and lower cervical spine flexion/extension Table 1 summarizes the maximal available flexion and extension angles and flexion/extension range in the cervical spine for both groups. The older group commenced the movements from a more forward head position, i.e. upper cervical extension (old vs. young: 126.6 vs. 114.4 ) and lower cervical flexion (old vs. young: 70.4 vs. 79.6 ). When subjects were instructed to look downward the older group achieved a smaller upper cervical flexion angle (t ¼ 4.80, P < 0.001) and a larger lower cervical flexion angle (t ¼ 2.35, P ¼ 0.02). Although the young group extended more in both regions of the cervical spine when looking upward, the significant difference between groups was only found in the lower cervical spine (t ¼ 6.49, P < 0.001) not in the upper cervical spine (t ¼ 1.06, P ¼ 0.3). Overall, the older group had significantly smaller total

ranges of flexion/extension in the upper (t ¼ 5.36, P < 0.001) and lower (t ¼ 5.65, P < 0.001) cervical spine. 3.2. Thoracic flexion/extension When arching the back toward the ceiling during the movement of cat-stretch, the older group achieved a larger thoracic flexion angle (58.8  9.0 ) than the young group (52.4  11.4 ). The mean difference of 6.4 between age groups was significant (t ¼ 2.09, P ¼ 0.04). The maximal available thoracic extension angle (expressed as the minimal thoracic angle) was influenced by the main effects of group (F1,40 ¼ 19.91, SS ¼ 4196.11, MS ¼ 4196.11, P < 0.001) and method (F1,40 ¼ 21.73, SS ¼ 1016.68, MS ¼ 1016.68, P < 0.001). There was also a significant interaction effect of group and method (F1,40 ¼ 14.30, SS ¼ 668.69, MS ¼ 668.69, P ¼ 0.001). The older group achieved a significantly smaller minimal thoracic angle in the all-fours position than in the sitting position (t ¼ 4.82, P < 0.001, 95% CI 7.1 to 18.1). In other words, the older group was able to extend their thoracic spine further in the allfours position. However, the young group obtained a similar minimal thoracic angle in both positions (t ¼ 0.84, P ¼ 0.4, 95% CI 2.0 to 4.6). In both position, the older group demonstrated a significantly larger minimal thoracic flexion angle than the young group (all-fours position: t ¼ 6.03, P < 0.001, 95% CI 28.2 to 14.0; sitting: z ¼ 2.24, P ¼ 0.03) (Fig. 3), which means that older subjects had decreased maximal available thoracic extension. Overall, the total range of thoracic flexion/extension during catstretch for the older group (33.6  15.6 ) was significantly smaller than that (48.5  12.4 ) for the young group by 14.9 (t ¼ 3.59, P ¼ 0.001, 95% CI 6.5–23.2). 3.3. Lumbar flexion/extension Similar to results for thoracic extension, the maximal available lumbar flexion angle was affected by the main effects of group (F1,43 ¼ 29.70, SS ¼ 2017.58, MS ¼ 2017.58, P < 0.001) and method (F1,43 ¼ 107.31, SS ¼ 5265.25, MS ¼ 5265.25, P < 0.001). There was also a significant interaction effect of group and method (F1,43 ¼ 5.58, SS ¼ 453.05, MS ¼ 453.05, P ¼ 0.02). Both groups achieved a greater maximal available lumbar flexion angle during toe-touch in standing than during cat-stretch in all-fours (older group: t ¼ 7.0, P < 0.001, 95% CI 14.0 to 7.6; young group: t ¼ 7.85, P < 0.001, 95% CI 21.7 to 12.7) (Fig. 4).

Table 1 Sagittal ranges of motion in the cervical spine for the young (n ¼ 24) and older (n ¼ 22) groups. Angles

Young

Old

(Mean  SD)

(Mean  SD)

93.1  7.9 152.4  8.8 60.0  8.0

103.9  6.9 150.0  6.4 46.5  8.7

54.6  4.3 90.9  8.4 36.9  8.2

51.3  4.9 74.7  8.6 23.5  7.4

Mean Difference (95% CI) Upper Cervical Flexion* Extension Total range* Lower Cervical Flexion* Extension* Total range*

10.7 (6.2–15.3) 2.4 (7.0 to 2.2) 13.5 (8.4–18.6) 3.3 (6.0 to 0.5) 16.2 (21.3 to 11.2) 13.3 (8.6–18.1)

Abbreviation: SD ¼ standard deviation, CI ¼ confidence interval. * Denotes a statistical significant difference, P < 0.05.

Fig. 3. Mean and 95% confidence intervals for maximal available thoracic extension angle (expressed as minimal thoracic angle) achieved in the sitting and all-fours positions in the young and older groups.

Y.-L. Kuo et al. / Manual Therapy 14 (2009) 618–622

621

4.2. Thoracic spine

Fig. 4. Mean and 95% confidence interval for maximal available lumbar flexion angle achieved in the all-fours and standing positions in the young and older groups.

The older group also demonstrated decreased maximal available lumbar flexion angle than the young group in both all-fours (t ¼ 2.91, P ¼ 0.006, 95% CI 2.3–12.8) and standing positions (t ¼ 6.62, P < 0.001, 95% CI 9.7–18.2). No significant difference was found in the maximal lumbar extension angle between the young (18.9  13.6 ) and older (11.1  9.2 ) groups during the movement of cat-stretch (t ¼ 1.85, P ¼ 0.07, 95% CI 12.5 to 0.5). Overall, the total range of lumbar flexion/extension during catstretch for the old group (28.9  11.5 ) was significantly smaller than that (42.4  15.8 ) of the young group by 13.5 (t ¼ 3.30, P ¼ 0.002, 95% CI 5.3–21.8).

4. Discussion This study has established reference values for sagittal range of spinal motion in young and older adults using image-based measurement. The comparison of traditional and alternative test positions provides useful information for clinicians who are involved in designing an exercise program for older adults to improve spinal ROM and in measuring the effects of the intervention.

Although older adults achieved a slightly larger (6.2 ) thoracic flexion angle, again possibly associated with their more kyphotic posture (old vs. young: 42.8 vs. 38.3 ) in standing, there was a large difference in the results for thoracic extension (21 ) indicating stiffness in the thoracic spine associated with age. Whether or not this amount of limited thoracic extension is sufficient to interfere with daily tasks that older subjects would usually perform, including those requiring full arm elevation remains to be determined. Results suggest that the movement of cat-stretch is more suitable for testing thoracic extension because it allows greater ROM. Performing thoracic extension in sitting appeared unnatural to most subjects, because they habitually initiated the movement from the lumbar spine, or swayed backwards from the hips. As a result, many appeared to simultaneously restrict movement in the thoracic spine. Persson et al. (2007) observed a similar finding in the movement of head protraction and retraction. When subjects were instructed to restrain their back against the backrest of the chair, their sagittal protraction/retraction excursion of the head significantly reduced. These findings suggest that there exists a close relationship between the adjacent segments in the kinematic chain and between posture and ROM. The advantage of the cat-stretch is that it allows simultaneous movement in the adjacent cervical and lumbar spine, and maximises the physiologic ROM in the thoracic spine. Therefore, both groups, especially young subjects, achieved a smaller thoracic flexion angle (increased extension) when performing the catstretch. Although other positions could have been trialled to measure maximal thoracic flexion, including sitting and standing, the focus of this study was on the more clinically relevant movement of thoracic extension. A limitation of testing thoracic extension in the all-fours position was that the cat-stretch was a novel task. However, subjects became familiarised with the movement sequence after a few practice trials. In addition, although stable, older adults who have limited wrist extension or painful knees may require modification in positioning to minimise discomfort at these joints, and some older adults may require assistance to get down or up from the position. 4.3. Lumbar spine

4.1. Cervical spine The separate measurement of upper and lower cervical ROM provided valuable information about the contribution of these functionally different regions to overall head movement. When older adults flexed their head the movement was primarily limited in the upper cervical spine. On the other hand, the lower cervical spine was more restricted during attempts to extend the head and neck. These age-related changes in upper and lower cervical flexibility may possibly be explained by the forward head posture seen in the older group. As the upper cervical starting position was more extended (by 12.2 ) it is possible that adaptive shortening in suboccipital muscles and ligaments may have limited head nodding. In contrast, older adults’ lower cervical spine had the biomechanical advantage of moving into flexion because it was already positioned in more flexion (by 9.2 ). This mechanism involving habitual posture and structural adaptation can explain age-related changes in the maximal available upper and lower cervical extension angles. Similar findings were found in young adults where a forward head posture affected the total sagittal motion of the cervical spine (Fiebert et al., 1999).

Results confirmed that the commonly used movement test, toetouch in standing, produced greater lumbar flexion than the alternative movement test, cat-stretch in the all-fours position. At the end position of toe-touch, tension in hamstrings possibly limited movement of the pelvis, and the gravity acting on the upper body aided lumbar flexion. In other words, the lumbar spine was ‘passively’ stretched from both ends. On the other hand, arching the lumbar spine toward the ceiling in the all-fours position involved active contraction of abdominal muscles to flex the lumbar region against gravity. Therefore, it was not unexpected that the maximal available lumbar flexion angle achieved by toe-touch was greater than that obtained during the cat-stretch. Although lumbar flexion was decreased in the older subjects, lumbar extension was not significantly altered, possibly because at best the lumbar spine only has a relatively small range of extension at each segmental level, as shown by the radiological studies of Pearcy et al. (1984). A direct comparison of lumbar extension values with those previously reported was limited due to different measurement instruments and test movements. An advantage of the cat-stretch for measurement of lumbar extension is the removal of potential balance problems associated with use of dual

622

Y.-L. Kuo et al. / Manual Therapy 14 (2009) 618–622

inclinometers (Gerhardt et al., 2002) in standing. However, a greater range of (passive) lumbar extension may be achieved by instructing subjects to push up on their hands in the prone position. These results showing decreased ranges of spinal motion in older adults are in agreement with previous studies, however few studies have measured the upper and lower cervical spine separately and no study has compared age-related differences using surface-based methods. Greater differences in ranges of spinal motion would be expected in a more sedentary group of older adults or older adults with pathology. As a result of these findings, future studies need to include age-matched controls when investigating ROM. As with all surface-based measurement techniques, the reliability of the angles measured in this study depended largely on the operator’s ability to locate body landmarks for marker placement. Although high reliability was established in a test-retest pilot study by the investigator on the same day, the reliability over a longer time frame, and between operators, needs to be established for clinicians wishing to adopt this method. 4.4. Clinical implication The measurement method used in this study has several advantages over use of simple clinical tools, such as a universal goniometer (Norkin and White, 2003) or dual inclinometers (Gerhardt et al., 2002). Video analysis removes the problem of trying to align the stationary arm of the goniometer to an estimated vertical line, or hold the flat base of two inclinometers against a curved surface. Moreover, patients do not have to hold the end range position, which may be painful in many cases. They can move easily towards and away from the limit position without restraint from the investigator’s attempt to position and read the measurement tool. In addition, as the effect of hypomobility of one spinal region may be accompanied by compensatory hypermobility in an adjacent region, video analysis has the advantage of measuring more than one joint or region at the same time. Thus the interaction of the spinal regions within the kinematic chain can be evaluated. The model of skin marker placement has a broader implication in the clinical setting. Skin reference markers can be quickly attached to the subject, and a digital camera used to obtain a sagittal image of the patient in the end range position. The limit angle for the joint of interest can then be measured on the image at a later time, using easy-to-use and freely downloadable image analysis software, ImageJ (Rasband, 1997–2007). 5. Conclusion Using surface-based measurement, older adults demonstrated significantly decreased flexion/extension ranges in the cervical, thoracic and lumbar spine compared to young adults. The movement of ‘cat-stretch’ was a feasible alternative for ROM measurement in the thoracic and lumbar spine. Thoracic extension achieved in the all-fours position was greater than in sitting, however the

‘cat-stretch’ did not appear effective in showing possible group differences in lumbar extension, and the ‘toe-touch’ in standing permitted greater lumbar flexion. The obtained images, with ROM values attached, can provide a useful record in the patient’s history. References Dillard J, Trafimow J, Andersson GBJ, Cronin K. Motion of the lumbar spine – reliability of 2 measurement techniques. Spine 1991;16:321–4. Dvorak J, Vajda EG, Grob D, Panjabi MM. Normal motion of the lumbar spine as related to age and gender. European Spine Journal 1995;4:18–23. Fiebert IM, Roach KE, Yang SS, Dierking LD, Hart FE. Cervical range of motion and strength during resting and neutral head postures in healthy young adults. Journal of Back and Musculoskeletal Rehabilitation 1999;12:165–78. Gerhardt J, Cocchiarella L, Lea R. Measuring joints in the spine. In: The practical guide to range of motion assessment. The American Medical Association; 2002. p. 25–45 [chapter 2]. Hu HT, Li ZZ, Yan JB, Wang XF, Xiao H, Duan JY, et al. Measurements of voluntary joint range of motion of the Chinese elderly living in Beijing area by a photographic method. International Journal of Industrial Ergonomics 2006;36:861–7. Jackson K. Fitting of mathematical functions to biomechanical data. IEEE Transactions on Biomedical Engineering 1979;26:122–4. Kuhlman KA. Cervical range of motion in the elderly. Archives of Physical Medicine and Rehabilitation 1993;74:1071–9. Kuo Y-L, Tully EA, Galea MP. Skin movement errors in measurement of sagittal lumbar and hip angles in young and elderly subjects. Gait & Posture 2008;27:264–70. Loebl WY. Measurement of spinal posture and range of spinal movement. Rheumatology 1967;9:103–10. McGill SM, Yingling VR, Peach JP. Three-dimensional kinematics and trunk muscle myoelectric activity in the elderly spine: a database compared to young people. Clinical Biomechanics 1999;14:389–95. Merritt JL, McLean TJ, Erickson RP, Offord KP. Measurement of trunk flexibility in normal subjects: reproducibility of 3 clinical methods. Mayo Clinic Proceedings 1986;61:192–7. Miller SA, Mayer T, Cox R, Gatchel RJ. Reliability problems associated with the modified Schober technique for true lumbar flexion measurement. Spine 1992;17:345–8. Moll JMH, Wright V. Normal range of spinal mobility: objective clinical study. Annals of the Rheumatic Diseases 1971;30:381–6. doi:10.1136/ard.30.4.381. Norkin CC, White DJ. The cervical spine. In: Measurement of joint motion: a guide to goniometry. 3rd spiral ed. F.A. Davis Company; 2003. p. 181–96 [chapter 10]. Pearcy M, Portek I, Shepherd J. Three-dimensional x-ray analysis of normal movement in the lumbar spine. Spine 1984;9(3):294–7. Persson PR, Hirschfeld H, Nilsson-Wikmar L. Associated sagittal spinal movements in performance of head pro- and retraction in healthy women: a kinematic analysis. Manual Therapy 2007;12:119–25. Portek I, Pearcy MJ, Reader GP, Mowat AG. Correlation between radiographic and clinical measurement of lumbar spine movement. British Journal of Rheumatology 1983;22:197–205. Rasband WS. ImageJ, http://rsb.info.nih.gov/ij/ 1997–2007 [accessed 20.02.07]. Saur PMM, Ensink F-BM, Frese K, Seeger D, Hildebrandt J. Lumbar range of motion: reliability and validity of the inclinometer technique in the clinical measurement of trunk flexibility. Spine 1996;21:1332–8. Sforza C, Grassi G, Fragnito N, Turci M, Ferrario VF. Three-dimensional analysis of active head and cervical spine range of motion: effect of age in healthy male subjects. Clinical Biomechanics 2002;17:611–4. Tully EA, Stillman BC. Computer-aided video analysis of vertebrofemoral motion during toe touching in healthy subjects. Archives of Physical Medicine and Rehabilitation 1997;78:759–66. Tully EA, Wagh P, Galea MP. Lumbofemoral rhythm during hip flexion in young adults and children. Spine 2002;27:E432–40. Winter DA. Kinematics, Biomechanics and motor control of human movement. 3rd ed. New Jersey: John Wiley & Sons; 2005 [chapter 2], pp 13–57. Wu SK, Lan HHC, Kuo LC, Tsai SW, Chen CL, Su FC. The feasibility of a video-based motion analysis system in measuring the segmental movements between upper and lower cervical spine. Gait & Posture 2007;26:161–6.

Manual Therapy 14 (2009) 623–629

Contents lists available at ScienceDirect

Manual Therapy journal homepage: www.elsevier.com/math

Original Article

Reliability, validity and diagnostic accuracy of palpation of the sciatic, tibial and common peroneal nerves in the examination of low back related leg painq Jeremy Walsh a, *, Toby Hall b, c a

School of Physiotherapy, Royal College of Surgeons in Ireland, 123 St. Stephen’s Green, Dublin 2, Ireland School of Physiotherapy, Curtin University, Perth, Australia c Manual Concepts, Perth, Australia b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 24 June 2008 Received in revised form 2 December 2008 Accepted 14 December 2008

This study investigated the reliability, validity and diagnostic accuracy of manual palpation of the sciatic, tibial and common peroneal nerves in the examination of 45 subjects with low-back related leg pain. The nerves were palpated manually and with an algometer, to determine pressure pain thresholds (PPTs). A second examiner performed the straight leg raise (SLR) and slump tests to determine nerve trunk mechanosensitivity. The procedure was repeated by another examiner to determine inter-rater reliability (n ¼ 20). Kappa scores for agreement between raters for manual palpation were 0.80, 0.70 and 0.79 for the sciatic, tibial and common peroneal nerves respectively, demonstrating excellent reliability. PPTs were significantly lower on the symptomatic side, for each of the three nerves, in subjects who were positive on manual palpation. In subjects who were negative on manual palpation, PPTs were not significantly different between sides, demonstrating criterion-based validity, using PPT as the criterion. Highest scores of diagnostic accuracy were obtained when two or more of the three nerves were positive on palpation (sensitivity ¼ 0.83; specificity ¼ 0.73). Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Sciatic Tibial Common peroneal Nerve Palpation Reliability Validity Sensitivity and specificity

1. Introduction Neural tissue mechanosensitivity (local tenderness over nerve trunks and pain in response to limb movements that elongate the nerve) is a recognised feature of pain of neural origin (Dilley et al., 2005; Hall and Elvey, 2005). The straight leg raise (SLR) (Hall et al., 1998) and slump (Maitland, 1979) tests are used to assess mechanosensitivity of the sciatic nerve tract. Reproduction of symptoms in response to the SLR or slump tests, which is intensified by ankle dorsiflexion, is considered as one factor in the determination of sciatic nerve mechanosensitivity (Hall and Elvey, 2005). Nerve palpation has been advocated as an additional assessment technique in the examination of neural tissue pain disorders (Butler, 1989; Elvey and Hall, 1997; Jepsen et al., 2006). Under normal circumstances, peripheral nerve trunks are usually painless to non-noxious stimuli (Hall and Quintner, 1996). However, if the nerve trunks are inflamed, even mild mechanical provocation, such as gentle palpation, can cause pain and protective

q This work is attributed to the institution: Discipline of Physiotherapy, Trinity College Dublin, Dublin 2, Ireland. * Corresponding author. Tel.: þ353 1 4022258; fax: þ353 1 4022471. E-mail address: [email protected] (J. Walsh). 1356-689X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2008.12.007

muscle responses (Hall and Quintner, 1996). Therefore, if the sciatic nerve tract is sensitized and pain is provoked by the SLR and slump tests, then a similar pain response should be elicited by gentle nerve palpation. Furthermore, the increased sensitivity of nerve trunks to palpation (Hall and Quintner, 1996; Dilley et al., 2005) should be manifested by reduced pressure pain thresholds (PPTs) (Sterling et al., 2000). However, no studies have evaluated nerve palpation in the lower limb. The aim of this study was to determine the reliability, validity and diagnostic accuracy of manual palpation of the sciatic, tibial and common peroneal nerves in the examination of low-back related leg pain. 2. Methods In studies of diagnostic accuracy, the index test under review is compared with a reference standard (Bossuyt et al., 2003). Manual palpation was the index test and in the absence of a gold standard for sciatic nerve mechanosensitivity, the SLR and slump tests were used as the reference standard. Ethical approval was granted by the St. James’s Hospital/Adelaide and Meath hospitals incorporating the National Children’s Hospital Joint Research Ethics Committee. Subjects were able to withdraw from the study at any time and gave written informed consent prior to the study commencement.

624

J. Walsh, T. Hall / Manual Therapy 14 (2009) 623–629

2.1. Subjects Subjects were recruited from consecutive patients attending the Back Pain Screening Clinic (BPSC) at the Adelaide and Meath hospitals incorporating the National Children’s Hospital (AMNCH), Dublin, in June/July 2007. All patients underwent screening examination by one of the two attending BPSC physiotherapists as routine. Recruitment was based on presenting symptoms as determined during this examination. Consecutive patients who satisfied the inclusion criteria (presence of unilateral low-back related leg pain, able to understand English, age 18–70) and were not disqualified by the exclusion criteria (absence of unilateral lowback related leg pain, signs of serious pathology, history of spinal surgery or neurological disease, unable to tolerate testing process), were invited to participate in the study. Data collection was planned before the index test and reference standard were performed. 2.2. Procedure 2.2.1. Manual palpation Data were collected in the physiotherapy department at the AMNCH by three examiners who were aware of the inclusion and exclusion criteria and the presenting symptoms. After routine examination by the BPSC physiotherapist, participating subjects were seen immediately by the first examiner (Tester 1, who had been qualified as a physiotherapist for eleven years and had completed a Masters in Manipulative Therapy qualification seven years previously). Manual palpation was performed according to a standardised procedure (Fig. 1) using gentle pressure at three locations: the sciatic nerve at the midway point of a line from ischial tuberosity to the greater trochanter of the femur; the tibial nerve where it bisects the popliteal fossa at the mid-point of the popliteal crease; and the common peroneal nerve where it passes behind the head of fibula to wind around the neck of fibula (Field and Hutchinson, 2006; Moore and Dalley, 2006). Subjects wore shorts and were positioned in prone lying for palpation of the sciatic and tibial nerves and in crook lying for the common peroneal nerve. Nerves were palpated bilaterally, simultaneously. Subjects were asked if there was any pain or discomfort and if so, on which side. If pain or discomfort was reported bilaterally, the subject was asked if it was worse on one side and if so which side. Reporting of pain or discomfort on the symptomatic side, or more pain or discomfort on the symptomatic side compared to the asymptomatic side was recorded as positive. Otherwise, a negative finding was recorded. Fig. 1. Manual palpation at the a) sciatic, b) tibial and c) common peroneal nerves.

2.2.2. Mechanical palpation (PPT) Following manual palpation, mechanical palpation was performed (Fig. 2). An electronic digital algometer (Somedic AB) was used to record PPT. This consists of a circular probe with a 2 cm2 round rubber tip connected to a pressure transducer within the handle of the unit. The tester held the handle in his right hand and brought the rubber tip into contact with the site to be tested so that the probe was held perpendicular to the limb, stabilised by the testers left thumb and index finger (Sterling et al., 2000). Pressure was then applied by the tester at a rate of 50 kPa/s. Subjects were instructed to press a switch when the sensation under the probe changed from one of pressure, to one of pressure and pain. At this time the application of pressure was terminated and the measurement was stored in the memory of the algometer. To familiarise subjects with the procedure, a preliminary trial was first performed on the forearm. For each nerve, three measures were taken (at the same sites as used in the manual palpation component of the examination) on the asymptomatic side followed by the symptomatic side, with a 10 s rest period between each

measurement. The mean of these three measures was taken as the PPT for each site. The sciatic nerve was tested first followed by the tibial and common peroneal nerves in order. 2.2.3. SLR and slump tests On completion of the nerve palpation examination, the SLR and slump tests were immediately performed on each side (asymptomatic limb followed by symptomatic limb) on all subjects by a second examiner (Tester 2, who had been qualified as a physiotherapist for one year and was blinded to the findings of the first examiner). For the SLR test, the subject was positioned in supine lying with the head resting on a pillow (the same pillow was used for all subjects for standardisation). The examiner passively raised the limb into hip flexion (maintaining neutral adduction/abduction and internal/external rotation) with knee extension until significant resistance to the movement was detected by the examiner, or the subject reported pain, at which point the location of any

J. Walsh, T. Hall / Manual Therapy 14 (2009) 623–629

625

dorsiflexed and it was determined whether this had the effect of rendering the presenting symptoms the same, better or worse. For both tests, if the subject experienced pain in the starting position (supine lying for the SLR test, slumped sitting with cervical flexion for the slump test), hip flexion (SLR) or knee extension (slump) was performed to the onset of significant resistance, or an increase in starting pain (rather than the onset of pain), after which the procedure used for subjects without pain in the starting position was followed. For each test, reproduction of presenting symptoms, which was made worse by dorsiflexion, was recorded as a positive finding – any other responses were recorded as negative. Subjects who were positive on both SLR and slump tests were recorded as positive for sciatic nerve mechanosensitivity, while those who were negative on one or both tests were recorded as negative for sciatic nerve mechanosensitivity. To establish the reliability of testing procedures, a third examiner (Tester 3, a qualified physiotherapist with three months clinical experience, blinded to the findings of the other examiners) immediately repeated the entire procedure in the first 20 subjects. 2.3. Data analysis 2.3.1. Reliability Manual palpation findings of Tester 1 and SLR test and slump test findings of Tester 2 were cross-tabulated by those of Tester 3 and the Kappa (k) statistic was used to determine inter-rater reliability of manual palpation, the SLR and slump tests. To determine the inter-rater reliability of mechanical palpation, Intraclass Correlation Coefficients (ICCs) were determined for each site, using a two way ANOVA (mixed effects model). Mean differences (and 95% confidence intervals) in PPT measures at each site between the two raters were calculated (Rankin and Stokes, 1998). The standard error of measurement (SEM) was also calculated, using the formula (SEM ¼ S  O(1  ICC)), where S is the pooled standard deviation and ICC is the reliability coefficient (O’Sullivan et al., 2007). 2.3.2. Validity Subjects were categorised according to whether they were negative or positive on manual palpation. To determine validity of manual palpation, using PPT as the criterion, paired t-tests were used to compare PPTs between the symptomatic and the asymptomatic legs in subjects who were either negative or positive on manual palpation.

Fig. 2. Mechanical palpation, using an algometer at the a) sciatic, b) tibial and c) common peroneal nerves.

response was ascertained through verbal questioning. In the event that presenting symptoms were reproduced, the ankle was then passively dorsiflexed and it was ascertained whether this had the effect of rendering the presenting symptoms the same, better, or worse. For the slump test, the subject was placed in slumped sitting with cervical flexion by the examiner and asked to maintain this position for the duration of the test. The knee was passively extended to the point of significant resistance as detected by the examiner, or the onset of pain. The location of any response was determined through verbal questioning. In the event that presenting symptoms were reproduced, the ankle was then passively

2.3.3. Diagnostic accuracy Manual palpation findings were cross-tabulated by mechanosensitivity findings. Sensitivity, specificity, positive predictive values (PPVs) and negative predictive values (NPVs) were determined for manual palpation at the sciatic, tibial and common peroneal nerves and also for ‘one or more’, ‘two or more’ and ‘three out of three’ positive manual palpation sites. 95% confidence intervals around the observed k values and around the estimates of diagnostic accuracy were determined by the general method described by Fleiss (1981) and implemented in an online web calculator (www.statpages.org). 3. Results 3.1. Participants Of 134 consecutive new patients attending the BPSC, 55 were excluded from the study for the following reasons: absence of leg pain (47), unable to understand English (3), history of spinal surgery (1), suspected serious pathology (3), unable to tolerate

626

J. Walsh, T. Hall / Manual Therapy 14 (2009) 623–629

testing position (1) (Fig. 3). Therefore, 79 patients were invited to take part, of whom 34 declined, and so 45 subjects participated. Characteristics of the 45 study patients are detailed in Table 1, all of whom underwent the index test and the reference standard. There were no inconclusive or indeterminate results and no adverse events from performing any of the tests. 3.2. Reliability 3.2.1. Manual palpation Manual palpation findings of Tester 1 and SLR test and slump test findings of Tester 2 were cross-tabulated by those of Tester 3 (Table 2). k scores and 95% confidence intervals for agreement between the two raters for nerve palpation and mechanosensitivity tests are detailed in Table 3. Substantial agreement was found for all tests (Landis and Koch, 1977). 3.2.2. Mechanical palpation Mean PPTs for Tester 1 and Tester 3 at each of the three sites on both sides are presented in Table 4. ICCs ranged from 0.85 to 0.96, demonstrating excellent reliability. Mean differences between raters (ranging from 14 to 11) were all close to zero indicating excellent agreement (Rankin and Stokes, 1998), while the 95% confidence interval around the mean differences contained zero in all cases, indicating a lack of bias between raters (Brennan and Silman, 1992). 3.3. Validity Twenty-seven, 20 and 24 subjects were positive on manual palpation at the sciatic, tibial and common peroneal nerves, respectively. There were no significant differences in PPTs between sides at any of the nerves in subjects who were negative on manual palpation. In subjects who were positive on manual palpation, mean PPTs were significantly lower on the symptomatic side compared to the asymptomatic side for each of the nerves (Fig. 4 and Table 5).

Table 1 Participant characteristics. Characteristic Gender Male Female Age Mean (SD) Range Mean (SD) duration of symptoms Mean (SD) pain intensity

Value 22 23 46 (11) years 26–70 years 5.6 (5.7) months 6.1 (2.6)/10

3.4. Diagnostic accuracy No subjects reported pain in the starting position for either test. Twenty-three subjects were positive on SLR testing while 22 were positive on slump testing. Twenty subjects were positive on both tests and so determined positive for sciatic nerve mechanosensitivity. Cross tabulations of the results of the nerve palpation tests by the results of the mechanosensitivity test are presented in Table 6. 3.4.1. Estimates Sensitivity, specificity, PPVs, and NPVs, with 95% confidence intervals, for nerve palpation are detailed in Table 7.

4. Discussion Radiating leg pain is a common problem affecting up to 57% of patients with low-back pain (Selim et al., 1998). Twenty-five subjects were found to be negative on either or both the SLR and slump tests and so determined to be negative for sciatic nerve mechanosensitivity. These subjects were assumed to have some other source of low-back related leg pain, e.g. somatic referred pain, although this is only conjecture and goes beyond the scope of this study. The relatively high proportion of subjects with a positive SLR and slump test (20/45) reflects the importance of nerve trunk mechanosensitivity in low-back related leg pain. Classification of patients with low-back related leg pain into various sub-categories,

Fig. 3. Procedural flowchart for ‘2 or more’ positive manual palpation sites.

J. Walsh, T. Hall / Manual Therapy 14 (2009) 623–629 Table 2 Cross tabulations for manual palpation, SLR test and slump test findings of Tester 1 by those of Tester 3 (inter-rater reliability, n ¼ 20).

Manual palpation

Sciatic Tibial Common peroneal

Mechanosensitvity

SLR Slump

P N P N P N P N P N

a

Sciatic Nerve Symptomatic Leg

350

Tester 3 P

N

8 1 9 1 7 1 8 1 8 3

1 10 2 8 1 11 1 10 0 9

Asymptomatic Leg

300 250

PPT

Tester 1

627

**

200 150 100 50 0

P ¼ Positive, N ¼ Negative.

-ve (n=18)

+ve (n=27)

Manual Palpation

Manual palpation

Sciatic Tibial Peroneal

SLR Slump

k

(95% CI)

0.8 0.7 0.79 0.8 0.71

(0.39, (0.28, (0.38, (0.39, (0.33,

0.94) 0.86) 0.94) 0.94) 0.71)

b

Tibial Nerve

350

Symptomatic Leg

300

Asymptomatic Leg

250

PPT

Table 3 Inter-rater reliability of manual palpation. Kappa (k) scores for agreement for manual palpation, SLR and slump tests (n ¼ 20) with 95% confidence intervals (CI).

200 150

*

100

Table 4 Inter-rater reliability and agreement for mechanical palpation (PPT) (n ¼ 20). Site

Side Mean PPT (kPa)

Diff. (95%CI)

ICC (95%CI)

11 1 4 14 3 2

0.96 0.92 0.87 0.96 0.91 0.85

SEM (kPa)

Tester 1 Tester 3 Sciatic

A S Tibial A S Common peroneal A S

310 260 170 149 167 148

299 259 174 163 170 146

(2, 34) (31, 33) (26, 18) (29, 1) (24, 18) (20, 24)

(0.91, (0.79, (0.66, (0.91, (0.78, (0.63,

0.99) 0.97) 0.95) 0.99) 0.97) 0.94)

25 35 25 16 23 25

A ¼ asymptomatic, S ¼ symptomatic, kPa ¼ kilopascals, Diff. ¼ mean difference in PPT between testers, CI ¼ confidence interval, ICC ¼ intraclass correlation coefficient, SEM ¼ standard error of the measurement.

50 0

-ve (n=25)

+ve (n=20)

Manual Palpation

c

350

Common Peroneal Nerve Symptomatic Leg

300

Asymptomatic Leg

250

PPT

with targeted intervention, has been suggested as a mean of improving treatment outcome (Schafer et al., 2009) and there is preliminary evidence to support this (Schafer et al., 2008). The presence of increased neural tissue mechanosensitivity identified in part by nerve palpation is one of the key factors in the classification of low-back related leg pain (Hall and Elvey, 2005; Schafer et al., 2009). k coefficients ranging from 0.61 to 0.80 represent substantial agreement between raters (Landis and Koch, 1977). In this study, k coefficients for manual palpation of the sciatic and common peroneal nerves were at the top end of this range (0.80 and 0.79, respectively). Although agreement between raters of manual palpation at the tibial nerve was also substantial (k ¼ 0.70), this was slightly less than that of the sciatic or common peroneal nerves. Reliability of palpation of lower limb nerve trunks has not previously been investigated. However, Jepsen et al. (2006) studied the inter-rater reliability of manual palpation of upper limb nerves. Moderate reproducibility was determined (k ¼ 0.53). Schmid et al. (2008) also investigated the inter-rater reliability of manual palpation at a number of sites of the medial, radial and ulnar nerves. k coefficients ranged from 0.36 to 0.79, while overall interrater reliability was moderate (k ¼ 0.59). Lower reliability for

200 150

**

100 50 0

-ve (n=21)

+ve (n=24)

Manual Palpation Fig. 4. Mean PPTs on symptomatic and asymptomatic sides in subjects who were either negative or positive on manual palpation at the a) sciatic, b) tibial and c) common peroneal nerves. ve ¼ negative, þve ¼ positive, * ¼ difference is significant at the p < 0.05 level, ** ¼ significant at the p < 0.01 level.

manual palpation of upper limb nerves may be due to greater difficulty in isolating the nerves in the upper limb. Perhaps nerve size may be influential. Excellent reliability and agreement was determined for PPTs at all tested sites. This is consistent with asymptomatic upper limb nerve PPTs which were also found to have excellent inter-rater reliability with ICCs ranging from 0.92 to 0.97 (Sterling et al., 2000). To our knowledge there have been no previous reports of reliability of PPT for lower limb nerve sites in symptomatic subjects. The finding that PPTs were significantly lower on the symptomatic side in subjects who were positive on manual palpation, while there were no significant differences between sides in subjects who were negative on manual palpation, demonstrates

628

J. Walsh, T. Hall / Manual Therapy 14 (2009) 623–629

Table 5 Validity of manual palpation. Difference in PPTs between sides in subjects who were either negative or positive on manual palpation. Site

Manual palpation

Side

Mean PPT (kPa)

Sciatic

ve

A S A S A S A S A S A S

298 292 284 208 168 159 141 115 149 164 144 116

þve Tibial

ve þve

Common peroneal

ve þve

Mean Diff. (95% CI)

p

6 (60, 49)

0.84

76 (98, 54)

0.85). The weighted kappa for the interobserver reliability of the SB in healthy subjects and in patients was

N.A. Roussel et al. / Manual Therapy 14 (2009) 630–635

633

Table 1 Localization of the injuries in dancers. Number of injuries (n ¼ 26) Hip Knee Muscles lower legs Ankle & Foot Spine Upper extremities

Fig. 3. Standing Bow. Reprinted with kind permission of Ó PhysioTools Ltd.2

0.80 and 0.78 respectively (p < 0.001). The Cronbach a-coefficient for internal consistency for ASLR, BKFO and KLAT was 0.83 for the patients and 0.65 for the healthy subjects (p < 0.01).

3 4 4 8 5 2

(12%) (15%) (15%) (31%) (19%) (8%)

months prospective study (see Table 1). Table 2 display the results of the movement control tests ASLR, BKFO and KLAT. Four dancers (13%) could not maintain the neutral position of the lumbar spine during SB. The mean Beighton score for generalized joint hypermobility was 4.0  2.3 (range:[0–9]). Fourteen of the 32 dancers (44%) scored above the 4/9 criterion for hypermobility (see Fig. 4). Eight of these 14 dancers (25%) presented a score ranging from 4 to 6, and six dancers (19%) were excessively hypermobile (score 7–9 according to the classification of Stewart and Burden (2004)). The movement control test battery was used in combination with the assessment of generalized joint hypermobility in order to analyze the predictive value of these tests, i.e. the prediction of the probability of developing injuries to the lower extremities or the lumbar spine. The dancers were divided into 2 groups based on the results of the prospective study (i.e. developing musculoskeletal injuries during the 6-months follow-up or not). A logistic regression model using KLAT and SB, correctly allocated 78% of the dancers in one of the 2 groups (p < 0.05). Data of the regression analysis is presented in Table 3. Generalized joint hypermobility did not correlate with the motor control tests (rho ranging between 0.03 and 0.33), and was neither associated with the development of musculoskeletal injuries (rho ¼ 0.03, p ¼ 0.89), nor with a history of LBP (rho ¼ 0.03, p ¼ 0.89). Dancers with a history of LBP did not develop more injuries than dancers without a history of LBP (p ¼ 0.93, t ¼ 0.90).

2.5. Statistical analysis All data were analyzed using SPSS 12.0Ó for Windows.3 A 1sample Kolmogorov–Smirnov goodness-of-fit test was used to examine whether the variables were normally distributed. All variables were found to be normally distributed (p > 0.05). A stepwise conditional logistic regression analysis, an independent t-test and Spearman correlation-coefficients were used, in addition to descriptive statistics. The development of injuries to the lower limbs and lumbar spine during the prospective part of the study was considered as the dependant variable. The significance level was set at 0.05, except for the correlation analysis, where the significance level was set at 0.01 to help protect against potential type-I errors. A power analysis (using SigmaStat4) determined that 25 subjects per group were necessary for the reliability analysis to establish statistical significance at a power of 0.90. This power analysis was based on a presumed correlation of 0.60 between the observers. 3. Results At baseline assessment, 63% of the dancers reported a history of LBP. Twenty-six injuries were registered in 32 dancers during the 6-

2

PhysioTools UK, 8 Culverwell Cottages, Pilton BA4 4DG, United Kingdom. 3 SPSS Inc. Headquarters, 233s. Wacker Drive, 11th floor, Chicago, Illinois 60606, USA. 4 Systat Software, Inc. 1735, Technology Drive, Ste 430, San Jose, CA 95110, USA.

4. Discussion Results regarding the relationship between joint hypermobility and injury in dancers remain controversial (Klemp and Learmonth, 1984; McCormack et al., 2004). While hypermobile individuals may be asymptomatic, hypermobility may be a predisposing factor of musculoskeletal pain/injury (Kirk et al., 1967; Simmonds and Keer, 2007). However, it has been suggested recently that an evaluation of the quality of movement could be more important than measuring the quantity of movement in hypermobile individuals (Simmonds and Keer, 2007). For this reason, both movement control and generalized joint hypermobility were assessed in professional dancers in the present study. Our results show that two movement control tests are able to predict injuries in dancers. In contrast, generalized joint hypermobility is not associated with a higher prevalence of musculoskeletal injuries. Table 2 Mean (X) and Standard Deviations (SD) are given for Active Straight Leg Raise (ASLR), Bent Knee Fall Out (BKFO) and Knee Lift Abdominal Test (KLAT) in 32 dancers. Left side

ASLR Phase 1 (mm Hg) ASLR Phase 2 (mm Hg) BKFO (mm Hg) KLAT (mm Hg)

Left side

Right side

Right side

Mean (SD)

Range

Mean (SD)

Range

45.0 45.9 46.1 48.0

[34–52] [38–52] [40–54] [44–60]

43.9 45.1 45.3 47.2

[30–52] [38–54] [40–50] [44–54]

(3.93) (3.63) (2.73) (4.05)

(4.72) (3.56) (2.31) (2.68)

634

N.A. Roussel et al. / Manual Therapy 14 (2009) 630–635

Beigthon score 10

Count

8

6

4

2

0

0

1

2

3

4

5

6

7

8

9

B-Tot Fig. 4. : Spread of hypermobility ratings (Beigthon Total Score) in 32 dancers. B-Tot ¼ Beigthon Total Score (0–9); Count ¼ number of dancers with a particular Beigthon score.

Sixty-three percent of the dancers reported a history of low back pain. This is in line with the study by McMeeken et al. (2001), who found an incidence rate of 49% in female and 59% in male dancers. Twenty-six injuries occurred during the 6-months follow-up period: seventy-three percent to the lower extremities and nearly 20% to the spine. These results are in accordance with the literature about dance injuries (Garrick and Requa, 1993; Byhring and Bo, 2002). Dancers are therefore at increased risk for developing musculoskeletal complaints to the spine and lower extremities. The ability to stabilize the lumbopelvic region during limb movement has been studied in elite gymnasts (Mulhearn and George, 1999), but not in dancers. Mulhearn and George (1999) found an association between impaired postural muscle endurance, a lordotic posture and LBP. As they reported a cross-sectional study, no conclusions could be drawn about the causal relationship. In the present study, four simple tests were used to evaluate lumbopelvic movement control in a clinical setting. To our knowledge, ASLR, BKFO and KLAT have not been evaluated before with the PBU. Therefore the reliability and internal consistency were evaluated in LBP-patients and healthy subjects prior to the prospective study in dancers. Moderate to high ICC-values have been found for ASLR and BKFO, high ICC-coefficients were recorded for KLAT, and excellent inter-observer reliability was found for SB. The results of the reliability study therefore suggest that these tests can be used with acceptable reliability in clinical practice. The Cronbach a-coefficient for internal consistency for ASLR, BKFO and KLAT was high, suggesting that all these tests assess the same underlying dimension, i.e. impaired movement control. Interestingly, different compensatory strategies were observed during testing. While a posterior pelvic tilt was observed during the movement control tests in some subjects, anterior pelvic tilt was Table 3 Logistic Regression analysis in 32 dancers. KLAT ¼ Knee Lift Abdominal Test, Exp(B) ¼ Exponent of B-coefficient, CI ¼ Confidence Interval. B-coefficient

KLAT right Standing bow

0.531 2.173

Wald Z score

Exp(B)

5.920 4.740

0.588 8.782

p-Value

0.015 0.029

95%CI for Exp(B) Lower

Upper

0.383 1.242

0.902 62.086

also seen in others. Posterior pelvic tilt leads to a pressure increase, whereas anterior pelvic tilt decreases the pressure (Richardson et al., 1992). Unfortunately, only the maximal pressure excursion was registered and not the variation in pressure within one test performance. Anterior pelvic tilt and variation in pressure were indeed observed during clinical evaluation in dancers, but were not registered in the present study. A (hyper)lordotic posture is common in dancers and gymnasts and has been associated with an increased injury risk in female gymnasts (Steele and White, 1986). The increase in hyperlordosis during dancing could be the result of a deficit in abdominal control to counteract anterior pelvic tilt during hip extension. Further study is nevertheless required to verify this assumption. The hypermobility scores found in the dancers are comparable to other studies performed in dancers (Gannon and Bird, 1999). However, generalized joint hypermobility did not correlate with the motor control tests and was not associated with a history of LBP. Moreover, neither joint hypermobility or a history of low back pain, but instead the outcome of two lumbopelvic movement control tests at baseline measurement were able to predict the probability of developing injuries to the lower extremities or lumbar spine in the present study. These results can be explained by an optimal neuromuscular control which compensates a decrease of the passive stability system, due to joint hypermobility (Panjabi, 1992; Reeves et al., 2007). Altered lumbopelvic movement control may force the dancer to compensate in the lower limbs, leading to musculoskeletal injuries. A research of the existing literature revealed only one study examining the predictive value of a lumbopelvic motor control evaluation. Zazulak et al. (2007a, b) demonstrated that impaired core stability predicted the risk of knee injuries with high sensitivity and moderate specificity in female athletes. However, injuries to the lumbar spine, hips or ankles were not examined in their study. There is no other data available regarding the predictive value of lumbopelvic motor control tests. These preliminary results are exciting, and could have an important clinical consequence. Indeed, it is possible to improve lumbopelvic motor control during physiotherapy sessions. Our data suggest that especially dancers with a positive SB and low pressure increase during KLAT are at risk to develop injuries to the lower limbs. An uncontrolled anterior pelvic tilt may account for this negative relationship in the regression analysis between the pressure results during KLAT and the increased risk for developing injuries. As the pelvic movement was not directly measured in the present study, further study of these interactions is required. 4.1. Study limitations Firstly, only the maximal pressure deviation was monitored during the tests. Some subjects first increased the pressure and afterwards decreased the pressure during the movement control tests. These variations in pressure were not registered. Secondly, the physical activity levels were not taken into account. All the students were equally active during the day (as they all have the same dance programme) but the amount of physical activity outside the dance lessons was not evaluated. This could have influenced the predictive analysis. Further research is therefore necessary. Finally, a standardized questionnaire was used for the registration of the injuries in combination with a subjective evaluation. There is no data available regarding the reliability and the validity of this questionnaire. 5. Conclusion The Knee Lift Abdominal Test and the Standing Bow can be used for the assessment of lumbopelvic movement control. Since these

N.A. Roussel et al. / Manual Therapy 14 (2009) 630–635

tests correctly allocated 78% of the dancers, they may be useful for the identification of dancers at risk for developing musculoskeletal injuries to the lower extremities and lumbar spine. In contrast, neither generalized joint hypermobility, evaluated with the Beigthon score, or a history of LBP is predictive of musculoskeletal injuries. Further research regarding the interaction between altered movement control and the prevention of injuries in dancers is required. Acknowledgement The authors would like to thank all the participants, physicians and physical therapists for their kind cooperation. Special thanks to Hilke Heselmans, Lander Gils, Joke Moonen, Ines Smits and Davina Caproni for aiding in data collection, to Cathy Devel for editing the manuscript, and to Mark Comerford and Raymond Lee for critical review of the manuscript. References Beighton P, Grahame R, Bird H. Hypermobility of joints. London: Springer Verlag; 1999. Byhring S, Bo K. Musculoskeletal injuries in the Norweigan National Ballet: a prospective cohort study. Scandinavian Journal of Medicine & Science in Sports 2002;12(6):365–70. Cairns MC, Harrison K, Wright C. Pressure biofeedback: a useful tool in the quantification of abdominal muscular dysfunction? Physiotherapy 2000;86(3):127–38. Comerford MJ, Mottram SL. Functional stability re-training: principles and strategies for managing mechanical dysfunction. Manual Therapy 2001;6(1):3–14. Comerford MJ, Mottram SL, Gibbons SGT. Diagnosis of mechanical back pain subgroups & stability retraining of the lumbar spine. UK: Kinetic Control, http:// www.kineticcontrol.com/clinicalNotes.asp; 2007. Crookshanks D. Safe dance report III: the occurrence of injury in the australian professional dance population. Caberra, Australia: Australia Dance Council; 1999. Cumps E, Verhagen E, Meeusen R. Prospective epidemiological study of basketball injuries during one competitive season: ankle sprains and overuse knee injuries. Journal of Sports Science and Medicine 2007;6:204–11. Falla DL, Campbell CD, Fagan AE, et al. Relationship between cranio-cervical flexion range of motion and pressure change during the cranio-cervical flexion test. Manual Therapy 2003;8(2):92–6. Ferrell WR, Tennant N, Sturrock RD, Ashton L, Creed G, Brydson G, et al. Amelioration of symptoms by enhancement of proprioception in patients with joint hypermobility syndrome. Arthritis & Rheumatism 2004;50(10):3323–8. Fitzcharles MA. Is hypermobility a factor in fibromyalgia? Journal of Rheumatology 2000;27:1587–9. Gannon LM, Bird HA. The quantification of joint laxity in dancers and gymnasts. Journal of Sports Sciences 1999;17:743–50. Garrick J, Requa R. Ballet injuries. An analysis of epidemiology and financial outcome. The American Journal of Sports Medicine 1993;21(4):586–90. Hall MG, Ferrell WR, Sturrock RD, Hamblen DL, Baxendale RH. The effect of the hypermobility syndrome on knee proprioception. British Journal of Rheumatology 1995;34(2):121–5. Hodges P, Richardson C, Jull G. Evaluation of the relationship between laboratory and clinical tests of transversus abdominis function. Physiotherapy Research International 1996;1(1):30–40. Hubley-Kozey CL, Vezina MJ. Differentiating temporal electromyographic waveforms between those with chronic low back pain and healthy controls. Clinical Biomechanics 2002;17(9–10):621–9. Jensen MP, Karoly P, Braver S. The measurement of clinical pain intensity: a comparison of six methods. Pain 1986;27(1):117–26. Jull G, Richardson CA, Toppenberg R, Comerford M, Bui B. Towards a measurement of active muscle control for lumbar stabilisation. Australian Journal of Physiotherapy 1993;39:187–93.

635

Kirk JA, Ansell BM, Bywaters EG. The hypermobility syndrome. Musculoskeletal complaints associated with generalized joint hypermobility. Annals of the Rheumatic Diseases 1967;26:419–25. Klemp P, Learmonth ID. Hypermobility and injuries in a professional ballet company. British Journal of Sports Medicine 1984;18:143–8. Klemp P, Stevens JE, Isaacs S. A hypermobility study in ballet dancers. Journal of Rheumatology 1984;11:692–6. Luomajoki H, Kool J, de Bruin ED, Airaksinen O. Reliability of movement control tests in the lumbar spine. BMC Musculoskeletal Disorders 2007;8:90. Maluf KS, Sahrmann SA, van Dillen LR. Use of a classification system to guide nonsurgical management of a patient with chronic low back pain. Physical Therapy 2000;80(11):1097–111. Mallik AK, Ferrell WR, McDonald AG, Sturrock RD. Impaired proprioceptive acuity at the proximal interphalangeal joint in patients with the hypermobility syndrome. British Journal of Rheumatology 1994;33(7):631–7. McMeeken JM, Tully E, Stillman B, Natrass C, Bygott I, Story I. The experience of back pain in young Australians. Manual Therapy 2001;6(4):213–20. McCormack M, Briggs J, Hakim A, Grahame R. Joint laxity and the benign joint hypermobility syndrome in student and professional ballet dancers. The Journal of Rheumatology 2004;31(1):173–8. Mottram S, Comerford M. A new perspective on risk assessment. Physical Therapy in Sport 2008;9:40–51. Mulhearn S, George K. Abdominal muscle endurance and its association with posture and low back pain. Physiotherapy 1999;85(5):210–6. Negus V, Hopper D, Briffa N. Associations between turnout and lower extremity injuries in classical ballet dancers. Journal of Orthopedic & Sports Physical Therapies 2005;35(5):307–18. Nijs J. Generalized joint hypermobility: an issue in fibromyalgia and chronic fatigue syndrome? Journal of Bodywork and Movement Therapies 2005;9:310–7. 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(4):242–55. Ogon M, Krismer M, So¨llner W, Kantner-Rumplmair W, Lampe A. Chronic low back pain measurement with visual analogue scales in different settings. Pain 1996;64(3):425–8. Panjabi MM. The stabilizing system of the spine. Part I. Function, dysfunction, adaptation, and enhancement. Journal of Spinal Disorders 1992;5:383–9. PhysioTools. Lumbar spine dynamic stability. Mark Comerford [Computer software module]. Reeves NP, Narendra KS, Cholewicki J. Spine stability: the six blind men and the elephant. Clinical Biomechanics 2007;22(3):266–74. Richardson CA, Jull GA, Toppenberg R, Comerford MJ. Techniques for active lumbar stabilisation for spinal protection: a pilot study. Australian Journal of Physiotherapy 1992;38:105–12. Roussel NA, Nijs J, Truijen S, Smeuninx L, Stassijns G. Low back pain. Clinimetric properties of the Trendelenburg test, the Active Straight Leg Raise test and the breathing pattern during the Active Straight Leg Raise test. Journal of Manipulative and Physiological Therapeutics 2007;30(4):270–8. Russek LN. Examination and treatment of a patient with hypermobility syndrome. Physical Therapy 2000;80:386–98. Sahrmann SA. Diagnosis and treatment of movement impairment syndromes. St Louis: Mosby; 2002. Simmonds JV, Keer RJ. Hypermobility and the hypermobility syndrome. Manual Therapy 2007;12:298–309. Steele VA, White JA. Injury prediction in female gymnasts. British Journal Sports Medicine 1986;20:31–3. Stewart DR, Burden SB. Does generalised ligamentous laxity increase seasonal incidence of injuries in male first division club rugby players? British Journal of Sports Medicine 2004;38:457–60. Wohlfahrt D, Jull GA, Richardson CA. The relationship between the dynamic and static function of abdominal muscles. Australian Journal of Physiotherapy 1993;39:9–13. Zazulak BT, Hewett TE, Reeves NP, Goldberg B, Cholewicki J. Deficits in neuromuscular control of the trunk predict knee injury risk: a prospective biomechanical-epidemiologic study. The American Journal Of Sports Medicine 2007a;35(7):1123–30. Zazulak BT, Hewett TE, Reeves NP, Goldberg B, Cholewicki J. The effects of core proprioception on knee injury: a prospective biomechanical-epidemiological study. The American Journal Of Sports Medicine 2007b;35(3):368–73.

Manual Therapy 14 (2009) 636–641

Contents lists available at ScienceDirect

Manual Therapy journal homepage: www.elsevier.com/math

Original Article

Cervical musculoskeletal impairment is common in elders with headache Sureeporn Uthaikhup a, *, Michele Sterling a, b, Gwendolen Jull a a

Division of Physiotherapy and National Health and Medical Research Council, Centre for Clinical Research Excellence in Spinal Pain, Injury and Health (CCRE Spine), School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia b Centre for National Research on Disability and Rehabilitation Medicine (CONROD), The University of Queensland, Queensland 4006, Australia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 11 September 2008 Received in revised form 2 December 2008 Accepted 19 December 2008

There is an opinion that with increasing cervical degenerative joint disease with ageing, cervicogenic headaches become more frequent. This study aimed to determine if cervical musculoskeletal dysfunction was specific to headache classifiable as cervicogenic or was more generic to headache in elders. Subjects (n ¼ 118), aged 60–75 years with recurrent headache and 44 controls were recruited. Neck function measures included range of motion (ROM), cervical joint dysfunction, cranio-cervical flexor muscle function, joint position sense (JPS) and cervical muscle strength. A questionnaire documented the characteristics of headaches for classification. A cluster analysis based on three musculoskeletal variables aligned previously with cervicogenic headache, divided headache subjects into two groups; cluster 1 (n ¼ 57), cluster 2 (n ¼ 50). Dysfunctions were greater in cluster 1 than in 2 for extension range and C1–2 joint dysfunction (p < 0.05). Most cervicogenic headaches were grouped in cluster 1, but musculoskeletal dysfunction was also found in headaches classifiable as migraine or tension-type headache. Neck dysfunction is not uniquely confined to cervicogenic headache in elders. Further research such as headache responsiveness to management of the neck disorder is required to better understand about the neck’s causative or contributing role to elders’ headache. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Elderly Headache Cervical spine Musculoskeletal dysfunction

1. Introduction Migraine and tension-type headaches are classified as primary headaches while cervicogenic headache is a secondary headache to a primary cervical musculoskeletal disorder (International Headache Society, 2004). A number of studies have documented cervical musculoskeletal dysfunction (CMD) in cervicogenic headache (Hall and Robinson, 2004; Zito et al., 2005). Not surprisingly, while CMD is the predominant feature of cervicogenic headache, it has been found to be generally absent in the primary migraine and tensiontype headaches (Zwart, 1997; Amiri et al., 2007; Jull et al., 2007). Headache continues to be a common complaint in the elderly, although the incidence declines with advancing age (Lyngberg et al., 2005). Classical features of migraine tend to change with age (Haan et al., 2007). Throbbing, nausea and vomiting are less common and neck pain triggers more frequent. It is possible that the incidence of secondary headache increases in the elderly. It is the opinion of some clinical researchers (Pearce, 1995; Biondi and Saper, 2000) that with increasing cervical degenerative joint disease with ageing, cervicogenic headache is common in the

* Corresponding author. Tel.: þ61 7 3365 2275; fax: þ61 7 3365 1622. E-mail address: [email protected] (S. Uthaikhup). 1356-689X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2008.12.008

otherwise healthy over 50 population. Little is known about the role of CMD in headache in elders although recent studies indicate that neck pain is a frequent feature of primary headaches in this age group (Kelman, 2006; Martins et al., 2006). Nevertheless age alone affects musculoskeletal function for example, both cervical range of motion (ROM) and muscle strength decrease with age (Dvorak et al., 1992; Jorden et al., 1999). Thus CMD may merely reflect agerelated changes rather than indicating a cervicogenic origin of headache. The aim of this study was to measure several aspects of cervical musculoskeletal function in elders with and without headache, to investigate whether CMD was more specific to headaches classifiable as cervicogenic or if it was also present in other headache types as a generic feature and an age-related factor. The measures included range of cervical movement, muscle function, JPS and manual examination of cervical joint dysfunction, features which have been found previously to be impaired in cervicogenic headache and cervical disorders (Zwart, 1997; Zito et al., 2005). The combination of reduced range of movement, symptomatic cervical joint dysfunction and impaired muscle function in the craniocervical flexion test has been shown to have high sensitivity and specificity for cervicogenic headache and differentiates it from primary headaches, such as migraine and tension-type and control subjects (Amiri et al., 2007; Jull et al., 2007). Thus in this study,

S. Uthaikhup et al. / Manual Therapy 14 (2009) 636–641

participants were sub-grouped on the basis of this combination of signs of CMD and the relationship between this grouping and classification of headache type was investigated. Muscle strength and JPS were added as secondary measures for a more complete musculoskeletal assessment. It was hypothesized that CMD would be greater in cervicogenic headache when compared to other headache and non-headache groups of elders.

2. Materials and methods 2.1. Subjects Volunteer healthy elders (age range 60–75 years) were sought for the study from the general community through a University Centre of Ageing and advertising in the local press. Headache group inclusion criteria were headaches at least once per month for the past year. A structured questionnaire was used to gain a medical history from all volunteers. Volunteers were excluded if headaches had been diagnosed as secondary to neurological or systemic disorders. Control subjects were eligible if they did not suffer from neck pain and were either headache free, or had no more than occasional mild headache ( 0.05). Variables

Cluster 1 (n ¼ 57)

Cluster 2 (n ¼ 50)

Control (n ¼ 44)

F

p Value

Extension (degrees)

31.0  1.06

48.6  1.00a

47.3  1.68a

66.8

0.00

14.0a,b (4.4–23.6) 46.0 (32.2–59.8) 58.0a (44.3–71.7) 0.45  0.03a

6.8b (0.6 to 14.2) 11.4 (1.8–20.2) 20.5 (9.0–33.0) 0.42  0.03a

Joint dysfunction (mean% (CI)) C0–1 28.1a (16.3–39.7) C1–2 64.9 (52.6–77.4) C2–3 68.4a (55.9–80.1) CCFT 22–26 0.40  0.02a mmHg (normalized RMS)c

CI: 95% confidence intervals. Values are mean  SE or as otherwise indicated. c The values are transformed data. d Chi-square value.

8.4d

0.02

29.3d

0.00

24.3d

0.00

0.9

0.41

S. Uthaikhup et al. / Manual Therapy 14 (2009) 636–641

639

flexion and rotation range and in the frequency of symptomatic joint dysfunction (C3–4 to C7–T1) (all p  0.01) (Table 3). There were no significant between group differences in flexion ROM, cranio-cervical muscle strength and cervical JPS (p > 0.01). There were trends for higher levels of dysfunction in cluster 1 than in cluster 2 in the majority of measures, but these only reached significance for cervical rotation range.

Table 4 Distribution of headache types in clusters.

Cluster 1 (n ¼ 57)

Cluster 2 (n ¼ 50)

Single headaches Migraine Tension-type Cervicogenic

11 (45.8) 7 (77.8) 16 (72.7)

13 (54.2) 2 (22.2) 6 (27.3)

24 9 22

3.4. Headache distribution between clusters

Non-classifiable headaches

13 (39.4)

20 (60.6)

33

5 (55.6) 5 (50)

4 (44.4) 5 (50)

9 10

In the classification of the 107 headache subjects, 24 were classified as migraine, 9 as tension-type, 22 as cervicogenic headaches, 33 headaches were unclassifiable and 19 subjects presented with two or more headaches. Cross-tabulations between headache classification and assigned cluster are presented in Table 4. As can be observed, while cluster 1 contained the majority of headaches classified as cervicogenic, it nevertheless contained all headache types. 3.5. Characteristics of headaches in clusters Headache characteristics were compared between clusters to determine whether or not there were distinguishing features of elders’ headache in cluster 1 with higher levels of associated CMD (Table 5). This analysis indicated that cluster 1 subjects had higher headache frequency (headaches  15 per month) and more frequently had a previous history of head or neck trauma (p < 0.05). 4. Discussion This study revealed the presence of CMD in elders with headache compared to healthy controls and CMD appears to be a generic feature of headache in this age group. Some distinction was made between headache in elders on the basis of the magnitude of CMD.

Table 3 Results of the differences in other cervical musculoskeletal variables. Means with the same letter (a or b) were not significantly different in post hoc between group analysis (p > 0.01). Variables ROM (degrees) Flexion Lateral flexion Axial rotation

Cluster 1 (n ¼ 57)

Cluster 2 (n ¼ 50)

Control (n ¼ 44)

F

p Value

40.9  1.38a 20.6  0.80a 46.0  1.20

42.4  1.29a 23.5  0.94a,b 52.6  1.34a

45.5  1.50a 25.0  0.85b 53.2  1.14a

2.6 6.5 10.9

0.07 0.00 0.00

Symptomatic cervical joint dysfunction (mean% (CI)) 48.0a 9.1 C3–4 54.4a (41.1–67.0) (34.2–61.8) (0.5–17.5) a a 42.0 6.8 C4–5 47.4 (34.0–60.0) (28.3–55.7) (0.6 to 14.2) a a 34.0 4.5 C5–6 43.9 (31.1–56.9) (20.9–47.1) (1.6 to 10.6) 22.0a 0 C6–7 24.0a (12.9–35.1) (10.5–33.5) (0–0) 0a C7–T1 15.8 4.0a (1.4 to 9.4) (0–0) (6.5–25.5)

23.9d

0.00

20.5

d

0.00

19.4

d

0.00

12.4d

0.00

10.4d

0.01

Muscle strength (Nm) 2.7  0.08a Cranio-flexionc Cranio-extensionc 2.7  0.10

2.7  0.09a 2.8  0.10a

2.6  0.09c 3.0  0.11a

0.2 3.6

0.80 0.03

Joint position error (degrees) Extension 5.1  0.36a Rotation (left) 3.8  0.28a Rotation (right) 5.5  0.53a

5.1  0.45a 3.3  0.22a 5.2  0.59a

4.3  0.37a 3.9  0.36a 5.2  0.55a

1.2 1.3 0.1

0.30 0.29 0.93

CI: 95% confidence interval. Values are mean  SE or as otherwise indicated. c The values are transformed data after controlling for gender. d Chi-square values.

Classification

Two or more headaches Cervicogenic headachea No cervicogenic headacheb Total

No. (%) of subjects

57

Total

50

107

a

Cervicogenic headache was classified as one of the subjects’ two or more headaches. b None of the headaches were classified as cervicogenic.

Subjects in cluster 1 (53% of the sample) displayed higher levels of CMD than those in cluster 2 and both clusters displayed more CMD than control subjects. The values for cervical musculoskeletal features measured across all groups are reduced when compared to values from younger populations (Dall’Alba et al., 2001; Prushansky et al., 2006) and would reflect age changes (ten Have and Eulderink, 1981; Dvorak et al., 1992). The changes in these elder headache groups cannot be attributed to ageing alone as they were significantly greater than those measured in the control group. Pearce (1995) and Biondi and Saper (2000) reasoned that with increasing cervical degenerative joint disease with age, cervicogenic headache becomes more common. Our results indicate a less distinct and perhaps more complex picture of headache in the elderly regarding the potential role of CMD. The majority of subjects with cervicogenic headache as a single headache (16/22) were grouped into cluster 1, the group with greater levels of CMD. Nevertheless elders with other headache types (11/24 migraine, 7/9 tension-type) were also grouped in this cluster. All headache types were represented in cluster 2 although only 20% were classified as cervicogenic headache (as a single or one of multiple headache). This cluster had less measured CMD than cluster 1, but still presented with more dysfunction than control subjects. Thus all headache subjects had CMD to a greater or lesser degree, regardless of headache classification or length of headache history, although a higher percentage of cluster 1 subjects (53% versus 32% in cluster 2) had frequent headaches (15 days per month). Our hypothesis of the greater relationship of CMD with cervicogenic headache than other headache types was rejected for our elders with headache. Hagen et al. (2002) also observed this interaction between musculoskeletal symptoms and both migrainous and nonmigrainous headache. Table 5 Summary of categorical variables in clusters 1 and 2 and significance values.

Demographics Gender, female (%) Age, years (mean  SD) BMI, kg/m2 (mean  SD) Headache history, years (mean  SD) Headache frequency, 15 days/month (%) Headache intensity, 1–10 VAS (mean  SD) NDI score, % score (mean  SD) Associated neck pain with headache (%) History of head-neck trauma (%) Co-existing musculoskeletal pain (%) VAS ¼ visual analogue scale.

Cluster 1 (n ¼ 57)

Cluster 2 (n ¼ 50)

p Value

52.6 65.8  4.3 27.0  4.0 26.3  19.0 52.6 6.4  2.0 26.2  13.4 77.2 43.9 66.7

64.0 65.7  4.7 25.7  4.4 25.7  18.6 32.0 6.3  2.3 21.8  12.3 67.3 22.0 56.0

0.24 0.91 0.11 0.87 0.03 0.87 0.08 0.26 0.02 0.26

640

S. Uthaikhup et al. / Manual Therapy 14 (2009) 636–641

The CMD in the headache of elders reflects that documented in other studies of cervicogenic headache. Reduced range of cervical extension and rotation has been reported previously (Zwart, 1997; Jull et al., 2007), as has palpable tenderness over the upper cervical joints (Jull et al., 2007; Sjaastad and Bakketeig, 2008). The results of the CCFT did not differ between the headache clusters when compared to controls as previously found in cervicogenic headache and neck pain disorders (Jull et al., 2004, 2007). The CCFT is a cognitive test which relies on fine motor skills. The performance of the test may reflect age effects on cognition, learning and motor skill acquisition (Wishart and Lee, 1997). The lack of differences between headache and control subjects in cranio-cervical extensor muscle strength may also reflect age-related changes in the muscle system (Jorden et al., 1999). There were no between group differences in cervical JPS as also noted by others (Zito et al., 2005; Jull et al., 2007). Headache classification was challenging. Approximately 30% could not be classified as the descriptions presented features that crossed the characteristics of tension-type, migraine and cervicogenic headaches. There was an unusually low incidence of tensiontype headache. It is probable, based on general headache epidemiology, that many of the unclassifiable headaches were tension-type. In addition, 19 subjects reported concurrent headaches. Difficulty in classification is not novel (Fishbain et al., 2001) and the overlap in headache symptoms has often been encountered (D’Amico et al., 1994; van Suijlekom et al., 1999). Indeed Srikiatkhachorn (1991) found that a large number of headaches in elders (61%) could not be classified using the IHS criteria, having characteristics of a combination of vascular and tension-type. This probably reflects the age-related changes in headache features (Haan et al., 2007). Even though an exclusive link between CMD and cervicogenic headache was not made in this study, the changing nature of headache together with the widespread presence of CMD in all headache types could support the possibility of a primary headache evolving to a secondary cervicogenic or mixed headache in the elderly (Kelman, 2006). Our results might suggest a possible cervical musculoskeletal contribution to a variety of headaches in the elderly. In line with this contention, the presence of neck pain with headache in our elders was common (75%), supporting Kelman’s (2006) findings in elders with primary headaches. Neck pain accompanies up to 60–80% of headaches in the general population (Hagen et al., 2002; Fishbain et al., 2003) but this does not necessarily infer a cervicogenic origin of pain (Jull et al., 2007). Neck pain may be a referred pain of a primary headache, reflecting the bidirectional pathway in the trigeminocervical nucleus (Bartsch and Goadsby, 2003). Conversely its origin may be in the periphery (cervical structures) consistent with the CMD measured in this study. Elders with headache also reported more frequent coexisting musculoskeletal pain than controls. The relative high incidence of co-morbid shoulder, back and knee pains in both headache clusters is consistent with other studies of chronic headache (Terwindt et al., 2000; Wiendels et al., 2006). Wiendels et al. (2006) also found that subjects with chronic headache had more co-morbid musculoskeletal pain than those with infrequent headache, which was supported in this study. Additionally, a history of neck trauma was more prevalent in cluster 1 subjects but trauma can precipitate either primary or secondary headaches (Radanov et al., 2001). This study demonstrated that symptomatic CMD beyond that which could be attributed to ageing is present in elders with headache which challenges diagnosis. While its role cannot be explained by this study, the results suggest that CMD might, in some cases, be the origin of headache (cervicogenic headache), in others it could be a trigger of headache (Cook et al., 1989; Solomon

et al., 1990), or its presence may indicate a transition from a primary to a secondary headache as an age-related process. Alternately the CMD may be merely a co-morbid feature which may compound the pain of an elder’s headache syndrome. Further research is required to better understand the role or impact of CMD on headache in elders and this might be achieved by examining the relative outcomes in a clinical trial of treatment to the neck. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.math.2008.12.008. References Amiri M, Jull G, Bullock-Saxton J, Darnell R, Lander C. Cervical musculoskeletal impairment in frequent intermittent headache, part 2: subjects with concurrent headache types. Cephalalgia 2007;27(8):891–8. Bartsch T, Goadsby PJ. Increased responses in trigeminocervical nociceptive neurons to cervical input after stimulation of the dura mater. Brain 2003;126(8): 1801–13. Biondi DM, Saper JR. Geriatric headache: how to make the diagnosis and manage the pain. Geriatric 2000;55(12):40–50. Cook N, Evans DA, Funkenstein HH, Scherr PA, Ostfeld AM, Taylor JO, et al. Correlates of headache in a population-based cohort of elderly. Archives of Neurology 1989;46:1338–44. Dall’Alba PT, Sterling MM, Treleaven JM, Edwards SL, Jull GA. Cervical range of motion discriminates between asymptomatic persons and those with whiplash. Spine 2001;26(19):2090–4. D’Amico D, Leone M, Bussone G. Side-locked unilaterality and pain localization in long-lasting headaches – migraine, tension-type headache, and cervicogenic headache. Headache 1994;34(9):526–30. Dvorak J, Antinnes JA, Panjabi M, Loustalot D, Bonomo M. Age and gender related normal motion of the cervical spine. Spine 1992;17(Suppl. 10):S393–8. Falla D, Dall’Alba P, Rainoldi A, Merletti R, Jull G. Location of innervation zones of sternocleidomastoid and scalene muscles: a basis for clinical and research electromyography applications. Clinical Neurophysiology 2002;113(1):57–63. Fishbain DA, Cutler R, Cole B, Rosomoff HL, Rosomoff RS. International Headache Society: headache diagnostic patterns in pain facility patients. Clinical Journal of Pain 2001;17(1):78–93. Fishbain DA, Lewis J, Cole B, Cutler RB, Rosomoff RS, Rosomoff HL. Do the proposed cervicogenic headache diagnostic criteria demonstrate specificity in terms of separating cervicogenic headache from migraine? Current Pain and Headache Reports 2003;7(5):387–94. Haan J, Hollander J, Ferrari M. Migraine in the elderly: a review. Cephalalgia 2007;27(2):97–106. Hagen K, Einarsen C, Zwart JA, Svebak S, Bovim G. The co-occurrence of headache and musculoskeletal symptoms amongst 51,050 adults in Norway. European Journal of Neurology 2002;9(5):527–33. Hall T, Robinson K. The flexion-rotation test and active cervical mobility: a comparative measurement study in cervicogenic headache. Manual Therapy 2004;9(4):197–202. ten Have HA, Eulderink F. Mobility and degenerative changes of the ageing cervical spine: a macroscopic and statistical study. Gerontology 1981;27(1–2):42–50. International Headache Society. The international classification of headache disorders: 2nd edition. Cephalalgia 2004;24(Suppl. 1):S1–151. Jorden A, Mehlsen J, Bulow PM, Ostergaard K, Danneskiold SB. Maximal isometric strength of the cervical musculature in 100 healthy volunteers. Spine 1999;24(13):1343–8. Jull G, Bogduk N, Marsland A. The accuracy of manual diagnosis for cervical zygapophysial joint pain syndromes. Medical Journal of Australia 1988;148(5):233–6. Jull G, Kristjansson E, Dall’Alba P. Impairment in the cervical flexors: a comparison of whiplash and insidious onset neck pain patients. Manual Therapy 2004;9(2):89–94. Jull G, Amiri M, Bullock-Saxton J, Darnell R, Lander C. Cervical musculoskeletal impairment in frequent intermittent headache, part 1: subjects with single headaches. Cephalalgia 2007;27(7):793–802. Kelman L. Migraine changes with age: IMPACT on migraine classification. Headache 2006;46(7):1161–71. Lyngberg AC, Rasmussen BK, Jorgensen T, Jensen R. Incidence of primary headache: a Danish epidemiologic follow-up study. American Journal of Epidemiology 2005;161(11):1066–73. Martins KM, Bordini CA, Bigal ME, Speciali JG. Migraine in the elderly: a comparison with migraine in young adults. Headache 2006;46(2):312–6. O’Leary SP, Vicenzino BT, Jull GA. A new method of isometric dynamometry for the craniocervical flexor muscles. Physical Therapy 2005;85(6):556–64. Pearce JMS. The importance of cervicogenic headache in the over-fifties. Headache Quarterly-Current Treatment and Research 1995;6(4):293–6.

S. Uthaikhup et al. / Manual Therapy 14 (2009) 636–641 Prushansky T, Pevzner E, Gordon C, Dvir Z. Performance of cervical motion in chronic whiplash patients and healthy subjects: the case of atypical patients. Spine 2006;31(1):37–43. Radanov BP, Stefano GD, Augustiny KF. Symptomatic approach to posttraumatic headache and its possible implications for treatment. European Spine Journal 2001;10:403–7. Revel M, Andre-Deshays C, Minguet M. Cervicocephalic kinesthetic sensibility in patients with cervical pain. Archives of Physical Medicine and Rehabilitation 1991;72(5):288–91. Sjaastad O, Fredriksen TA, Pfaffenrath V. Cervicogenic headache: diagnostic criteria. Headache 1998;38(6):442–5. Sjaastad O, Bakketeig LS. Migraine without aura: comparison with cervicogenic headache: vaga study of headache epidemiology. Acta Neurologica Scandinavia 2008;117(6):377–83. Solomon GD, Kunkel RS, Frame J. Demographics of headache in elderly patients. Headache 1990;30(5):273–6. Srikiatkhachorn A. Epidemiology of headache in the Thai elderly: a study in the Bangkae home for the aged. Headache 1991;31(10):677–81.

641

van Suijlekom JA, de Vet HCW, van den Berg SGM, Weber WEJ. Interobserver reliability of diagnostic criteria for cervicogenic headache. Cephalalgia 1999;19(9):817–23. Terwindt GM, Ferrari MD, Tijhuis M, Groenen SM, Picavet HS, Launer LJ. The impact of migraine on quality of life in the general population: the GEM study. Neurology 2000;55(5):624–9. Vernon H, Mior S. The Neck Disability Index: a study of reliability and validity. Journal of Manipulative and Physiological Therapeutics 1991;14(7):409–15. Wiendels NJ, van Haestregt A, Knuistingh Neven A, Spinhoven P, Zitman FG, Assendelft WJ, et al. Chronic frequent headache in the general population: comorbidity and quality of life. Cephalalgia 2006;26(12):1443–50. Williamson A, Hoggart B. Pain: a review of three commonly used pain rating scales. Journal of Clinical Nursing 2005;14(7):798–804. Wishart LR, Lee TD. Effects of aging and reduced relative frequency of knowledge of results on learning a motor skill. Perceptual and Motor Skills 1997;84(3 Pt 1):1107–22. Zito G, Jull G, Story I. Clinical tests of musculoskeletal dysfunction in the diagnosis of cervicogenic headache. Manual Therapy 2005;11(2):118–29. Zwart JA. Neck mobility in different headache disorders. Headache 1997;37(1):6–11.

Manual Therapy 14 (2009) 642–646

Contents lists available at ScienceDirect

Manual Therapy journal homepage: www.elsevier.com/math

Original Article

Abdominal muscle activity during abdominal hollowing in four starting positions Pakkanaporn Chanthapetch*, Rotsalai Kanlayanaphotporn 1, Chitanongk Gaogasigam, Adit Chiradejnant Department of Physical Therapy, Faculty of Allied Health Sciences, Chulalongkorn University, Soi Chula 12 Pathumwan, Bangkok 10330, Thailand

a r t i c l e i n f o

a b s t r a c t

Article history: Received 21 January 2008 Received in revised form 3 December 2008 Accepted 19 December 2008

The aim of this study was to investigate the activity of the rectus abdominis (RA), external abdominal oblique (EO), and transversus abdominis/internal abdominal oblique (TrA/IO) muscles during abdominal hollowing (AH) in four positions: crook lying, prone lying, four-point kneeling, and wall support standing. Thirty-two healthy participants, aged 21.3  0.8 years were recruited. They were instructed to perform maximal voluntary contraction (MVC) and AH. The electromyography (EMG) data of each muscle during AH were normalized as a percentage of MVC. During AH in all four starting positions, significant differences were found in the EMG activity of RA, EO, and TrA/IO (p < 0.001). The TrA/IO exhibited the highest while the RA exhibited the lowest EMG activity. Among the four different starting positions, only the TrA/IO showed significant difference in mean EMG activity (p < 0.001). The results suggest that all four starting positions can facilitate TrA/IO activity with minimal activity from RA and EO. Crown Copyright Ó 2009 Published by Elsevier Ltd. All rights reserved.

Keywords: Exercises Abdominal muscles Transversus abdominis Low back pain

1. Introduction Low back pain (LBP) is a common problem that occurs in the general population. One year prevalence of LBP has been reported to range from 40.5 percent to 64 percent (Barrero et al., 2006; Ihlebaek et al., 2006). It has been found that approximately 60–80 percent of the population report LBP once in their life time (Manchikanti, 2000; Ihlebaek et al., 2006). One hypothesis for the development of LBP is that there is a dysfunction in the control of the abdominal and back muscles (Panjabi, 1992; Richardson and Jull, 1995; O’Sullivan et al., 1997; Hides et al., 2001). Specific exercises that aim to train these trunk muscles to function properly are, thus, a contemporary approach for treating LBP. Abdominal hollowing (AH) is one of these exercises that is widely used in patients suffering from LBP (O’Sullivan et al., 1997; Hides et al., 2001; Rasmussen-Barr et al., 2003; Shaughnessy and Caulfield, 2004; Goldby et al., 2006). To learn how to perform AH, it is recommended that a patient with LBP should start practising AH in a position that facilitates the co-contraction of the deep abdominal and back muscles. When the patient can master AH, the starting position can be changed. The muscles that should be activated during AH are the transversus abdominis (TrA), the internal abdominal oblique (IO) (lower fibres), and the lumbar multifidus (deep fibres) which have * Corresponding author. E-mail addresses: [email protected] (P. Chanthapetch), rotsalai.k@ chula.ac.th, [email protected] (R. Kanlayanaphotporn). 1 Tel.: þ66 2 218 3765; fax: þ66 2 218 3766.

been proposed to function synergistically (Richardson et al., 2004). To be effective, co-contraction of these deep trunk muscles should occur in isolation from the rectus abdominis (RA) and the external abdominal oblique (EO) which lie superficially. Empirically, four positions have been suggested by clinicians as the starting positions for performing AH. These positions are crook lying (O’Sullivan, 2000), prone lying (Richardson and Jull, 1995; O’Sullivan, 2000), four-point kneeling (Richardson and Jull, 1995; Norris, 1999; O’Sullivan, 2000), and wall support standing (Norris, 1999). To date, there have been only two studies that have compared the effectiveness of the starting positions for performing AH (Beith et al., 2001; Urquhart et al., 2005). Beith et al. (2001) compared the prone lying to the four-point kneeling position and found no statistical difference in the activity of IO between positions. However, an isolated activation of IO tended to occur more easily in the four-point kneeling position than in prone lying position. Urquhart et al. (2005) compared crook lying with prone lying positions. They found that crook lying could encourage the TrA to work in isolation better than the prone lying position. The aims of this study were to determine 1) whether there was any significant difference in electromyography (EMG) activity among the three abdominal muscles in each of the four starting positions (crook lying, prone lying, four-point kneeling, and wall support standing); 2) whether there was any significant difference in the EMG activity of each muscle among the four different starting positions; and 3) whether there was any difference in the frequency of non-activation and isolation of three abdominal muscles among the four starting positions.

1356-689X/$ – see front matter Crown Copyright Ó 2009 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2008.12.009

P. Chanthapetch et al. / Manual Therapy 14 (2009) 642–646

2. Methods 2.1. Participants A convenience sample of 32 asymptomatic LBP (14 male, 18 female) took part in this study. Their mean  standard deviation of age was 21.3  0.8 years, their weight 50.2  8.2 kg, their height 1.64  0.08 m, and their body mass index was 18.6  1.8 kg/m2. The participants were recruited from the students and staff of the Faculty of Allied Health Sciences at the Chulalongkorn University. Participant recruitment commenced in September 2005 and continued until January 2006. They were excluded if they had a history of LBP, practised AH, or any abnormalities of the spinal column or abdominal region such as fractures, surgery, burns, or cancer. Moreover, participants with a skinfold thickness in the abdominal and supra-iliac area greater than 20 mm were also excluded. This aimed to decrease the EMG artifact due to adipose tissue lying between the surface electrodes and the tested muscles (Neumann and Gill, 2002). All the participants had thin skinfold (abdominal skinfold thickness was 16  4 mm and supra-iliac skinfold thickness was 9  3 mm). Ethical approval for the study was granted by the Research Ethics Committee, Chulalongkorn University, Thailand. 2.2. Procedure Participants gave written informed consent prior to participation in the study. Initially, all participants were trained to perform AH in four positions. The standard protocol suggested by Richardson and Jull (1995) as described below was practised until they were able to correctly perform the AH. After the training session, only the participants who could perform AH correctly continued with the study. Then, they were instructed to perform maximal voluntary contraction (MVC) and AH. The order of the position was randomly assigned using a 4  4 balanced Latin square (Portney and Watkins, 2000). All participants were tested in the afternoon.

643

extended. The distance from the wall to their heels was 6 inches (Norris, 1995). Briefly, the AH was performed by gently pulling the navel in and up while not allowing any movement at the spine, rib, or pelvis (Norris, 1995; Richardson and Jull, 1995; O’Sullivan, 2000). After the navel has been drawn close to the spine, the participants were instructed to hold the abdominal contraction for 10 s while continually breathing normally. This aimed to activate the TrA at a low level of muscle contraction which should be approximately 25 percent of its MVC (Richardson and Jull, 1995). The lumbar spine was kept in a neutral position such that the anterior superior iliac spine and posterior superior iliac spine were aligned vertically (Richardson et al., 2004). The duration of training for each participant varied from 10 to 40 min. 2.3. Measurement EMG recordings were made using silver/silver chloride surface electrodes of 1 cm in diameter which were placed with a centre-tocentre spacing of 2.2 cm (Ng et al., 1998). The three channels method was used in which a reference electrode for each muscle was placed adjacent to the paired electrodes of that muscle. All abdominal muscles were recorded on the right side by positioning the surface electrodes in parallel to the muscle fibres (Fig. 1). All EMG placements followed those recommended by Ng et al. (1998). For the RA, the electrodes were placed in a cephalad/caudad orientation at 2 cm inferior to the navel and 1 cm lateral to the midline. For the EO, the electrodes were placed diagonally on the inferior edge along a line connecting the most inferior point of the costal margin and the contralateral pubic tubercle. For the TrA and IO, the electrodes were placed in the area where the TrA and IO fuse together and this was called TrA/IO. The TrA/IO electrodes were placed horizontally at 2 cm inferior and medial to the anterior superior iliac spine (Marshall and Murphy, 2003). EMG were sampled at 1000 Hz over a bandwidth of 8–500 Hz using the ME3000P8 EMG systemÒ (Mega Electronics Ltd, Kuopio, Finland):

2.2.1. Maximal voluntary contraction All participants were asked to perform three manoeuvres which were expected to generate maximal EMG activity for each of the three abdominal muscles. These manoeuvres were trunk flexion, trunk flexion with rotation to the left, and trunk flexion with rotation to the right. Each manoeuvre was performed against manual resistance once in crook lying and then in sitting (Beith et al., 2001). During the performances, the participants were instructed to avoid any jerky contractions in order to decrease the chance of injury. Each manoeuvre was held for 5 s with a 2-min rest between trials to prevent muscle fatigue (Ng et al., 2002). For each muscle, the greater EMG that was produced either in the crook lying or sitting position was chosen as a reference value for normalization. 2.2.2. Abdominal hollowing All participants were required to perform AH for 10 s, three times in each position, with a 1-min rest between each time. For the crook lying position, the knees were flexed at 90 (Drysdale et al., 2004). For the prone lying position, a small pillow was placed under the ankles (Richardson and Jull, 1995). For the four-point kneeling position, the participants were asked to look at the floor with their ears in horizontal line to the shoulder joints, their knees directly below their hips and their wrists directly below the shoulders (Norris, 1999). A small pillow was placed under their ankles (Richardson and Jull, 1995). For the wall support standing position, participants were asked to stand with their backs against the wall while their hips were slightly flexed and their knees were

Fig. 1. Location for attaching surface electrodes to the abdominal wall. (A1 ¼ Paired electrode of the rectus abdominis muscle, A2 ¼ Reference electrode of the rectus abdominis muscle, B1 ¼ Paired electrode of the external abdominal oblique, B2 ¼ Reference electrode of the external abdominal oblique, C1 ¼ Paired electrode of the transversus abdominis/internal abdominal oblique, and C2 ¼ Reference electrode of the transversus abdominis/internal abdominal oblique).

644

P. Chanthapetch et al. / Manual Therapy 14 (2009) 642–646

with a differential amplification gain of 375 and a common mode rejection ratio >110 dB. The data were converted from analogue to digital and simultaneously displayed on a personal computer monitor which was recording for subsequent analysis. 2.4. Data processing

3. Results

The raw surface EMG signals generated during both MVC and AH were analyzed using the root mean squared technique. The mean EMG activity over a 1-s period was calculated for both MVC and AH. The average was performed at the highest area for MVC while it was collected at a 2-s period prior to the end of the EMG activity for AH (Beith et al., 2001). The EMG activity during AH was normalized by the MVC for each muscle. 2.5. Statistical analysis Statistical analysis was performed using the SPSS version 13.0 for Windows. Based on analysis by one-sample Kolmogorov– Smirnov test which found that the EMG data were not normally distributed, the non-parametric statistical analyses were therefore used. Initially, the Friedman two-way analysis of variance (ANOVA) was performed to test for the differences in EMG activity due to the muscles or the starting positions. The significant difference level was set at p < 0.05. Where a significant difference emerged, a multiple comparison procedure with the Wilcoxon signed-ranks test was used to test which pairwise differences were significant. A Bonferroni adjusted alpha level was used to safeguard for the overall Type I error to be accepted as significant (Portney and Watkins, 2000). The percentage of participants who showed non-activation of the global muscles (RA or EO) and isolation of the local muscles (contraction of TrA/IO with non-activation of RA and EO) was calculated. Participants who could keep their RA, EO, or both unchanged from the baseline over the three trials of AH were categorized as the ‘always’ non-activation group. The participants who could keep neither their RA, EO, nor both unchanged at all three trials were categorized as the ‘never’ non-activation group. The participants who could sometimes keep their RA, EO, or both unchanged over the three trials were categorized as the ‘sometimes’ non-activation group. For the isolated activation of the local muscles, the participants were also classified into three categories. They were always, never, and sometimes activation groups. The same percentages of participants in each category of the nonactivation groups were also applied to each category of the isolated Table 1 Descriptive statistics of electromyographic activity of three abdominal muscles [percentage of maximal voluntary contraction (MVC)] during abdominal hollowing in four positions (N ¼ 32).

Crook lying

Prone lying

Four-point kneeling

Wall support standing

Muscles

RA EO TrA/IO RA EO TrA/IO RA EO TrA/IO RA EO TrA/IO

Table 1 presents the mean, minimum, maximum, and standard deviation of the EMG activity of three abdominal muscles during AH in four positions. 3.1. Comparison of EMG activity within starting positions The highest EMG activity was always found in TrA/IO with minimal EMG activity in EO and RA. Approximately 20–30 percent of MVC was demonstrated in TrA/IO while the associated EMG activity of EO and RA was less than 6.5 percent of MVC (Table 1, Fig. 2). The Friedman two-way ANOVA showed significant differences in the EMG activity of three abdominal muscles in all four starting positions (p < 0.001) (Table 2). To determine in each starting position which pairwise comparisons of the EMG activity of three abdominal muscles were significantly different, post hoc analysis was performed. The results showed that the EMG activity of all three abdominal muscles was significantly different from each other in all four starting positions (p < 0.001). 3.2. Comparison of EMG activity within muscles The TrA/IO EMG activity was highest in the prone lying position (Fig. 2). Only the TrA/IO showed significant difference in mean EMG activity among four different starting positions (p < 0.001) (Table 3). The EO EMG activity, however, approached significance (p ¼ 0.053). For TrA/IO, post hoc analysis showed significant difference only between the prone lying and four-point kneeling positions (p < 0.001). 3.3. Non-activation and isolation of abdominal muscle in four starting positions In all four positions, more participants could reduce RA EMG activity than EO EMG activity (Fig. 3A and B). Forty percent or more of participants could sometimes perform AH with no contribution from RA. By contrast, 75 percent or more of participants could never perform AH without contribution from EO (Fig. 3B). During AH, the number of participants who could activate TrA/IO in isolation from RA and EO was similar across all four positions

60 RA

Abdominal muscle activity (% MVC) Minimum

Mean (SD)

Maximum

0.00 0.00 4.96 0.00 0.00 4.60 0.00 0.00 3.94 0.00 0.11 5.91

1.84 4.82 26.21 1.35 6.09 27.59 1.35 4.52 18.75 2.09 6.28 20.89

16.67 34.57 84.00 4.67 35.65 69.60 6.67 29.17 77.36 13.88 24.54 82.60

(3.16) (6.78) (22.86) (1.49) (6.87) (19.22) (1.93) (6.01) (16.68) (3.40) (5.58) (16.01)

RA ¼ Rectus abdominis, EO ¼ External abdominal oblique, TrA/IO ¼ Transversus abdominis/internal abdominal oblique.

EO

TrA/IO

50

MVC

Position

activation groups. This was because all participants were required to activate their local muscles while trying to keep their global muscles non-activated during AH. The non-activation of the global muscles would in turn reflect the isolated activation of the local muscles.

40 30 20 10 0

CR

PR

FO

WA

Fig. 2. Mean and standard deviation of electromyographic activity of three abdominal muscles during abdominal hollowing in four positions. RA, EO, and TrA/IO represented rectus abdominis, external abdominal oblique, and transversus abdominis/internal abdominal oblique, respectively. (CR, PR, FO, and WA represented crook lying, prone lying, four-point kneeling, and wall support standing positions, respectively).

P. Chanthapetch et al. / Manual Therapy 14 (2009) 642–646

Testing conditions

p-value

Crook lying Prone lying Four-point kneeling Wall support standing