Manual Therapy Journal - Volume 9, Issue 2, Pages 59-120 (May 2004)

VOLUME 9 NUMBER 2 PAGES 59– 122 MAY 2004 Editors International Advisory Board Ann Moore PhD, GradDipPhys, FCSP, CertE...

Author: Editors: Ann Moore and Gwen Jull

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VOLUME 9 NUMBER 2 PAGES 59– 122 MAY 2004

Editors

International Advisory Board

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

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

Gwendolen Jull PhD, MPhty, Grad Dip ManTher, FACP Department of Physiotherapy University of Queensland Brisbane QLD 4072, Australia Editorial Committee Karen Beeton MPhty, BSc(Hons), MCSP MACP ex o⁄cio member Department of Allied Health Professions—Physiotherapy University of Hertfordshire College Lane Hat¢eld AL10 9AB, UK Je¡rey D. Boyling MSc, BPhty, GradDipAdvManTher, MAPA, MCSP, MErgS Je¡rey Boyling Associates Broadway Chambers Hammersmith Broadway London W6 7AF, UK Darren A. Rivett PhD, MAppSc (ManiPhty) GradDip ManipTher, BAppSc (Phty) Discipline of Physiotherapy Faculty of Health The University of Newcastle Callaghan, NSW 2308, Australia Kevin P. Singer PhD Centre for Musculoskeletal Studies Department of Surgery The University of Western Australia, Royal Perth Hospital Level 2, MRF Building, 50 rear, Murray Street Perth,WA 6000, Australia Raymond Swinkels MSc, PT, MT (Book Review editor and NVMTex o⁄cio member) Ulenpas 80 5655 JD Eindoven The Netherlands

Visit the journal website at http://www.elsevierhealth.com/journals/math doi: 10.1016/S1356-689X (04)00012-8

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Manual Therapy 9 (2004) 59

www.elsevier.com/locate/math

Editorial

Clinical anatomy serving manual therapy Manual therapy primarily involves the application, by hand, of forces intended to move joints and surrounding tissues, in an effort to improve function and relieve symptoms, such as pain. Fundamental to understanding theories on how manual therapy might work is a thorough knowledge of the anatomy and biomechanics of the structures treated. This same knowledge is also crucial to understanding limitations of theories, and appreciating why they might be incorrect. Clinical anatomy can be an ambiguous term because it can mean different things to different people. In textbooks of anatomy it can mean little more than a short paragraph at the end of a chapter or section, which describes one or two clinical applications of the material just covered by the text. To some teachers clinical anatomy means ensuring that the material taught appears to have some clinical relevance. What is frustrating for manual therapists is that these clinical applications are typically directed at surgical or medical practice. A more demanding yet relevant definition of clinical anatomy can be formulated. It is the application, both in research and in teaching, of the discipline and scientific principles of anatomy to the comprehension and solution of problems that occur in clinical practice. This definition requires the clinical anatomist not only to be trained and well versed in the skills of anatomy but also to be thoroughly familiar with the problems that arise in clinical practice. In the context of manual therapy, the clinical anatomist should not only know, in detail, the structure and biomechanics of the neuromusculoskeletal system but also must be aware of what manual therapists believe they are doing when assessing patients and applying treatment, as well as the various theories that underlie this treatment. This definition does not require that the anatomist has consummate clinical competence in how to execute the treatment, but they must have more than a superficial insight into the nature of that treatment and its purported biological basis. Unencumbered by patient loads and other demands of clinical practice, the clinical anatomist can afford the time to reflect on the alleged basis of various interventions. They can serve clinicians by providing insightful analyses that practitioners themselves cannot produce, either for lack of time, or for lack of knowledge and skills to analyze anatomy and biomechanics in detail. The value of this service to practitioners is that from clinical anatomists, they can learn the errors and limitations of the traditional literature upon which 1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2003.12.001

clinical practice has often been based, and thereby avoid becoming victims (and perhaps unwitting promulgators) of misperceptions and misrepresentations of biological facts. This serves to ensure a high intellectual level of clinical practice. Such clinical anatomy relevant to manual therapy practice has been published over the last 30 years. Until the 1980s the anatomical basis for pain arising from the lumbar or cervical disc had not been established. Strange as it seems now, until these simple contributions were made it was common belief that the intervertebral disc could not be a source of pain. In the mid-1980s a complete revision of the anatomy of the erector spinae and multifidus was made, revolutionising the development of clinical and biomechanical models of trunk function. Textbooks of anatomy would have us believe that cervical and lumbar spine intervertebral discs are the same and clinical models were developed along these lines. However, clinical anatomical studies have shown that this is not the case. These same textbooks still deny that the zygapophysial joints are innervated but clinical anatomical studies have demonstrated their innervation which has lead to successful diagnosis and treatment of zygapophysial joint pain. The anatomy of the abdominal wall is often taught from the perspective of general surgery by traditional anatomists not aware of the current importance of the abdominal muscles in the context of lumbar spine stabilization and interventions for back pain. Indeed recent research of the clinical anatomy of the trunk and pelvic musculature highlights the problems of applying this traditional or textbook anatomy to the biological basis of current clinical practice. Clinical anatomy is not an unchanging collection of facts but an evolving field of science. The unique insight it can offer serves manual therapy by challenging and advancing clinical practices and providing biological evidence to support their application.

Susan R. Mercer Department of Anatomy and Structural Biology, University of Otago, Lindo Ferguson Building, PO Box 913, Dunedin, Otago, New Zealand E-mail address: [email protected] Darren A. Rivett Discipline of Physiotherapy, University of Newcastle, Callaghan, Australia

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Masterclass

A proposed new classification system for whiplash associated disorders—implications for assessment and management Michele Sterling* Division of Physiotherapy, School of Health and Rehabilitation Sciences, The University of Queensland, St. Lucia 4072, Australia Received 9 December 2003; accepted 6 January 2004

Abstract The development of chronic symptoms following whiplash injury is common and contributes substantially to costs associated with this condition. The currently used Quebec Task Force classification system of whiplash associated disorders is primarily based on the severity of signs and symptoms following injury and its usefulness has been questioned. Recent evidence is emerging that demonstrates differences in physical and psychological impairments between individuals who recover from the injury and those who develop persistent pain and disability. Motor dysfunction, local cervical mechanical hyperalgesia and psychological distress are present soon after injury in all whiplash injured persons irrespective of recovery. In contrast those individuals who develop persistent moderate/severe pain and disability show a more complex picture, characterized by additional impairments of widespread sensory hypersensitivity indicative of underlying disturbances in central pain processing as well as acute posttraumatic stress reaction, with these changes present from soon after injury. Based on this heterogeneity a new classification system is proposed that takes into account measurable disturbances in motor, sensory and psychological dysfunction. The implications for the management of this condition are discussed. r 2004 Elsevier Ltd. All rights reserved.

1. Introduction Whiplash injuries from motor vehicle crashes, although common, remain a poorly understood clinical entity. Most individuals recover within a few weeks of injury but a significant proportion (14–42%) will develop persistent ongoing pain with 10% reporting constant severe pain (Barnsley et al., 1994). It is these people with persistent symptoms who contribute substantially to the significant economic costs related to this condition. The most optimal management of whiplash associated disorders (WAD) is unknown. Evidence provided from systematic reviews would suggest that active interventions that stimulate the patient to return to daily activities as soon as possible are preferable to rest and wearing of a collar (Magee et al., 2000; Scholten-Peeters et al., 2002). While trials of physical management have enhanced the rate of recovery of those who are likely to obtain a reasonable recovery after injury, no treatment has been shown to decrease the incidence of chronicity *Tel.: +61-7-3365-4569; fax: +61-7-3365-2775. E-mail address: [email protected] (M. Sterling). 1356-689X/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2004.01.006

associated with this condition (Borchgrevink et al., 1998; Rosenfeld et al., 2000, 2003). One reason for this may be that such treatments do not specifically target the physical and psychological impairments shown to be associated with WAD. Furthermore attempts to develop a classification system of WAD based on signs and symptoms (Spitzer et al., 1995), suffer similar flaws and this could explain the dubious value of the Quebec Task Force (QTF) classification of WAD (Kivioja et al., 1999). This paper will outline recent advances made in the understanding of the physical and psychological impairments associated with both the acute and chronic stages of this enigmatic condition. A new classification system that takes into account specific impairments will be proposed and the implications these findings provide for the future management of WAD will be discussed.

2. Quebec Task Force classification of WAD Symptoms reported following whiplash injury, particularly those whose condition fails to resolve, can be

ARTICLE IN PRESS M. Sterling / Manual Therapy 9 (2004) 60–70 Table 1 The Quebec Task Force classification of whiplash associated disorders QTF classification grade

Clinical presentation

0

No complaint about neck pain No physical signs

I

Neck complaint of pain, stiffness or tenderness only No physical signs

II

Neck complaint Musculoskeletal signs including: Decreased range of movement Point tenderness

III

Neck complaint Musculoskeletal signs Neurological signs including: Decreased or absent deep tendon reflexes Muscle weakness Sensory deficits

IV

Neck complaint and fracture or dislocation

diverse and may include neck pain, headache, dizziness, tingling, numbness, arm, thoracic and lumbar spine pain. The varied nature of symptoms reported following whiplash injury lends itself to suggest that a classification system of the condition would be useful in order to guide both research investigation and treatment decision-making. In 1995, the QTF developed the Quebec classification of WAD (Spitzer et al., 1995). The authors proposed this classification system (Table 1) in order to facilitate the evaluation of research and to provide clinicians with useful guidelines for making decisions about therapeutic management. It classified patients with whiplash according to the type and severity of signs and symptoms observed shortly after the injury (Spitzer et al., 1995). Since its release, the QTF classification has been criticized. Much of this criticism has identified that whilst the QTF review of WAD rejected many articles that did not meet rigorous scientific criteria, the guidelines themselves suffered from the same faults—they were adopted and promoted without scientific validation (Freeman et al., 1998; Teasell and Shapiro, 1998; Hartling et al., 2001). The potential usefulness by which such a classification may be judged are as predictors of the long-term outcome following whiplash injury. Kivioja et al.’s (1999) longitudinal study of 100 patients with WAD suggested that the application of the Quebec classification was of limited prognostic value. However, more recently Hartling et al. (2001) showed that the classification was prognostic of outcome at 6, 12, 18 and 24

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months postinjury but these authors recommended that a modification of Grade II classification be made to distinguish between those with normal or limited range of movement. The reason for this was that those with less range of movement had a poorer outcome. A major drawback of this study was that the classification of the WAD patients was made retrospectively using the patients’ clinical notes and therefore emphasizes the need for more prospective studies on outcome. Nevertheless, Hartling et al. (2001) may have a valid point when they suggest modification of the WAD II subgroup. WAD II, although exclusive of clinical findings of neurological deficit, still covers a very broad range of symptoms and as such, suggests variance in outcome will be a feature of such a broad classification. Furthermore, WAD II is the most common of the four QTF classifications of whiplash and it is important that it accurately represents the whiplash subgroup it is supposed to portray. While the QTF also recognize the shortcomings of their classification system, it was probably the best that could be developed at the time as knowledge about WAD was virtually limited to patient reported signs and symptoms. This situation is being slowly reversed and in recent years wide ranging physical and psychological impairments and the involvement of complex physiological mechanisms have been demonstrated to occur in chronic WAD (Radanov and Sturzenegger, 1996; Dall’Alba et al., 2001; Peebles et al., 2001; Nederhand et al., 2002; Sterling et al., 2002). These findings lay the foundation for future development of an improved classification system.

3. Physical and psychological features of chronic WAD Early investigation of whiplash injury sought to determine the pathoanatomical structures involved. In vivo identification of structural pathology has proved difficult due to the insensitivity of current radiological diagnostic imaging techniques including conventional radiology, magnetic resonance imaging (MRI) and computed tomography scanning (CT) (Davis et al., 1991; Pettersson et al., 1994; Uhrenholt et al., 2002), although recent studies begin to provide hope that this situation may change in the future for at least some structures (Krakenes et al., 2002, 2003). Nevertheless, in vitro evidence from cadaveric and animal studies indicates that lesions may occur to virtually any cervical structure including bony elements, intervertebral discs and zygapophyseal joints, ligaments, muscles and nerve tissues (Schonstrom et al., 1993; Jonsson et al., 1994; Taylor and Taylor, 1996). It has been argued that the identification of the pathoanatomical source of symptoms provides little basis for appropriate management of musculoskeletal pain and emphasis should

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M. Sterling / Manual Therapy 9 (2004) 60–70

be directed toward a treatment approach directed toward mechanisms and processes underlying the condition (Woolf and Decosterd, 1999; Jensen and Baron, 2003). In keeping with this argument, chronic WAD have been shown to be characterized by disturbances in the motor and sensory systems as well as psychological distress. Motor system changes observed include reduced active cervical spine movements and altered patterns of muscle recruitment within the cervical spine and upper quadrant (Bono et al., 2000; Jull, 2000; Nederhand et al., 2000; Dall’Alba et al., 2001; Elert et al., 2001; Nederhand et al., 2002). Disturbances in postural control mechanisms such as deficits in kinaesthetic awareness, balance and eye movement control have also been identified (Alund et al., 1993; Tjell and Rosenhall 1998; Treleaven et al., 2003). Other studies have demonstrated findings that suggest chronic whiplash subjects show alterations in the neurobiological processing of pain mechanisms most likely occurring within the central nervous system. Generalized hypersensitive responses both local (in the cervical spine) and remote to the site of injury have been demonstrated to a variety of stimuli including induced experimental pain (Koelbaek-Johansen et al., 1999), electro-cutaneous stimulation (Sheather-Reid and Cohen, 1998; Curatolo et al., 2001) and mechanical stimulation (Moog et al., 2002; Sterling et al., 2002). Perhaps not surprisingly, those with chronic WAD also show evidence of psychological distress, which has been proposed to occur as a consequence of persisting symptoms (Radanov et al., 1996; Peeters et al., 2001).

4. The development of physical and psychological impairments following whiplash injury This improved understanding of chronic WAD began to demonstrate further inadequacies of the QTF classification system. That is, the QTF classification system takes no account of the presence of both physical and psychological impairments as outlined above. However improvement of the classification system can really only be made when there is greater understanding of these impairments in the acute stage of whiplash injury and their role in the transition to either recovery or symptom persistence. This will allow the classification system to be used for treatment decision making and prognostic indication. In contrast to the explosion of knowledge of mechanisms involved in chronic WAD, features detected and documented in acute WAD were limited to the presence of decreased active range of neck movement and local mechanical hyperalgesia within the cervical spine (Gargan et al., 1997; Kasch et al., 2001a, b).

Psychological responses appeared to be within normal ranges soon after the accident with the psychological distress seen later proposed to be as a consequence of ongoing pain and disability (Radanov et al., 1996; Gargan et al., 1997). In order to better understand the whiplash condition from the time of injury until the patient either recovered or developed persistent symptoms, a prospective longitudinal study was conducted in The Whiplash and Cervical Spine Research Unit, The University of Queensland. This study followed 76 whiplash patients from a few weeks after injury until six months post injury. It measured a wide range of physical and psychological factors (Sterling et al., 2003a–c, 2004). The assessment of physical factors in this study included measures of motor function (range of neck movement, neck kinaesthetic awareness (joint position error—JPE) and cervical flexor muscle recruitment patterns during the cranio-cervical flexion test); sensory function (pressure, heat and cold pain thresholds) as well as sympathetic nervous system activity via the sympathetic vasoconstrictor response (SVR) (Schurmann et al., 1999). The study also utilized questionnaires measuring psychological distress (GHQ-28, mental health components of the SF-36), the patient’s fear of movement due to the injury (Tampa scale of kinesiphobia—TSK (Kori et al., 1990)) and acute posttraumatic stress as a consequence of the accident (Impact of Events Scale—IES (Horowitz et al., 1979)). In order to investigate the differences in processes involved between those who recovered and those who reported persistent symptoms based on their status at 6 months post injury, the subjects were classified at this latter time point into one of three groups using the Neck Disability Index (NDI) (Vernon, 1996). The three groups were: those patients who fully recovered (38%), those with residual milder symptoms (39%) and those with persistent moderate/ severe symptoms (23%) (Table 2). The groups were compared for differences on the physical and psychological measures. The majority of the 76 participants (93.4%) who completed the study could be classified as WAD II, 2.4% were WAD I and 4.2% were WAD III as per the QTF classification (Spitzer et al., 1995). All of the WAD I participants were part of the group who recovered by 6 months and all WAD III participants were part of the group who continued to report moderate/severe symptoms (Table 2). All three groups contained participants who could be defined as WAD II. It was not the aim of the study to investigate the effect of treatment. Subjects were free to pursue any form of treatment. The types and numbers of treatments received (including medication) were not different between the three whiplash groups.

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Table 2 The age, gender and classification of subject groups at 6 months according to the NDI scores (Vernon, 1996) Group

Recovered group Mild pain and disability group Moderate/severe pain and disability group Control group

Number

Age (years) (mean7SD)

Gender % female

NDI classification

NDI (mean7SD)

QTF classification %I

%II 93.1 100

0 0

82.4

17.6

29 30

29.3711.72 34.3712.5

50 77

o8 10–28

2.972.9 16.575.6

6.9 0

17

43.7714.5

94

>30

42.8712.2

0

20

40.1713.6

60

—

—

%III

The percentage of subjects for each group that fitted the QTF classification is also shown.

5. Changes in motor function Decreased cervical range of movement was present in all three whiplash groups within a month of injury. Range of movement improved within 2–3 months in those who recovered and those who continued to report milder symptoms at 6 months. In contrast loss of cervical range of movement persisted in those participants with persistent moderate/severe symptoms at 6 months post injury (Sterling et al., 2003b). (Fig. 1 depicts range of cervical extension throughout the study period. Other movement directions showed a similar picture). Whilst decreased cervical range of movement had been demonstrated previously in acute WAD (Kasch et al., 2001a), these authors reported that restoration of movement loss had occurred by three months post injury. However the recovered participants were not differentiated from those with persistent symptoms. It would appear that such differentiation is important. Altered patterns of cervical muscle recruitment were also apparent in all whiplash groups within a month of injury. This was exemplified in this study by increased activity in the superficial neck flexor muscles at the lower stages of the cranio-cervical flexion test (Fig. 2) (Sterling et al., 2003b). Interestingly, the altered muscle recruitment patterns persisted to 6 months in all the whiplash patients, even in those patients who reported full recovery. Research into low back pain has also shown that some muscle changes persisted despite the patient reporting recovery and may be one factor involved in the high rate of symptom recurrence associated with this condition (Hides et al., 2001). Whether the whiplash patients who recovered in this study continue to demonstrate increased muscle activity past the 6-month period and whether this persistence of muscle dysfunction has any relationship to recurrence of pain at some later date requires further investigation and will be assessed at a 2 year follow-up. In addition to altered patterns of cervical muscle recruitment, changes have also been demonstrated in the shoulder girdle muscles. Nederhand et al. (2003) showed

Fig. 1. Mean (SEM) for whiplash groups (recovered, mild pain and disability, moderate/severe pain and disability) and controls at o1 month, 2, 3 and 6 months postinjury for active extension.

Fig. 2. Normalized EMG (mean and standard deviation) of the superficial neck flexors at the lower stages of the cranio-cervical flexion test for three whiplash groups (recovered, mild pain and disability, moderate/severe pain and disability) and the control group.

reorganization of muscle activation patterns of the upper trapezius during functional tasks that occurred soon after injury and persisted to 24 weeks postinjury. Kinaesthetic disturbances, in this case greater joint repositioning errors, also occurred soon after injury. Whilst differences were statistically significant only in those with moderate/severe symptoms, participants with less severe symptoms and those who recovered also tended toward higher joint repositioning errors when

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compared to asymptomatic subjects (Sterling et al., 2003b). These kinaesthetic disturbances were present within a month of injury, showed no change over time and persisted until 6 months postinjury. These results support previous research where chronic WAD participants with a higher neck disability index (in this case the Northwick Park questionnaire) demonstrated greater JPE (Treleaven et al., 2003). Impaired postural control as manifested by greater errors in joint positioning may be one reason for the frequently reported symptoms of dizziness and unsteadiness reported by some with chronic WAD (Heikkila and Astrom, 1996; Treleaven et al., 2003). In keeping with this proposal, it is of interest to note that a much higher proportion (42%) of those with persistent moderate/severe symptoms reported dizziness or unsteadiness when compared to recovered participants (7%) and those with residual mild pain and disability (7%). In summary, longitudinal data has demonstrated that whiplash injury induces disturbances in motor function that are present soon after the accident. While these motor disturbances are greater in those reporting greater levels of pain and disability, they are also apparent in those with lesser symptoms and even in those who recover from the injury. It has been suggested that beliefs about the fear of movement and/or reinjury play a role in the motor system changes seen in WAD (Nederhand et al., 2002). The motor changes seen in our study were shown to occur independently of such psychological factors and as such may represent alterations in underlying physiological processes as a consequence of pain and injury (Sterling et al., 2003b).

6. Development of sensory changes In the acute stage of whiplash injury, local mechanical hyperalgesia (decreased pressure pain thresholds) has been shown to be present within the cervical spine

irrespective of symptom intensity (Kasch et al., 2001b; Sterner et al., 2001; Sterling et al., 2003a). Local mechanical hyperalgesia tended to resolve over time (2–3 months) in those who recover or report continuing milder symptoms but persisted unchanged in whiplash patients reporting persistent symptoms of a moderate/ severe nature (Sterling et al., 2003a). More widespread sensory hypersensitivity is recognized as a feature of chronic WAD (Koelbaek-Johansen et al., 1999; Curatolo et al., 2001; Sterling et al., 2002). The existence of this phenomenon in the earlier stages of the condition has been disputed (Kasch et al., 2001b). It is now clear that this hypersensitivity, including widespread mechanical and thermal hyperalgesia as well as heightened responses to the Brachial Plexus Provocation Test (BPPT), is present soon after injury in whiplash patients who develop persistent moderate/severe symptoms (Fig. 3) (Sterling et al., 2003a). Furthermore such sensory changes persist unchanged into the chronic phase of the condition. Sensory hypersensitivity does not appear to be a feature of those with persistent milder symptoms or those who recover from the injury, at any stage of the condition (Sterling et al., 2003a). The sub-group of whiplash patients who develop persistent moderate/severe symptoms showed additional changes in sensory function including cold hyperalgesia and, in some cases, altered peripheral vasoconstrictor responses indicative of sympathetic nervous system function. These findings suggest that a neuropathic component to these patients’ pain syndrome cannot be ruled out and this adds to the complexity of their condition (Sterling et al., 2003a). It is recognized that measures of pain threshold responses may be influenced by the patients’ levels of psychological distress (Rhudy and Meagher, 2000). We were able to show that the sensory changes demonstrated in this study occurred independently of psychological distress and for this reason the presence of generalized sensory hypersensitivity may be explained

Fig. 3. Cold and heat pain thresholds of the cervical spine, PPT of remote site (Tibialis Anterior) and elbow extension with BPPT in whiplash groups (recovered, mild pain and disability, moderate/severe pain and disability) at o1 month, 2, 3 and 6 months postinjury.


by the involvement of changes within central pain processing mechanisms (Sterling et al., 2003a).

7. Development of psychological changes Psychological stress, affective disturbances, anxiety, depression and behavioural abnormalities have been found in patients with chronic WAD (Peebles et al., 2001; Wenzel et al., 2002). It is generally thought that the psychological distress seen in the chronic stage of the condition is most likely as a result of ongoing pain and disability (Radanov et al., 1995; Gargan et al., 1997). Whilst psychological factors are believed to play a role in the transition from acute to chronic spinal pain (Linton, 2000), this has not been well investigated in WAD. Our recent longitudinal investigation of whiplash injury demonstrated that all whiplash groups displayed initial (within a month of injury) psychological distress to some extent. All whiplash patients, regardless of their recovery rate, showed lower scores on the mental health components of SF-36 when compared to Australian population norms and above or close to threshold scores on the GHQ-28 questionnaire (Sterling et al., 2003c). In addition the whiplash groups who reported persistent symptoms at 6 months (either milder or moderate/severe symptoms) also showed higher scores on the TSK indicating elevated fears of movement and reinjury. The psychological distress of those who eventually recovered by six months postinjury and those with lesser symptoms at this time point decreased to normal levels and appeared to parallel decreasing levels of pain and disability. Psychological distress and elevated levels of fear of movement/reinjury continued in those with persistent moderate/severe symptoms but this group of patients also showed a unique psychological reaction. They could be distinguished from the other groups by the early presence of moderate levels of acute posttraumatic stress that did not resolve over the study period. This acute stress response was not a feature of whiplash participants with a better outcome or full recovery at 6 months.

8. A proposed new classification system for acute WAD The findings of this prospective longitudinal study, that the continuum of WAD involves a complex array of physiological and psychological mechanisms, has revealed the limitation of the QTF’s symptom-based classification of the condition. The QTF’s WAD II classification essentially covers all patients who report neck pain following a motor vehicle crash and who show some physical impairment such as cervical movement loss and/or the presence of tender points (Spitzer et al.,

65

1995). The results of this prospective longitudinal study demonstrated the heterogeneity of those individuals classifiable as WAD II (the majority of participants in this study) in terms of the varying extents of physical impairments. Furthermore, the QTF’s classification takes no account of psychological disturbances. It is apparent that psychological distress, especially acute posttraumatic stress reactions are important factors, particularly in those with persistent moderate/severe symptoms. The outcome of the participants in this study who were classifiable as WAD II varied enormously, ranging from full recovery at 6 months post injury to reporting continued moderate/severe symptoms. This high variability in outcome within the same classification group would be an explanation for the poor predictive capacity of the QTF’s classification system (Kivioja et al., 1999; Hartling et al., 2001). Reclassification of WAD, particularly WAD II is urgent. This category should be reclassified based on measurable disturbances in motor, sensory and psychological function. A preliminary proposal for an alternative classification system built onto the QTF classification is outlined in Table 3.

9. Implications for the assessment of the whiplash injured patient The presence of physical impairments and psychological disturbances was not uniform in all the whiplash participants and demonstrates the heterogeneity of WAD at both the acute and chronic stages of the condition. It is evident from the data that more in depth evaluation of both physical and psychological factors and potential underlying processes is required with examination of each individual whiplash injured patient’s condition. Conventional clinical tests of the cervical spine such as manual palpation and visual inspection of range of movement lack reliability or validity (Fjellner et al., 1999; Smedmark et al., 2000). The clinical evaluation of pain syndromes (including neck pain and whiplash) currently involves the identification or diagnosis of the primary patho-anatomical structure that is considered responsible for producing the pain. Sensory examination such as that required to detect the sensory disturbances seen in this study is rarely performed and if it is performed is usually limited to rudimentary assessment of muscle power, deep tendon reflexes and light touch sensation. Similarly, examination of motor function is usually limited to a visual estimate of cervical range of movement. In the context of whiplash where patients often perceive scepticism directed toward their reported symptoms, identification of the anatomical structure involved might reassure both the clinician and the patient. However it does little to provide understanding


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Table 3 Proposed new classification system for acute whiplash associated disorders (WAD) Proposed classification grade

Physical and psychological impairments present

WAD 0

No complaint about neck pain No physical signs

WAD I

Neck complaint of pain, stiffness or tenderness only No physical signs

WAD IIA

Neck pain Motor Impairment Decreased ROM Altered muscle recruitment patterns (CCFT) Sensory Impairment Local cervical mechanical hyperalgesia

WAD II B

Neck pain Motor Impairment Decreased ROM Altered muscle recruitment patterns (CCFT) Sensory Impairment Local cervical mechanical hyperalgesia Psychological impairment Elevated psychological distress (GHQ-28, TAMPA)

WAD II C

Neck pain Motor Impairment Decreased ROM Altered muscle recruitment patterns (CCFT) Increased JPE Sensory Impairment Local cervical mechanical hyperalgesia Generalised sensory hypersensitivity (mechanical, thermal, BPPT) Some may show SNS disturbances Psychological Impairment Psychological distress (GHQ-28, TAMPA) Elevated levels of acute posttraumatic stress (IES)

WAD III

Neck pain Motor Impairment Decreased ROM Altered muscle recruitment patterns (CCFT) Increased JPE Sensory Impairment Local cervical mechanical hyperalgesia Generalised sensory hypersensitivity (mechanical, thermal, BPPT) Some may show SNS disturbances Psychological Impairment Psychological distress (GHQ-28, TAMPA) Elevated levels of acute posttraumatic stress (IES) Neurological signs of conduction loss including: Decreased or absent deep tendon reflexes Muscle weakness Sensory deficits

WAD IV

Fracture or dislocation

of the underlying processes involved in the perpetuation of symptoms that may be amenable to treatment. Recent calls have been made to direct clinical examination toward the recognition and identification of mechanisms involved in the patient’s pain syndrome (Woolf and Decosterd, 1999; Max, 2000; Treede et al., 2002). It is apparent that the assessment of motor dysfunction in the whiplash injured patient will need to be extended to include assessment of cervical muscle recruitment patterns and kinaesthetic deficits. Clinically this can be achieved with specific muscle tests such as the cranio-cervical flexion test (Jull et al., 2004) (Fig. 4) and simple measures of joint repositioning error. Disturbances in activity of the upper trapezius muscle during functional tasks have also been demonstrated in acute WAD (Nederhand et al., 2003). This suggests that assessment of scapulo-cervical muscle function may also be useful. It is likely that other motor dysfunction will also be present following acute whiplash injury, such as: poor muscle control in posture, loss of muscle strength and endurance, balance disturbances and impaired eye movement control. Such motor and postural control impairments have been demonstrated in chronic WAD (Falla et al., 2004; Treleaven et al., 2004) and need to be investigated in the assessment of the acute whiplash patient. More detailed assessment of sensory changes will also be necessary. The first stage of this assessment would be thorough recording of the patient’s symptoms including

Fig. 4. Measurement of cervical muscle recruitment patterns using the cranio-cervical flexion test (Jull et al. 2003).


the nature of the pain. Although the usefulness of symptom classification as a way of clarifying pain mechanisms is debatable, it is a necessary part of the patient’s assessment (Jensen and Baron, 2003). Quantitative sensory testing can also be utilized. This could include the measurement of mechanical pain thresholds with pressure algometry (Fig. 5), determination of the presence of allodynia with light tactile stimulation. Thermal sensitivity can also be examined with thermorollers set at predetermined temperatures (Jensen and Baron, 2003). However, it should be noted that whilst such sensory assessments can provide useful information, at present there is no consensus about the most appropriate method to use and what to compare findings with (Jensen and Baron, 2003). The development of the most appropriate sensory examination of whiplash injured patients is at an early stage and moves toward further development into clinically valid and useful measures is of vital importance. While the assessment of physical impairments has been emphasized, recognition of psychological impairments must not be overlooked. This would be best achieved using validated questionnaires that encompass a broad overview of psychological distress. The results

Fig. 5. Measurement of mechanical hyperalgesia using pressure algometry.

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of the longitudinal study demonstrated that the presence of an acute posttraumatic stress reaction plays an important role in the development of persistent symptoms following whiplash injury (Sterling et al., 2003c). Physiotherapists should be alert to the presence of psychological distress, particularly acute posttraumatic stress reaction and institute early psychological referral.

10. Implications for the early management of WAD The results of this study have demonstrated that changes in motor function, sensory disturbance and psychological distress occur very soon after the occurrence of injury. In those patients who report moderate/ severe pain and disability that fails to resolve, these early disturbances remain unchanged through transition to symptom persistence. This finding is particularly important for those whose symptoms fail to resolve as it suggests that the window of opportunity to provide specific impairment based treatments should occur early post injury. Although speculative at present, it has been suggested that expeditious treatment may help to prevent transition from acute pain into persistent pain (Cousins, 2002). The proposal of the prevention of chronic pain has thus far been mainly confined to behavioural approaches to management (Cousins, 2002; Ferrari, 2002). It is apparent from the findings of this study that its application should extend to include treatment directed toward disturbances of both motor and sensory impairments. Certainly, this approach is likely to be more beneficial than the current situation where ad hoc treatments are usually prescribed for WAD. The knowledge of underlying processes in the acute stage of injury will not only benefit those whose moderate/severe symptoms are unlikely to resolve. Whiplash patients who continue to report residual mild symptoms show resolution of local sensory disturbances, cervical movement loss and psychological distress. However, some motor dysfunction remains in the form of altered patterns of movement with the cranio-cervical flexion test. It is likely that addressing these residual motor changes by a specific tailored exercise programme may facilitate these patients to full recovery. Although yet to investigated in WAD, the efficacy of such a programme has been demonstrated in idiopathic neck pain (Jull et al., 2002). In addition, the participants in our study who recovered fully also showed residual motor dysfunction. Whilst the significance of these persistent motor deficits in whiplash injured patients is unknown at this stage, findings from research of low back pain (Hides et al., 1996) would suggest that a recurrence of symptoms in these patients at some later date is possible. This suggests that the institution of early specific motor retraining may be optimal for these patients.

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In contrast those persons with persistent moderate/ severe symptoms showed a much more complex picture. Whilst these patients did indeed show similar persistent motor dysfunction, their clinical picture was complicated by the presence of widespread sensory hypersensitivity and acute posttraumatic stress reaction. These patients may be benefited more from an early multiprofessional approach to their management. Based on the findings of this study, such a treatment approach may need to involve physical rehabilitation, psychological support and pharmaceutical management. In view of the sensory disturbances seen in this whiplash group, it is apparent that any physical treatment performed be non pain provocative in nature. It is usually the norm that multiprofessional management of whiplash is not commenced until it is clear symptoms are not resolving, often up to months following injury. The physical and psychological changes that occurred following whiplash injury were apparent within a few weeks of injury. This would suggest that multiprofessional management must be commenced early (within weeks of injury) in those at risk of developing persistent pain and disability. In comparison, those who report residual mild symptoms did not demonstrate such extensive impairments. In this group, both local mechanical hyperalgesia and psychological distress resolved by 2–3 months postinjury. The only physical impairment seen to persist in this group was that of altered muscle recruitment patterns with the cranio-cervical flexion test. This implies that minimalist intervention comprising active exercise and specific rehabilitation of cervico-brachial control may be indicated for these patients.

11. Conclusion Whiplash is a complex multifaceted disorder involving varying degrees of both physical and psychological disturbance. A new classification system has been proposed which reflects the complexity of the condition and is inclusive of identified specific impairments. As a consequence of differences in processes between recovered patients and those who develop chronic pain, treatments will vary according to the presence or not of specific physical and psychological impairments. Physiotherapists play a pivotal role in the comprehensive assessment of whiplash injured patients, providing appropriate interventions and in the liaison with other health professionals.

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Review Article

The sensory and sympathetic nerve supply within the cervical spine: review of recent observations Gillian M. Johnson* Otago School of Physiotherapy, University of Otago, P.O. Box 56, Dunedin, New Zealand Received 16 December 2002; received in revised form 7 July 2003; accepted 22 July 2003

Abstract The purpose of this review is to identify recently observed features of the sympathetic and sensory systems and their pathways which characterize cervical spine innervation and their potential relevance to the clinical pain syndromes. The results of studies examining the innervation patterns of the zygoapophysial joints serve to demonstrate that structures in the cervical spine, as in other spinal regions, are partly innervated by sensory nerves traveling along sympathetic pathways. These studies also demonstrate that the neuropeptide levels in the cell bodies located within the dorsal root ganglion of these sensory nerves fluctuate according to the physiological state of the zygoapophysial joint. Additional to the sympathetic nerves accompanying the vertebral artery, the innervation patterns of dura and posterior longitudinal ligament in the upper cervical spine are distinctive features of cervical spine innervation. The possible clinical implications of cervical innervation patterns are considered with reference to referred pain, the pain patterns associated with a dissecting vertebral artery and cervicogenic headaches. r 2003 Elsevier Ltd. All rights reserved. Keywords: Cervical spine; Sensory nerves; Sympathetic nerves

1. Introduction In the cervical spine, and in keeping with the thoracic and lumbar spines, the single outstanding feature of innervation is the combined contribution of peripheral spinal nerves and the autonomic nervous system (Stilwell, 1956; Mulligan, 1957). There is a long-held index of suspicion amongst clinicians and scientists that the sympathetic nervous system is responsible for the generation of some of the more puzzling aspects of cervical pain. In the past, discussion has been directed towards the possibility that the thoracolumbar outflow of the sympathetic nervous system which emanate from cell bodies in the lateral gray columns of the spinal cord, could extend rostrally into the cervical spine (Hirsch and Zottermann, 1971). Conversely, in order to explain pain referral mechanisms of the head and neck, it was speculated that some of the sensory nerves supplying structures such as the intervertebral joints bypassed the normal route and instead, traveled along sympathetic *Tel.: 63-3-479-5424; fax: 64-3-479-8414. E-mail address: [email protected] (G.M. Johnson). 1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1356-689X(03)00093-6

pathways (Wall, 1971). More recently, there has been increasing debate as to the possible effects of manual therapy on the function of the sympathetic nervous system and the associated changes in autonomic activity and pain relief. Much of the focus in this latter discussion has been directed towards the descending inhibitory influences of the sympathetic nervous system on the spinal cord in order to explain the immediacy of effect observed with manipulation-induced analgesia (Wright, 1995). Fundamental in the current understanding of cervical spine and pain referral mechanisms is recognition of the overlap between trigeminal and upper cervical afferents throughout the trigeminocervical complex from the caudal trigeminal nucleus to the upper cervical segments (Kerr, 1972; Abrahams et al., 1979; Sessle et al., 1986; Pfaller and Arvidsson, 1988). However this feature does not fully explain all the pain patterns experienced in cervical spine dysfunction. The need in such discussion is to also consider the origins and pathways of the sympathetic and somatic nervous system associated with the cervical spine in the light of new observations. The purpose of this review is to identify recently observed

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features of the sympathetic and sensory systems and their pathways which characterize cervical spine innervation. Reference is made to aspects of lumbar spine innervation and gross anatomical aspects of innervation where they serve to complement upon immunohistochemistry observations made in the cervical spine. Advances in immunocytochemistry and neurotracers provide new evidence of functional links between primary afferent and sympathetic fibres in the peripheral nervous system. It is now possible using such methods to specify sensory nerves innervating key spinal structures such as the zygoapophysial (ZA) joints, and to determine the extent to which they access sympathetic nervous system pathways. Antibodies to the neuropeptides substance P (SP), and calcitonin gene related peptide (CGRP) are frequently used as sensory markers. They are of particular interest to clinicians due to their presence in nociceptor unmyelinated (C type) and myelinated (A–d type) fibres (Lee et al., 1985). Antibodies against tyrosine hydroxylase (TH) the ratelimiting enzyme in catecholamine synthesis, and neuropeptide Y (NPY), (a neuropeptide co-existing with noradrenaline) identify sympathetic nerve fibres (Ahmed et al., 1993). Caution is needed when interpreting the findings in the literature with regard to antibodies and neurotracers used to locate sensory fibres since their presence does not provide unequivocal evidence of actual nociceptive function. For example, in addition to that of nociception, both SP and CGRP have a role in the plasma extravasation and vasodilatation events contributing to neurogenic inflammation (Brain and Willliams, 1985). Likewise neurotracers do not necessarily define nociceptive pathways as some substances travel selectively along myelinated fibres of different calibers. Whereas the retrograde neurotracer fluorogold is highly sensitive to all nerve fibres, other substances such as cholera toxin B are transported along large and medium-caliber axons. Wheatgerm agglutinin-horseradish peroxidase is taken up by small-caliber pain transmitting (A–d type) fibres (Robertson and Arvidsson, 1985; Fried et al., 1991).

2. Features of cervical spine innervation Details of the gross anatomical nerve supply and its clinically pertinent topographical features are now well established (Bogduk, 1982; Bogduk and Marsland, 1988). A clinically useful model for the consideration of spinal innervation is to assign the vertebral structures into ventral and dorsal compartments based on their location with respect to a virtual frontal plane taken through the dorsal wall of the intervertebral foramen (Groen and Stolker, 2000).

The ventral compartment of the cervical spine incorporates the vertebral bodies, anterior and posterior longitudinal ligaments, intervertebral disc, uncovertebral joints and dura mater. Three discrete sources of innervation to these structures have been identified: direct branches from the sympathetic trunk, branches of the sympathetic rami communicantes and the perivascular nerve plexuses associated with the vertebral arteries (Groen et al., 1990). As a result of this arrangement two major interconnected networks running within the anterior and posterior ligaments, and including the intervertebral discs, are formed. The sympathetic nerves within these networks extend over two or three vertebral segments forming a dense plexus (Groen et al., 1990). In animal models at least, this plexus provides an important route to sympathetic rami for afferent nerves supplying the lumbar intervertebral discs (Suseki et al., 1998). The region dorsal to the intervertebral foramina comprises the posterior neck muscles, the ZA joints, the ligamentum nuchae, and ligamentum flavum and adjoining portion of the dura mater. Gross anatomical studies have shown that the medial branch of the posterior primary rami from the C4–C8 nerves supply the ZA joints in a highly organized segmental fashion (Bogduk, 1982; Bogduk and Marsland, 1988). Small sensory nerves demonstrating SP- and CGRP-immunoreactivity have been located within the mensical or synovial folds of the human cervical ZA joints (Inami et al., 2001). These nerves are found distant from blood vessels which suggests they have an alternative role other than a vaso-afferent one. The nerve endings in the cervical ZA joint capsules have the morphological characteristics, at the ultrastructural level, of nociceptors and mechanoreceptors (McLain, 1994). Reports regarding innervation of the ligamentum flavum vary with a general consensus that these structures do not have a well-developed nerve supply (Soinila and Vanhatalo, 1994; Cramer, 2001). However, a recent immunohistochemistry study of the human ligamentum flavum in the lumbar spine revealed the presence of fine nerve fibres in 72% of specimens with a further 25% of these nerves estimated to be sensory in nature (Bucknill et al., 2002). The atlanto-occipital and lateral atlanto-axial joints are not in accord with the model of dorsal and ventral innervation in the cervical spine. These joints are supplied by C1/C2 ventral rami (Dreyfuss et al., 1994), with the dorsal aspect of the dura supplied via the sympathetic nerves from the ventral dura (Groen et al., 1988; Groen and Stolker, 2000). 2.1. The vertebral nerve Unique to the cervical spine is the vertebral nerve. It is sympathetic in nature and is essentially a set of deep gray rami communicantes which accompany the verteb-

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ral artery (Pick, 1970) to form intersegmental neural arcades between C3 and C6 (Bogduk et al., 1981). The vertebral nerve is macroscopically distinct from the perivascular nerves (the vertebral plexus), the intrinsic nerves located within the adventitia of the vertebral artery (Chen et al., 1988). During its course through the transverse foramina of the cervical vertebrae, the vertebral nerve receives additional sympathetic fibres from the middle cervical ganglion (Pick, 1970). The vertebral nerve is less distinct in the upper cervical spine where it merges with the vertebral plexus (Lang, 1993). The vertebral plexus receives additional nerve fibres from a number of sources including sympathetic fibres directly from the superior cervical ganglion (Lang and Kessler, 1991), via the gray ramus of C1 spinal nerve (Bogduk et al., 1981) and sensory fibres from the C2 and C3 dorsal root ganglion (DRG) (Kimmel, 1959). The functional significance of the vertebral nerve, often overlooked, is that its deep rami communicantes provide a sympathetic pathway additional to the superficial set which arise directly from the cervical sympathetic trunk (Pick, 1970). Rami communicantes from the vertebral nerve communicate with the ventral rami of cervical nerves at each segmental level in the lower cervical spine (Bogduk et al., 1981; Groen et al., 1990). Branches also contribute to the formation of the sinuvertebral nerves (Groen et al., 1990), and accompany the radicular arteries and veins to supply the internal venous plexus of the spinal cord (Lang, 1993). Also worthy of note is the fact that the perivascular sensory nerves located in blood vessels such as the vertebral plexus contain a number of neuropeptides including SP and may be a source of nociception in the case of a dissecting vertebral artery (Appenzeller, 1994). Most lesions to the vertebral artery occur at the C1/C2 level (Schievink, 2001) and characteristically, this pain presents as a dull, persistent pain often severe, with sudden onset and is localized to the neck and ipsilateral craniocervical junction (Appenzeller, 1994). Although as many as 50% of patients present with these symptoms (Prabhakar et al., 2001) the condition of a dissecting vertebral artery is easily overlooked because of its rarity, and the fact that the pain pattern bears a close similarity to other conditions such as cervicogenic headache (Edmeads, 1988). Even less well recognized is that transient vertigo may be caused by constriction of the vertebral artery (Tomita et al., 1987) due to the C2 ventral ramus as its winds anteriorly around the vessel at the C1–C2 level (Lang and Kessler, 1991). In addition, pathological lesions such as osteophyte formation in the uncovertebral joints may encroach on both the vertebral nerve and the vertebral artery (Hutchinson and Yates, 1956). The sinuvertebral nerve is also vulnerable to trauma due to its close relationship with the uncovertebral joints (Chen et al., 1988).

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3. Sensory nerve pathways within the cervical spine Research on laboratory animals using the ZA joint as an experimental model gives insight into the extent to which somatic afferent nerves use sympathetic pathways. Ohtori et al., (2001a) have demonstrated in the rat that somatic afferent fibres from the C5/C6 cervical ZA joints have their cell bodies in the DRG extending between the C3 and T3 levels. In contrast, after sympathectomy, the majority of labelled cell bodies of nerve fibres innervating the C5/C6 ZA joint were found at the corresponding segmental levels of the C5 and C6 DRG (Ohtori et al., 2001a). In a complementary experiment (Ohtori et al., 2002) demonstrated that in the sensory nerves supplying the C5/C6 facet joint of the rat, the ratio of CGRPimmunoreactive cells in the C5 and C6 DRG was significantly higher than those in the C3, C4, C7 and C8 DRG (Ohtori et al., 2002). These results imply in the normal physiological state, the cell bodies associated with the somatic afferent fibres that use the sympathetic pathways are distinguished by lower levels of CGRPimmunoreactvitiy than those nerves innervating the ZA joints segmentally. Further confirmation that a proportion of somatic afferent fibres supplying the ZA joints are innervated by fibres bypassing sympathetic pathways has been demonstrated in the lumbar spine of rats. For example, it has been estimated that up to 23% of the sensory fibres arising from the L5/L6 ZA joint travel along alternative routes, via ipsilateral rami communicantes and sympathetic pathways, before entering the L1 and L2 DRG (Suseki et al., 1997). Furthermore, in keeping with the cervical spine, the cell bodies of somatic afferent fibres from ZA joints in the lumbar spine using the sympathetic pathways were characterized with significantly lower levels of CGRP and SP than those associated with fibres taking the segmental route (Ohtori et al., 2000). Of particular interest clinically is the finding that altered levels of neuropeptide expression in DRG cells can be detected after experimentally induced ZA pathology (Ohtori et al., 2001b). In this experiment, an inflammatory reaction was induced by injection of complete Freund’s adjuvant into the L5–L6 ZA joint. The results showed that the ratio of CGRP-immunoreactive cells in the DRG at the L1–L5 levels increased significantly in the inflammatory ZA group when compared to the control group. Furthermore, the mean cross-sectional area of DRG cells demonstrating positive CGRP-immunoreactivity increased in size from 621762 mm2 in the control group to as much as 893763 mm2 in the inflammatory group (Ohtori et al., 2001b). The observed changes in DRG cells throughout the L1–L5 levels imply that in the abnormal physiological state, somatic afferent nerve fibres, including those using

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the sympathetic pathways undergo neuroplastic changes. This mechanism may be a contributing factor to overlapping pain referral patterns seen clinically in ZA joint dysfunction both in the cervical (Bogduk and Marsland, 1988) and in the lumbar spines (Mooney and Robertson, 1976). Futhermore, this finding highlights the difficulty of assuming the location of a spinal dysfunction based solely on symptoms of pain. Moreover, if the pattern of innervation applies to humans, then it may explain why only partial resolution of symptoms is achieved if treatment is focused on only one segmental level. Normally, sympathetic postganglionic neurons do not communicate with afferent neurons in the periphery and the sympathetic nervous system is not involved with the generation of pain (J.anig and Habler, 2000). However the sympathetic nervous system is involved in various protective reflex mechanisms including the sensory system. The finding of a small proportion (9.3%) of somatic afferent fibres (with CGRP-immunoreactivity) originating from the lumbar ZA joints in close proximity to postganglionic neurons in the adjoining sympathetic trunk raises the possibility that other forms of modulatory control may exist between the two systems (Suseki et al., 1996). Hypothetically this could mean that sensory impulses from the ZA joints could effect change in blood vessel diameter or connective tissue metabolism or, alternatively be related to sensory activity in the facet joints (Suseki et al., 1996).

4. Innervation features in the craniocervical region The upper cervical spine in the human is anatomically complex and connective tissue bridges extending between the dura mater and the rectus capitis posterior minor muscles in the upper cervical spine are considered to be of potential relevance with regard to certain cervicogenic headaches (Hack et al., 1995; Mitchell et al., 1998; Alix and Bates, 1999; Dean and Mitchell, 2002). It is therefore of interest to note the features of neuropeptide distribution which have been identified in the dura within the craniocervical region. The human spinal dura, particularly the ventral aspect, is richly innervated with nerve fibres principally from the sinuvertebral nerve plexus and which are a widely distributed over up to eight vertebral segments (Groen et al., 1988). Additional contributions from the perivascular nerve plexus originating from the radicular arteries has also been identified (Groen et al., 1988). In general terms, the pattern of innervation is relatively consistent throughout the length of the spinal column. However investigators have been able to identify discrete subpopulations of nerve fibres within the cervical spine dura mater by using immunocytochemistry localization

of different neuropeptides which have not been previously recognized. Yamada et al. (1998) have demonstrated the presence of small fibres expressing CGRP-immunoreactivity running within the epiradicular sheath of the dorsal root ganglion in the cervical spine of the rat. These fibres also innervate the neighbouring spinal dura mater (Yamada et al., 1998). Yet another set of sensory nerve fibres expressing SP-immunoreactive fibres in the epiradicular sheath has also been identified (Yamada et al., 2001). These nerve fibres originate directly from the DRG and represent an additional source of innervation independent from that of the sinuvertebral nerves. Recent attention in animal studies has also focused on a prominent set of sympathetic fibres located in the cranial dura of the craniocervical region (Keller et al., 1989; Keller and Marfurt, 1991) which extend into the spinal dura and posterior longitudinal ligament of the upper cervical spine (Yamada et al., 2001). This population of so-called ‘‘free’’ sympathetic nerves demonstrate NPY-immunoreactivity and, unlike the majority of sympathetic nerves expressing NPY, are distinguished by their lack of close proximity to blood vessels (Keller et al., 1989; Keller and Marfurt, 1991). These ‘‘free’’ nerves arise from two different sources within the cervical sympathetic trunk. ‘‘Free’’ nerves fibres in the upper cervical region originate from the stellate ganglion (Yamada et al., 2001) while those in corresponding cranial dura component arise from the superior cervical ganglion (Keller et al., 1989). Mast cells are strongly implicated in the pathogenesis of vascular headache and head pain (Keller and Marfurt, 1991) and contribute to inflammatory responses including neurogenic inflammation in association with neuropetides released from afferent terminals of the trigeminal ganglion (Coderre et al., 1989). The function of the non-vascular ‘‘free’’ sympathetic nerve fibres is a subject of debate but it is suggested that these cells may influence the mast cell population within the dura mater or alternatively, be involved with ‘‘cross talk’’ with other peptidergic nerves running within the cranial dura mater (Keller and Marfurt, 1991). The aetiology of some cervicogenic headaches is considered to have a neurogenic component (Jull, 1997) and the finding that sympathetic innervation of the spinal dura mater and posterior longitudinal ligament of the cervical region share characteristics in common with nerves of the cranial dura is of interest in this regard. Work done on the identification of neuropeptidergic populations of nerves in human cranial dura and spine is in its infancy. Nevertheless, the results of a recent study on the human cranial dura has revealed an increased density of sympathetic nerve fibres running in the basal region of the human occipital dura mater in which a small proportion were found to

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be independent from blood vessels (Artico and Cavallotti, 2001). Further work in defining the ultrastructural features and clarification of neuropeptide content in the nerves within the connective tissues of the human craniocervical region is needed to further develop understanding with regard to the pathogenesis of cervicogenic headaches and their responses to physiotherapy treatment. Recent evidence also suggests that convergence of afferent input from visceral organs such as the heart and gastrointestinal tract may also activate upper cervical cells that refer pain to the head and neck (Foreman, 2000). Symptoms of a distinctly visceral nature have not been reported in association with cervicogenic headache (Edmeads, 1988; Jull, 1997) but it is clear in the light of emerging research findings that the underlying contributing mechanisms are likely to be multifactorial but also implicate sympathetic nervous system involvement.

5. Conclusion There is strong evidence that cervical spine and its related structures are innervated by nerve fibres which have partly sympathetic and sensory nerve pathways. The early appreciation of this concept has been greatly enhanced by the ability in animal models to trace and identify different populations of sensory fibres within the peripheral nervous system. While the focus in this paper has been directed towards ZA joint nerve supply in order to illustrate the possible clinical implications of non-segmental innervation patterns this feature is not restricted to these joints or the cervical spine. In conclusion, and in summary there are three key findings of possible clinical relevance in recent studies investigating cervical spine innervation. The first one being potential sources of nociception include the perivascular nerve plexus and vertebral nerve which accompany the vertebral artery. Secondly, the animal model of ZA joint innervation and nonsegmental pathways of some sensory fibres serve to further highlight the difficulty of diagnosing cervical spinal dysfunction in patients based on symptoms of pain alone. Finally, there is some evidence to indicate that a sub-population of sympathetic nerves within the upper cervical spine region share certain characteristics with those in the cranial dura and that they may play a role in neurogenic inflammation.

Acknowledgements The author wishes to thank Professor Gareth Jones, Department of Anatomy and Structural Biology, University of Otago and Emeritus Professor Martin Kean

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for their comments and helpful suggestions during the preparation of this manuscript.

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Original article

The initial effects of a Mulligan’s mobilization with movement technique on dorsiflexion and pain in subacute ankle sprains Natalie Collins, Pamela Teys, Bill Vicenzino* Department of Physiotherapy, The University of Queensland, St. Lucia, Brisbane, QLD 4072, Australia Received 17 December 2002; received in revised form 25 July 2003; accepted 21 August 2003

Abstract Physiotherapists frequently use manipulative therapy techniques to treat dysfunction and pain resulting from ankle sprain. This study investigated whether a Mulligan’s mobilization with movement (MWM) technique improves talocrural dorsiflexion, a major impairment following ankle sprain, and relieves pain in subacute populations. Fourteen subjects with subacute grade II lateral ankle sprains served as their own control in a repeated measures, double-blind randomized controlled trial that measured the initial effects of the MWM treatment on weight bearing dorsiflexion and pressure and thermal pain threshold. The subacute ankle sprain group studied displayed deficits in dorsiflexion and local pressure pain threshold in the symptomatic ankle. Significant improvements in dorsiflexion occurred initially post-MWM (Fð2;26Þ ¼ 7:82; P ¼ 0:002), but no significant changes in pressure or thermal pain threshold were observed after the treatment condition. Results indicate that the MWM treatment for ankle dorsiflexion has a mechanical rather than hypoalgesic effect in subacute ankle sprains. The mechanism by which this occurs requires investigation if we are to better understand the role of manipulative therapy in ankle sprain management. r 2003 Elsevier Ltd. All rights reserved. Keywords: Manipulation; Ankle; Pain; Movement

1. Introduction The lateral ligament complex of the ankle, described as the body’s ‘‘most frequently injured single structure’’ (Garrick, 1977), is mechanically vulnerable to sprain injury. At extremes of plantarflexion and inversion, influenced by the shorter medial aspect of the ankle mortise, the relatively weak anterior talofibular ligament (ATFL) and calcaneofibular ligament (CFL) are prone to varying grades of rupture, often via minimal force (Hockenbury and Sammarco, 2001). Immediate inflammatory processes produce acute anterolateral pain and oedema, with avoidance of movement and weight bearing (Wolfe et al., 2001). Subsequent losses of joint range, particularly dorsiflexion, and muscle strength results in significant gait dysfunction. Recent data from our laboratory highlights the presence of a dorsiflexion deficit not only in the

*Corresponding author. Tel.: +61-7-3365-2781; fax: +61-7-33652775. E-mail address: [email protected] (B. Vicenzino). 1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1356-689X(03)00101-2

acute stage, but also in the subacute stage (Yang and Vicenzino, 2002). Early physiotherapy intervention consists of rest, ice, compression, elevation (RICE) and electrotherapy modalities to control inflammation, as well as manipulative therapy and therapeutic exercise techniques to address impairments of movement and strength (Wolfe et al., 2001; Hockenbury and Sammarco, 2001). Green et al. (2001) investigated the impact of combining nonweight-bearing talocrural anteroposterior (AP) passive mobilisations, believed to restore dorsiflexion range, with the RICE protocol in the treatment of acute ankle sprains. The experimental group ðn ¼ 19Þ demonstrated a more rapid improvement in pain-free dorsiflexion and function than the control group ðn ¼ 19Þ who were treated solely with RICE. This provides important evidence substantiating the role of passive joint mobilizations in an acutely injured population. The mobilization with movement (MWM) treatment approach for improving dorsiflexion post-ankle sprain combines a relative posteroanterior glide of the tibia on talus (or a relative anteroposterior glide of the talus on the tibia) with active dorsiflexion movements,

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preferentially in weight bearing (Mulligan, 1999). Claims of rapid restoration of pain-free movement are associated with MWM techniques generally (Mulligan, 1993, 1999; Exelby, 1996). Through examination of the effects of MWM on ankle dorsiflexion in asymptomatic mildly restricted ankle joints, Vicenzino et al. (2001) found that both the weight bearing and non-weightbearing variations of the dorsiflexion MWM technique produced significant gains in dorsiflexion range. However, weight-bearing treatment techniques are widely believed to be superior to non-weight-bearing techniques, as they replicate aspects of functional activities (Mulligan, 1999). Acute ankle sprains, whilst having marked reduction in dorsiflexion range of motion, are frequently painful in full weight bearing, and weightbearing techniques are not clinically indicated. The subacute ankle sprain is characterized by significant residual deficits in dorsiflexion (Yang and Vicenzino, 2002) and the capacity to fully weight bear, making it a good model on which to study the initial effects of weight-bearing MWM on dorsiflexion. The mechanism of action of manipulative therapy has been the focus of several reports in recent times, however spinal manipulative therapy appears to be the common subject of research. A synopsis of current evidence for the initial mechanism of action of manipulative therapy indicates in part a neurophysiological basis (Vicenzino et al., 1996, 1998, 2000). Manipulative therapy treatment techniques studied have exhibited non-opioid hypoalgesia to mechanical but not thermal pain stimuli (Vicenzino et al., 1995, 1998). The primary objective of this study was to test the hypothesis that application of Mulligan’s MWM technique for talocrural dorsiflexion to subacute lateral ankle sprains produces an initial dorsiflexion gain, and simultaneously produces a mechanical but not thermal hypoalgesia.

2. Methods The double-blind randomized controlled trial incorporated repeated measures into a cross over design, in which each participant served as their own control. 2.1. Participants Sixteen participants, eight males and eight females aged 18–50 (average 28.25 years and standard deviation 9.33 years), were recruited through the University Physiotherapy Clinic, local physiotherapy practices and sporting clubs, and University advertising. The primary criterion for inclusion was a grade II ankle lateral ligament sprain that was sustained on average 40 days (724 days standard deviation) prior to testing. We defined this sprain as ‘‘an incomplete tear of the

ligament with mild laxity and instability (and) slight reduction in functiony’’ (Safran et al., 1999); A minimum pain-free dorsiflexion asymmetry of 10 mm on weight-bearing measure (Vicenzino et al., 2001), anterolateral ankle tenderness, and full pain free weightbearing capacity were also required. Acute ankle sprains were excluded due to the potential for exacerbation of pain with repeated testing on the outcome measures. Exclusion also occurred if fracture or intra-articular ankle effusion were clinically detectable, or if there was a recent history of other lower limb or lumbar spine conditions. Physiotherapists and physiotherapy students were excluded to remove a potential source of bias from the participants. Ethical clearance was obtained from the relevant Institution Review Board for ethics at the University of Queensland, and all participants provided informed consent. 2.2. Outcome measures 2.2.1. Dorsiflexion Weight-bearing dorsiflexion (DF), found to have excellent inter- and intra-rater reliability (Bennel et al., 1998), was measured using the knee-to-wall principle. The participant stood in front of a wall, with the test foot’s second toe and midline of the heel and knee maintained in a plane perpendicular to the wall. The participant slowly lunged forward into talocrural dorsiflexion until the knee contacted the wall, and progressively moved the foot back to the point where the knee could just touch the wall with the heel sustained on the ground. This represented end of range dorsiflexion, and the distance between the wall and second toe was measured in millimetres using a tape measure. The examiner ensured maintenance of heel contact via verbal instructions and manual contact with the calcaneum. Vicenzino et al. (2001) found this measure to be more sensitive in detecting treatment effects than an angular weight-bearing measure and a non-weight-bearing measure. 2.2.2. Pain Quantitative measures of pain were obtained via pressure and thermal pain threshold. Pressure algometry, which has demonstrated reliability (Pontinen, 1988), was used to measure pressure pain threshold (PPT) at three lower limb sites: (1) over the proximal third of the tibialis anterior muscle belly; (2) directly distal to the lateral malleolus over the CFL; (3) directly anterior to the lateral malleolus over the ATFL. A digital pressure algometer (Somedic AB, Farsta, Sweden) was used to measure the pressure applied to the test site by a rubbertipped probe (area 1 cm2), which was positioned perpendicular to the skin. The pressure was applied at a rate of 40 kPa/s. Activation of a button by the

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participant at the precise moment that the pressure sensation changed to one of pain and pressure, signalled cessation of pressure application, and froze the measurement onscreen for manual recording. The Thermotest System (Somedic AB, Farsta, Sweden) measured hot and cold thermal pain threshold (TPT). A rectangular contact thermode was manually positioned over two sites: (i) the proximal third of the tibialis anterior muscle belly, and (ii) over the ATFL, extending from the anteroinferior border of the lateral malleolus toward the toes at an angle that allowed maximal contact with the foot contours. The hot or cold stimuli were increased at a rate of 1 C/s from a baseline of 30 C. Participants pressed a button at the precise moment that the thermal sensation changed to one of pain and heat for heat pain threshold, and one of pain and cold for cold pain threshold. At this point, stimulation ceased and the temperature reached was manually recorded. Automatic cut-off points of 52 C and 2.5 C were adopted to ensure safe stimulus application. 2.3. Treatment conditions Three treatment conditions, consisting of MWM for dorsiflexion, placebo and a no-treatment control, were studied. During the treatment condition, the dorsiflexion MWM technique was performed on the symptomatic talocrural joint, as described by Mulligan (1999). With the participant in relaxed stance on a bench, a nonelastic seatbelt was placed around the distal tibia and fibula and the therapist’s pelvis, with foam cushioning the Achilles tendon (Fig. 1). A backward translation by the therapist imparted tension on the seatbelt and a posteroanterior tibial glide, while the talus and forefoot were fixated with the webspace of one hand close to the

Fig. 1. The weight-bearing mobilization with movement technique in which the therapist applies a posteroanterior force to the distal leg through a treatment belt while manually stabilizing the foot and talus.

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anterior joint line. The other hand was positioned anteriorly over the proximal tibia and fibula to direct the knee over the second and third toes to maintain a consistent alignment of the distal leg and foot. The glide was sustained during slow active dorsiflexion to end of pain-free range, with the seatbelt kept perpendicular to the long axis of the tibia throughout movement, and released after return to the starting position. Three sets of 10 repetitions were applied, with one minute between sets (Exelby, 1996). Pain experienced during treatment resulted in immediate cessation of the technique and exclusion from the study. The placebo condition replicated the treatment condition, with the following exceptions. The seatbelt was placed over the calcaneum, and only minimal tension imparted to take up the slack. One hand remained on the proximal tibia and fibula, however the other hand was positioned across the metatarsal bases. Instructions were given to produce a small inner range dorsiflexion while the seatbelt was maintained perpendicular to the tibia. An identical number of repetitions, sets and interval period were used. In the control condition, the participant assumed the same relaxed stance position as for treatment and placebo, and maintained this for five minutes. No manual contact occurred between the therapist and participant. 2.4. Procedure A preliminary session, during which a clinical examination and the three outcome measures were performed on both ankles, was conducted initially to determine the participant’s suitability for inclusion. This session also served to familiarize participants with testing procedures. Suitable participants returned for three testing sessions within one week of the initial appointment. These were scheduled at similar times of the day to prevent diurnal variations in joint range and pain, and allow a 24-h interval for wash-out of any treatment effects. Testing was conducted in an environment-controlled laboratory, with constant temperature and humidity. Each testing session began with the asymptomatic then symptomatic ankles undergoing each of the three outcome measures. With the participant in side lying, a splint was applied to the testing ankle to maintain a standardized 10 of plantarflexion. PPT and TPT measures were then conducted in an order randomized by the toss of a coin, followed by weight-bearing dorsiflexion. Three repetitions of each measure were taken. The examiner then left the laboratory while the therapist then entered and applied one of the treatment conditions (MWM, placebo, control) to the symptomatic ankle. Following treatment, outcome measures were repeated on the symptomatic ankle by the


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Table 1 Intraclass correlation coefficient (standard error of measurement) for the pressure, heat and cold pain threshold measures Pain stimulus

ATFL

CFL

TA

Pressure Heat Cold

0.98 (5.57 kPa) 0.99 (0.40 C) 0.98 (0.64 C)

0.95 (8.93 kPa)

0.95 (12.00 kPa) 0.97 (0.22 C) 0.99 (0.74 C)

examiner to evaluate the effect of treatment. This procedure facilitated blinding of the examiner. The participant was unaware of the aim of the study and which treatment condition was under investigation. Over the 3 days of involvement in the primary study, each participant experienced all three treatment conditions in a randomised order as determined by the roll of a dice by the therapist.

3. Reliability Acceptable intrarater reliability was determined through analysis of pre-treatment data from the three testing sessions. The intraclass correlation coefficient (ICC) and standard error of measurement (SEM) data for the pain measures are presented in Table 1. The ICC and SEM for the dorsiflexion measure were 0.99 and 3.50 mm, respectively. The ICC for the pain measures ranged from 0.95 to 0.99. The SEM for pressure pain threshold ranged from 5.57 to 12.00 kPa, and the thermal pain threshold SEM ranged from 0.22 to 0.74 C. Note that both the size of the error (SEM) and the ICC are indicative of reliable measures.

4. Data management and analysis Two independent variables were incorporated into the research design; TREATMENT (MWM, placebo, control), and TIME of application (pre- and post-intervention). Three dependent variables, measures of pressure pain threshold (PPT), thermal pain threshold (TPT) and dorsiflexion (DF), were evaluated. Prior to analysis, triplicate DF, PPT and TPT data were averaged. Data pertaining to two of the participants were excluded from analysis; subject 4 who had a post-testing MRI that revealed an osteochondral lesion of the talus and ankle joint effusion, and subject 7 who experienced pain during the MWM technique. Pre-experiment differences between sides (symptomatic–asymptomatic) were evaluated by paired t-tests ða ¼ 0:05Þ: A two-factor analysis of variance (ANOVA) was then performed on each of the three dependent variables to test the hypothesis that MWM produced changes in excess of placebo and control from pre- to post-

application. Any significant interaction effects were followed up with tests of simple effects. Post hoc tests of main effects were performed in the absence of an interaction. A Bonferroni adjustment ðaadjusted ¼ 0:05=3 ¼ 0:017Þ was used to interpret results of the pair wise tests of simple effects and to adjust for any type I error resulting from multiple comparisons.

5. Results 5.1. Pre-experiment deficits in outcome measures Pre-experiment values for dorsiflexion and pain measures of the affected and unaffected ankles are displayed in Table 2. Statistical analysis of side-to-side differences revealed a deficit only for dorsiflexion (DF) (t ¼ 5:689; Po0:001) and pressure pain threshold over the anterior talofibular ligament (PPT ATFL) (t ¼ 2:570; P ¼ 0:025). No such deficits in thermal pain threshold (TPT) were found. 5.2. Primary study 5.2.1. Dorsiflexion A significant interaction time by condition effect for the dorsiflexion outcome measure was detected by the ANOVA (Fð2;26Þ ¼ 7:817; P ¼ 0:002). The interaction plot is shown in Fig. 2. Post hoc analysis revealed a significant treatment effect for dorsiflexion from pre- to post-application (t ¼ 2:870; P ¼ 0:013). The post hoc analysis for the pre- and post-application data showed no significant differences between the placebo (t ¼ 1:343; P ¼ 0:202) and control (t ¼ 1:324; P ¼ 0:208) conditions. Table 3 presents the dorsiflexion data.

Table 2 Pre-experiment mean (standard deviation) values of the outcome measures for asymptomatic and symptomatic sides Outcome measure Dorsiflexion (mm) Pressure pain threshold (kPa)

Region

Asymptomatic

Symptomatic

ATFL

100.93 (41.04) 212.61 (73.52)

58.57 (36.25) 154.82 (55.89)

CFL TA

348.28 (93.23) 378.78 (115.46)

323.46 (95.09) 348.29 (107.93)

Heat pain threshold ( C)

ATFL TA

43.48 (2.45) 43.83 (2.97)

43.39 (3.57) 44.26 (2.14)

Cold pain threshold ( C)

ATFL TA

10.74 (7.07) 8.24 (8.30)

11.07 (6.39) 8.85 (7.59)

Abbreviations: ATFL=anterior talofibular ligament; CFL=calcaneofibular ligament; TA=tibialis anterior. Denotes statistically significant difference ðPo0:05Þ:


81

5.2.2. Pain The data for pain thresholds for pressure, cold and heat stimuli are expressed as mean and standard deviation in Table 4. Statistical analysis of the pain related data revealed no interaction effects (see Fig. 2 for plots). However, there were main effects for time for PPT ATFL (Fð1;13Þ ¼ 6:401; P ¼ 0:025) and PPT TA (Fð1;13Þ ¼ 9:17; P ¼ 0:010). Post hoc tests of simple effects demonstrated significant pre- to post-differences for PPT ATFL in the placebo condition (t ¼ 2:774; P ¼ 0:016) (Fig. 3), but no significant change in PPT TA. No significant time or condition effects were evident for PPT CFL, or the TPT measures.

Fig. 2. The Treatment condition (MWM, Placebo, Control) by Time interaction plot for dorsiflexion (squares, significant interaction Fð2;26Þ ¼ 7:817; P ¼ 0:002), pressure pain threshold (PPT) at the anterior talofibular ligament (ATFL) test site (circles) and over the tibialis anterior muscle belly (Tib Ant) test site (triangles). Closed figures (squares, circles and triangles) indicate pre-treatment condition and open figures indicate post-treatment. The indicates a significant difference after treatment when compared to before treatment ðPadjusted o0:017Þ:

Table 3 Mean and standard deviation for dorsiflexion (mm) under the three treatment conditions Time

MWM

Placebo

Control

Pre Post

57.27 (41.00) 68.93 (45.44)

60.17 (38.49) 62.07 (38.97)

58.29 (32.67) 56.42 (33.48)

There were no significant differences between conditions in the preapplication data. Denotes significant change ðPo0:017Þ:

6. Discussion Application of the dorsiflexion mobilization with movement (MWM) technique to patients with subacute lateral ankle sprains produced a significant immediate improvement in dorsiflexion, but had no significant initial effect on mechanical and thermal pain threshold measures. This dorsiflexion gain following manipulative therapy parallels findings by Green et al. (2001) in acute ankle injuries, and Vicenzino and colleagues’ (2001) study of asymptomatic minimally restricted ankles. Current and previous research findings suggest that the predominant mechanism of action for the dorsiflexion MWM technique is most likely mechanical, rather than a direct hypoalgesic effect. An excessive anterior displacement of the talus is believed to occur during plantarflexion/inversion injury and persist with residual laxity of the anterior talofibular ligament (ATFL) (Mulligan, 1999). Denegar et al. (2002) reported increased ATFL laxity and restricted posterior talar

Table 4 Mean and standard deviation for the pain measures under the three treatment conditions before and after their application Stimulus

Region

Time

MWM

Pressure (kPa)

ATFL

Pre Post Pre Post Pre Post

154.19 166.74 327.44 335.04 371.85 394.79

Pre Post Pre Post

43.14 42.57 44.74 44.46

(2.49) (2.29) (2.46) (2.21)

43.20 44.14 44.73 44.14

(2.24) (3.36) (2.40) (2.42)

43.78 43.76 44.63 44.77

(3.26) (2.61) (2.43) (2.72)

Pre Post Pre Post

10.80 9.86 8.25 8.04

(5.87) (5.54) (6.23) (5.85)

11.06 10.77 8.18 7.95

(6.13) (6.56) (7.11) (7.19)

9.07 8.93 7.25 7.62

(5.41) (6.26) (6.10) (6.72)

CFL TA

Heat ( C)

ATFL TA

Cold ( C)

ATFL TA

(48.64) (78.68) (83.15) (76.56) (115.43) (147.81)

Placebo

Control

155.38 179.05 318.43 341.13 372.43 385.01

175.12 187.66 346.68 325.28 385.55 420.94

(68.69) (75.33) (96.31) (135.58) (144.57) (144.12)

(89.03) (101.55) (148.70) (146.88) (160.20) (185.79)

There were no significant differences between conditions in the pre-application data. Abbreviations: ATFL=anterior talofibular ligament; CFL=calcaneofibular ligament; TA=tibialis anterior.

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N. Collins et al. / Manual Therapy 9 (2004) 77–82

glide in twelve athletes who had sustained an ankle sprain 6 months earlier and had since returned to sport. The clinical rationale given for the anteroposterior glide component of the weight-bearing dorsiflexion MWM technique is to reduce any residual anterior displacement of the talus (Mulligan, 1999). Mulligan (1993, 1999) proposed that correction of the restricted posterior glide, via repetitions of DF with a sustained anteroposterior talar mobilization (mechanically similar to posteroanterior tibial glide on talus), restores the normal joint kinematics even after release of the glide. The mechanism by which this occurs in the presence of ATFL laxity requires further examination. Despite the presence of a reduction in pressure pain threshold (PPT) over the ATFL, the MWM technique did not produce a significant change in local PPT in the initial post-treatment period. The dorsiflexion MWM’s mechanism of action therefore appears to be mechanical, and not directly via changes in the pain system. The conduct of further research is required to identify a precise mechanism. While small but non-significant increases in pressure pain threshold occurred following treatment and control application, it was the placebo condition that produced a statistically significant improvement in pressure pain threshold over the ATFL. It is possible that the gentle inner range dorsiflexion movement performed during the placebo condition was more successful at altering the local pathophysiology peripherally at the ankle or via central neurophysiological mechanisms than the sustained end of range glide and larger range movement of the MWM technique. The application of small amplitude accessory glides of joints in an acute and painful state has been previously advocated (Maitland, 1985) and their benefits in the subacute population requires further investigation. The reasonably small sample size should also be considered to have influenced the results of the statistical analysis. It is possible that the pain measures have a lower sensitivity to change than the dorsiflexion measure, yet the significant dorsiflexion improvement seen post-treatment indicates that range gains are the predominant effect. In addition the failure to elicit prestudy deficits in thermal pain thresholds most likely lessened the likelihood of detecting a change with treatment. Research using a larger sample size and possibly acute ankle sprains with deficits in thermal pain, should they exist, may reveal differences not detected in this study.

7. Conclusion Mulligan’s dorsiflexion mobilization with movement technique significantly increases talocrural dorsiflexion initially after application in subacute ankle sprains. The

absence of hypoalgesia post-application suggests a predominant mechanical rather than hypoalgesic effect behind the technique’s success. Further research using a larger sample is required to determine the exact mechanism behind this.

References Bennel K, Talbot R, Wajswelner H, Techovanich W, Kelly D. Intrarater and inter-rater reliability of a weight-bearing lunge measure of ankle dorsiflexion. Australian Journal of Physiotherapy 1998;44(3):175–80. Denegar CR, Hertel J, Fonseca J. The effect of lateral ankle sprain on dorsiflexion range of motion, posterior talar glide, and joint laxity. The Journal of Orthopaedic and Sports Physical Therapy 2002;32(4):166–73. Exelby L. Peripheral mobilisations with movement. Manual Therapy 1996;1:118–26. Garrick JG. The frequency of injury, mechanism of injury, and epidemiology of ankle sprains. American Journal of Sports Medicine 1977;5(2):241–2. Green T, Refshauge K, Crosbie J, Adams R. A randomised controlled trial of a passive accessory joint mobilisation on acute ankle inversion sprains. Physical Therapy 2001;81(4):984–94. Hockenbury RT, Sammarco GJ. Evaluation and treatment of ankle sprains. The Physician and Sports medicine 2001;29(2):57–64. Maitland G. Passive movement techniques for intra-articular and periarticular disorders. Australian Journal of Physiotherapy 1985;31:3–8. Mulligan BR. Mobilisations with movement (MWM’S). The Journal of Manual and Manipulative Therapy 1993;1(4):154–6. Mulligan BR. Manual therapy ‘‘NAGS’’, ‘‘SNAGS’’, ‘‘MWM’S’’ etc, 4th ed. Wellington: Plane View Services Ltd; 1999. Pontinen PJ. Reliability, validity, reproducibility of algometry in diagnosis of active and latent tender spots and trigger points. Journal of Musculoskeletal Pain 1988;6(1):61–71. Safran MR, Benedetti RS, Bartozolli AR, Mandelbaum BR. Lateral ankle sprains: a comprehensive review. Part 1: etiology, pathoanatomy, histopathogenesis, and diagnosis. Medicine and Science in Sports and Exercise 1999;31(7 Suppl):S429–37. Vicenzino B, Collins D, Benson H, Wright A. An investigation of the interrelationship between manipulative therapy-induced hypoalgesia and sympathoexcitation. Journal of Manipulative and Physiological Therapeutics 1998;21(7):448–53. Vicenzino B, Collins D, Wright A. The initial effects of a cervical spine manipulative physiotherapy treatment on the pain and dysfunction of lateral epicondylalgia. Pain 1996;68:69–74. Vicenzino B, Gutschlag F, Collins D, Wright A. An investigation of the effects of spinal manual therapy on forequarter pressure and thermal pain thresholds and sympathetic nervous system activity in asymptomatic subjects: a preliminary report. In: Shacklock MO, editor. Moving in on pain. Melbourne: Butterworth-Heinemann; 1995. p. 164–73. Vicenzino B, Prangley I, Martin D. The initial effect of two Mulligan mobilisation with movement treatment techniques on ankle dorsiflexion. Australian Conference of Science and Medicine in Sport. A Sports Medicine Odyssey. Challenges, Controversies and Change [CD ROM]. Sports Medicine Australia; 2001. Wolfe MW, Uhl TL, Mattacola CG, McCluskey LC. Management of ankle sprains. American Family Physician 2001;63(1):93–104. Yang CH, Vicenzino B. Impairments in dorsiflexion and joint repositioning in acute, subacute and recurrent ankle sprain: a preliminary report. Journal of Science and Medicine in Sport 2002;5(4):S17.

ARTICLE IN PRESS



Original Article

Reliability of ultrasonography for the cervical multifidus muscle in asymptomatic and symptomatic subjects$ Eythor Kristjansson* Health Sciences at the Faculty of Medicine, The University of Iceland, Skildinganes 36, Reykjav!ık, IS-101, Iceland Received 9 January 2003; received in revised form 6 May 2003; accepted 5 June 2003

Abstract A test–retest and inter-tester study was designed to assess the reliability of ultrasonography to depict the size of the cervical multifidus muscle in asymptomatic and symptomatic subjects. Ten asymptomatic women (range 19–48 years) and 10 women with chronic whiplash associated disorder (WAD), grade II, (range 19–49 years), matched for height and weight participated. The women were imaged by ultrasonography on two separate occasions by two different testers. On each occasion the cross-sectional area (CSA), and the transverse versus the anterior–posterior dimensions (shape ratio) at the C4 level were measured. The repeated measurements of the CSA were plotted against their means to reveal the limit of agreement. Good agreement was found for the asymptomatic group measurements and the intra-tester agreement for the symptomatic group. The inter-tester agreement for the symptomatic group was questionable. The size of the multifidus muscle was significantly reduced in the symptomatic group (Po0:05). The results indicate that loss of clarity of the fascial layer between the semispinalis cervicis muscle and the cervical multifidus muscle may be a diagnostic sign of muscle atrophy. Ultrasonography can be used to precisely measure the size of the cervical multifidus muscle at the C4-level in asymptomatic young female subjects; it is also reliable for symptomatic subjects if the same tester performs the measurements. Additional criteria are recommended to improve the inter-tester agreement for symptomatic subjects. r 2003 Elsevier Ltd. All rights reserved. Keywords: Ultrasonography; Cervical; Multifidus; Assessment; Whiplash; Atrophy

1. Introduction Research has shown that ultrasonography can be used to precisely evaluate muscle dimensions both on the appendicular (Stokes and Young, 1986; Kelly and Stokes, 1993) and the axial skeleton (Rezasoltani et al., 1996, 1998; Emshoff et al., 1999). Among the imaging modalities it is the most cost-effective and feasible method for measurements of the muscular tissue. The muscles are visualized in real-time and measurements can be obtained in a relaxed state and in different states of contraction as well as during movements (Harcke et al., 1988; Rezasoltani et al., 2002). Ultrasonography has been used as a diagnostic tool for the lumbar multifidus (Hides et al., 1995) and is now also used as a $ This study was conducted at an outpatient physiotherapy research clinic. *Tel.: +354-511-1575; fax: + 354-511-1576. E-mail address: [email protected] (E. Kristjansson).

1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1356-689X(03)00059-6

biofeedback method for recruiting the deep muscles in the lumbo-pelvic region (Richardson et al., 1999). Due to the load differences between the cervical and lumbar spine, the cervical multifidus is a much smaller muscle than its counterpart in the lumbo-sacral region. It may therefore be more difficult to identify the cervical multifidus muscle. Recent research into the passive integrity of the cervical spine has demonstrated that women with chronic whiplash associated disorders (WAD), grade II, have a different configuration of the cervical lordosis ! from asymptomatic women (Kristjansson and Jonsson, 2002). The relatively increased lordosis in the upper cervical spine and diminished lordosis in the lower cervical spine observed in this patient group are of great ! clinical importance (Kristjansson and Jonsson, 2002). Interestingly, the same pattern was found in the whole study sample of 100 young asymptomatic subjects when a heavy experimental load was imposed on the cervical spine (Ingelmark, 1942). The altered configuration of

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E. Kristjansson / Manual Therapy 9 (2004) 83–88

the cervical lordosis in this experimental study, conducted 60 years ago, strongly indicates that this pattern was due to increased muscle activity of the superficial torque-producing muscles and the incapability of the tonic deep segmental cervical muscles to maintain the cervical alignment under such great load conditions. One explanation for the altered configuration of the cervical lordosis in patients with WAD may therefore be muscle imbalance due to overactive superficial muscle and/or the diminished holding capacity of the deep cervical muscles. Another recent study exploring sagittal plane segmental motion, conducted on the very same study sample as the above study on the configuration of the ! lordosis, (Kristjansson and Jonsson, 2002) found a subgroup of WAD patients who exhibited increased sagittal plane segmental motion of the mid-cervical segments (Kristjansson et al., 2003). The compromise on the passive integrity of the mid-cervical segments and kyphotic alignment at the C4-level in some WAD patients, grade II, indicates that the passive load-bearing capacity of the mid-cervical spine may be reduced ! (Kristjansson and Jonsson, 2002; Kristjansson et al., 2003). The relatively increased lordosis in the upper cervical spine in WAD patients, grades II, may therefore be a compensatory mechanism reflecting an attempt by the body to bear the weight of the head under these ! circumstances (Kristjansson and Jonsson, 2002). The compromises to the passive integrity of the cervical spine may be the primary source of dysfunction in these patients, and the aforementioned muscle imbalance in the cervical spine may develop secondarily to pain, further increasing the dysfunctional state of these patients. Cumulative evidence suggests that the deeper muscles are better suited to producing fine graded reflex mediated muscle stiffness than the more superficial . muscles (Sjolander et al., 2002). It has recently been suggested that scaling muscle spindle counts to a motor unit number may better represent the sensitivity of the g muscle spindle system (Boyd-Clark et al., 2002). Moreover, the distribution of the spindles seems to be strategically arranged for a particular function. New evidence shows that the longus colli muscle has significantly greater spindle density than the multifidus in the same cervical region, but the multifidus comprises a greater proportion of Type I fibres. The muscle spindles of this muscle pair are also arranged differently (Boyd-Clark et al., 2001, 2002). This might reflect the different functional requirements of these muscles i.e. the longus colli may act more as a balancer of the cervical lordosis (Mayoux-Benhamou et al., 1994) while the cervical multifidus acts as a segmental adjuster (Conley et al., 1995). A measure of cervical multifidus size is an important indicator for whether the muscle is capable of perform-

ing its important segmental stabilizing functions. The purpose of this study was to assess whether ultrasonography can be used to reliably depict the size of the cervical multifidus in asymptomatic and symptomatic subjects. The shape ratio was also measured to be able to, in future research, to compare the geometry of the multifidus muscle with the geometry obtained of the cervical multifidus muscle by other imaging modalities.

2. Methods 2.1. Subjects The participants included 10 asymptomatic women and 10 women with chronic WAD, grade II, according to the Quebec task force classification of WAD (Spitzer et al., 1995). The women were matched according to age, weight and height to minimize the effect of these factors may have on actual muscle size in different individuals (Table 1). The asymptomatic women were a sample of convenience from university students who had no previous history of neck pain or injury. The women in the chronic WAD group were recruited from an outpatient physiotherapy research clinic and had to have had bilateral symptoms in the neck. Their average length of history of whiplash was 22.6 months 712.5. To be included the women had to be non-trainers so training effects would not confound the results. Subjects were not considered for either group if they suffered from diseases affecting the neck or throat, rheumatic or neurological disorders of any kind. All participants completed the Northwick Park Disability Index (Leak et al., 1994), and the whiplash subjects recorded their average pain level on a 100-mm visual analogue scale (VAS). All women gave their informed consent, and ethical clearance for the study was obtained from the Medical Ethics Committee at Landspitalinn University Hospital in Reykjav!ık, Iceland. 2.2. Ultrasonography protocol A 7.5 MHz linear probe (Logiq 200, General Electrics, Milwaukee, WI) was used for the scanning. The subjects were positioned prone on an examination table with both arms lying along the sides of the body. A stable position for the head and neck was obtained by resting the face in the hole of the head section of the table. The whole forehead rested on the table requiring the tester to passively induce slight flexion movement of the occiput upon the atlas. A cushion supported the head in this position to prevent side bending and rotation. The head section of the table was maintained 20 below the horizontal plane to reduce the cervical lordosis. Effort was taken to ensure axial alignment of the spinous processes by inspection. The spinous process at the

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85

Table 1 The characteristics of the asymptomatic group and the symptomatic group Group

Mean7SD Age (years)

Height (m)

Weight (kg)

Asymptomatic (n=10)

31.5711.40 (19–48)

1.6975.48 (1.63–1.78)

67.176.78 (54–78)

Symptomatic (n=10)

32.5711.76 (19–49)

1.6874.95 (1.60–1.77)

70.3710.14 (60–86)

VAS (mm)

NPDI (%)

5.2571.62 (2–7)

45%714% (25–71)

Table 2 Measurements of the cervical multifidus muscle at the C4-level Variable

Mean7SD (range) Asymptomatic (n=10)

Symptomatic (n=10)

Left

Right

Left

Right

CSA (cm2)

1.2570.10 (1.14–1.48)

1.2370.09 (1.12–1.43)

1.0670.19 (0.77–1.31)

0.9670.19 (0.68–1.30)

Shape ratio (LD/APD)

1.5870.14 (1.35–1.88)

1.6870.19 (1.42–2.12)

1.6870.15 (1.35–2.04)

1.7070.32 (1.33–2.39)

Po0.05 by the Mann–Whitney U-test.

Fig. 1. Ultrasonogram of the multifidus muscle cross-sectional area at C4-level in an asymptomatic subject.

C4-level was identified by palpation in the prone position and marked with a pen. This location was double checked by moving the probe from the C2 area down to C4, by following distinctive spinous processes. The configuration of the multifidus muscle was best revealed at this level. The intention was also to measure the multifidus muscle at the C7-level but this was not possible because the muscle was not visible on ultrasonography imaging at this level. Axial images were obtained by placing the middle of the probe perpendicular to the long axis of the posterior neck at the C4-level. The left and right sides were imaged separately. The outlines of the cervical multifidus muscle were identified by the following landmarks: inferiorly by the echogenic vertebral lamina; medially by the echogenic spinous process, and superiorly laterally by the echogenic fascia layer dividing the semispinalis cervicis muscle and the cervical multifidus muscle. The CSA was measured by using on-screen calipers to follow the aforementioned contours of the multifidus muscle (Fig. 1), and the anterior–posterior dimension (APD) and lateral dimension (LD) were measured at right angles to each other as the greatest distance from border to border (Rezasoltani et al., 1996). Each subject was imaged and measured twice on day I by one tester; the

same procedures were repeated on day II by a second tester. The within-day measurements were performed at a 30-min interval and required repositioning of the subjects. Two participating women were imaged in the 30-min interval between each subsequent test–retest trial to minimize the possibility of the testers remembering the measurements from the first test session. All measurements were performed in the afternoon in a darkened room. The testers were blind to the women’s group. 2.3. Data management and analyses Data analysis was performed with the procedures implemented by using SPSS 10.0. Data are presented as mean 7 SD. The CSA (cm2) and the shape ratio (LD/ APD) were calculated and compared using the Mann– Whitney U- test to reveal any between group differences. The intra- and inter-tester agreement for the CSA measurements was assessed and presented by plotting the differences between repeated measurements against their means according to Bland and Altman (1986).

3. Results The subjects’ characteristics are presented in Table 1. The descriptive results of the measurements of the cervical multifidus muscle at the C4-level are summarized in Table 2. The mean difference between groups


86

Table 3 Limit of intra-tester and intertester agreement for CSA measurements at the C4-level Group

Mean difference72SD (cm2) Intra-tester Tester 1

Asymptomatic (n=10) Symptomatic (n=10)

0.070.2 0.0270.16

Inter-tester Tester 2

Tester 1 vs. Tester 2

0.0270.10

0.0270.18

0.0170.12

0.0770.30

was 0.23 cm2 (95% confidence interval, 0.13 – 0.33). The Mann–Whitney U-test revealed that this difference was significant (P ¼ 0:03). The shape ratio was similar between groups and sides (Table 2). The plots of the CSA trials performed within days and between the left and the right sides showed the same pattern as plotting the averaged values of these trials. This confirmed the appropriateness of using averaged values to plot the intra-tester and the inter-tester agreement. The limit of intra- and inter-tester agreement is shown in Table 3. The mean difference of these trials was not significantly different from zero.

4. Discussion The results of this study indicate that the ultrasonography protocol used in this study is reliable in detecting the size of the cervical multifidus muscle at the C4-level in asymptomatic subjects (Table 3). For the symptomatic group, the intra-tester agreement was acceptable (Table 3) but the inter-tester agreement was questionable (Table 3). This is apparent when the limit of agreement (Table 3) is compared to the standard deviations of the measurements (Table 2) and the 95% confidence interval (0.13 – 0.33) for the mean difference between the asymptomatic and the symptomatic groups. As noted, the broader limit of inter-tester agreement for the symptomatic group (0.0770.30) is partly outside the above-mentioned 95% confidence interval. The lack of inter-tester agreement for the symptomatic group (Table 3) makes it therefore more difficult to monitor the changes in the size of the cervical multifidus muscle when comparing results between two or more testers. The wider limit of agreement for the symptomatic group was due to the fact that the outline of the fascia layer dividing the semispinalis cervicis muscle and the cervical multifidus muscle superiorly-laterally was not readily visible in seven out of 10 symptomatic subjects. This can be visualized by comparing Figs. 1 and 2, which show an asymptomatic subject and a symptomatic subject, respectively. This is probably a diagnostic

Fig. 2. Ultrasonogram of the multifidus muscle cross-sectional area at the C4-level in a symptomatic subject.

sign indicating muscle atrophy of the deep cervical muscles and a consequent shrinkage of the fascia layer obscuring its outlines. It has been pointed out in earlier ultrasonography imaging of the semispinalis capitis muscle that the fascia and aponeurotic intersections are clearer in athletes than in non-athletes (Rezasoltani et al., 1999), indicating greater thickness and tensioning of the fascia layers due to muscle hypertrophy in athletes. The ultrasonography imaging in this study supports this. Three symptomatic subjects in this study had similar CSA of the multifidus muscle to the asymptomatic subjects, and the fascia layer in these subjects was also clearly visible. It seems therefore that the measurements of the CSA in the symptomatic group are not reliable until the muscle has reached a certain size. However, the present results also suggest that the multifidus muscle can be ranked as dysfunctional until its fascia layer becomes clearly visible. Different interpretation of the presence of the small rotatores muscles (Figs. 1 and 2) may also have compromised the inter-tester reliability in this study. To enhance objectivity in future research, it is possible to detect the relative brightness of the fascia layer by computer technology. For clinicians it is important to note that the reliability of the CSA measurements seem to be acceptable in clinical settings when one tester is involved in the measurements. The shape ratio, an unitless index, can be used in future studies to compare the geometry of multifidus muscle between different imaging modalities to reveal the validity of the ultrasonography measurements. Prior ultrasonography studies of the splenius (Rezasoltani et al., 1996) and semispinalis capitis (Rezasoltani et al., 1998) muscles, as well as of the lumbar multifidus (Hides et al., 1995), used different statistical methods to assess the reliability of repeated measurements. Plotting the differences against their mean, as in this study, was considered more appropriate as data on repeated measures may show a fairly high correlation coefficient in spite of poor agreement (Bland and Altman, 1986). Ultrasonography depends on a strict measurement protocol as slight angulations of the probe and the


probe pressure exerted on the underlying muscle greatly influence the image produced. The investigator must also have a thorough knowledge of cross-sectional anatomy as the resolution of the image is not as good as on a CT and MRI. Marking the boundaries of the muscle with the cursor is dependent on the investigator’s level of training, and as shown in this present study, on whether the muscle is enclosed in a readily identifiable fascia (Harcke et al., 1988). In order to minimize the error inherent in any measurement, it is necessary to standardize ultrasonography measurements for each muscle or muscle group. Upon inspecting several images taken by computerised tomography (CT) of the same subjects it became clear that the cervical multifidus muscle is a very small muscle at the C7-level. The reason is probably that the C7-level has very tight ligamentous connections, which make this cervical level a very rigid one. Some clinicians even refer to the C7-level as the ‘‘sacrum’’ of the cervical spine. Despite this, clinical experience indicates that the C7-level may exhibit kyphotic alignment in some chronic neck pain patients which was hypothesized might indicate gapping of the zygapohysial joints due to inadequate support from the deep segmental muscles. The C4-level was chosen for imaging in this study for two reasons. Firstly, the passive integrity of the midcervical spine, as already mentioned in the introductory section, seems to be compromised in a subgroup of patients with chronic WAD. Secondly, the configuration of the multifidus muscle was best revealed at the C4level in asymptomatic subjects. Future studies should correlate the size of the multifidus muscle at different cervical levels to cervical pain and dysfunction. It has been shown that in the lumbar spine the multifidus muscle may become inhibited and atrophied unilaterally at a painful segmental level (Hides et al., 1994; Danneels et al., 2000). The segmental innervation of the multifidus muscle explains this (Macintosh et al., 1986). However, new research indicates that the nerve supply to the zygapophysial joints may control activation of the deep paraspinal muscles (Indahl et al., 1997). As each zygapophysial joint is innervated from the medial branch of the posterior primary rami of three cervical segments (Bogduk, 1982) it is possible that the multifidus muscle at the C4-level may also become inhibited from stimuli one segment above and below. Ultrasonography can be used as a biofeedback at the initial stage of training for the cervical multifidus muscle using a similar procedure to the one established for the lumbar multifidus (Richardson et al., 1999). Physiotherapists are encouraged to conduct more research into this field which will help them to relate observed changes in the size of the cervical multifidus muscle to dysfunctional states and help them to better direct successful treatment interventions.

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5. Conclusion Therapists can use ultrasonography to depict the size of the cervical multifidus muscle at the C4-level by following a strict measurement protocol. The lack of agreement for the symptomatic group in this study was due to loss of clarity of the fascial layer between the semispinalis cervicis and the multifidus muscles. This is probably a diagnostic sign of muscle atrophy that can be used as an indicator of whether treatment interventions are successful in building up the size of the cervical multifidus muscle.

Acknowledgements The author would like to thank radiologist Pa! lmar Hallgr!ımsson for his participation in this study and Sandra Eaton M.A., M.Ed. for grammatical corrections to the manuscript.

References Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986; 1(8476):307–10. Bogduk N. The clinical anatomy of the cervical dorsal rami. Spine 1982;7:319–30. Boyd-Clark LC, Briggs CA, Galea MP. Comparative histochemical composition of muscle fibres in a pre- and a postvertebral muscle of the cervical spine. Journal of Anatomy 2001;199:709–16. Boyd-Clark LC, Briggs CA, Galea MP. Muscle spindle distribution, morphology, and density in longus colli and multifidus muscle of the cervical spine. Spine 2002;27:694–701. Conley MS, Meyer RA, Bloomberg JJ, Feeback DL, Dudley GA. Noninvasive analysis of human neck muscle function. Spine 1995;20:2505–12. Danneels LA, Vanderstraeten GG, Cambier DC, Witvrouw EE, De Cuyper HJ. CT imaging of trunk muscles in chronic low back pain patients and healthy control subjects. European Spine Journal 2000;9:266–72. Emshoff R, Bertram S, Strobl H. Ultrasonographic cross-sectional characteristics of the head and neck. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endotontics 1999;87:93–106. Harcke HT, Grissom LE, Finkelstein MS. Evaluation of the musculoskeletal system with sonography. American Journal of Roentgenology 1988;150:1253–61. Hides JA, Richardson CA, Jull GA. Magnetic resonance imaging and ultrasonography of the lumbar multifidus muscle. Spine 1995;20: 54–8. Hides JA, Stokes MJ, Saide M, Jull GA, Cooper DH. Evidence of lumbar multifidus wasting ipsilateral to symptoms in patients with acute/subacute low back pain. Spine 1994;19:165–72. Indahl A, Kaigle AM, Reikeras O, Holm SH. Interaction between the porcine lumbar intervertebral disc, zygapohysial joints, and paraspinal muscles. Spine 1997;22:2834–40. . Ingelmark B-E. Uber schmertzhafte Insuffizientzzust.ande im Halse. Acta Medica Scandinavica 1942;111:172–89. Kelly SJ, Stokes MJ. Symmetry of anterior tibial muscle size measured by real—time ultrasound imaging in young females. Clinical Rehabilitation 1993;7:222–8.

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! Kristjansson E, Jonsson Jr H. Is the sagittal configuration of the cervical spine changed in women with chronic whiplash syndrome? Journal of Manipulative and Physiological Therapeutics 2002;25: 550–5. Kristjansson E, Leivseth G, Brinckmann P, Frobin W. Increased sagittal plane segmental motion in the lower cervical spine in women with chronic whiplash associated disorders, grades I–II. Spine 2003; in press. Leak AM, Cooper J, Dyer S, Williams KA, Stokes LT, Frank AO. The Northwick Park neck pain questionnaire, devised to measure neck pain and disability. British Journal of Rheumatology 1994;33: 469–74. Macintosh JE, Valencia F, Bogduk N, Munro RR. The morphology of the lumbar multifidus muscle. Clinical Biomechanics 1986;1: 196–204. Mayoux-Benhamou MA, Revel M, Vall!ee C, Roudier R, Barbet JP, Bargy F. Longus colli has a postural function on cervical curvature. Surgical and Radiologic Anatomy 1994;16:367–71. Rezasoltani A, Kallinen M, M.alki.a E, Vihko V. Ultrasonography of the neck splenius capitis muscle. Acta Radiologica 1996;37:647–50. Rezasoltani A, Kallinen M, M.alki.a E, Vihko V. Neck semispinalis capitis muscle size in sitting and prone positions measured

by real-time ultrasonography. Clinical Rehabilitation 1998;12: 36–44. Rezasoltani A, M.alk.a E, Vihko V. Neck muscle ultrasonography of male weight-lifters, wrestlers and controls. Scandinavian Journal of Medicine and Science in Sports 1999;9:214–8. Rezasoltani A, Ylinen J, Vihko V. Isometric cervical extension force and dimensions of semispinalis capitis muscle. Journal of Rehabilitation Research and Development 2002;39:423–8. Richardson C, Jull G, Hodges P, Hides J. Therapeutic exercise for spinal segmental stabilization in low back pain. Edinburgh: Churchill Livingstone, 1999; p. 105–43. . . Sjolander P, Johansson H, Djupsjobacka M. Spinal and supraspinal effects of activity in ligament afferents. Journal of Electromyography and Kinesilogy 2002;12:167–76. Spitzer WO, Skovron ML, Salmi LR, Cassidy JD, Duranceau J, Suissa S, Zeiss E. Scientific monograph of the Quebec task force on whiplash-associated disorders: redefining ‘‘whiplash’’ and its management. Spine 1995;20(Suppl.):1–73. Stokes M, Young A. Measurement of quadriceps cross-sectional area by ultrasonography: a description of the technique and its application in physiotherapy. Physiotherapy Practice 1986;2: 31–6.

ARTICLE IN PRESS



Original article

Impairment in the cervical flexors: a comparison of whiplash and insidious onset neck pain patients G. Julla,*, E. Kristjanssonb, P. Dall’Albaa a

Department of Physiotherapy, The University of Queensland, Queensland 4072, Australia b The Faculty of Medicine, The University of Iceland, Reykjav!ık, Iceland

Received 22 August 2002; received in revised form 20 June 2003; accepted 30 June 2003

Abstract There has been little investigation into whether or not differences exist in the nature of physical impairment associated with neck pain of whiplash and insidious origin. This study examined the neck flexor synergy during performance of the cranio-cervical flexion test, a test targeting the action of the deep neck flexors. Seventy-five volunteer subjects participated in this study and were equally divided between Group 1, asymptomatic control subjects, Group 2, subjects with insidious onset neck pain and Group 3, subjects with neck pain following a whiplash injury. The cranio-cervical flexion test was performed in five progressive stages of increasing cranio-cervical flexion range. Subjects’ performance was guided by feedback from a pressure sensor inserted behind the neck which monitored the slight flattening of the cervical lordosis which occurs with the contraction of longus colli. Myoelectric signals (EMG) were detected from the muscles during performance of the test. The results indicated that both the insidious onset neck pain and whiplash groups had higher measures of EMG signal amplitude (normalized root mean square) in the sternocleidomastoid during each stage of the test compared to the control subjects (all Po0.05) and had significantly greater shortfalls from the pressure targets in the test stages (Po0.05). No significant differences were evident between the neck pain groups in either parameter indicating that this physical impairment in the neck flexor synergy is common to neck pain of both whiplash and insidious origin. r 2003 Elsevier Ltd. All rights reserved. Keywords: Neck flexors; Whiplash; Neck pain

1. Introduction Neck pain is a common condition causing substantial # e! et al., 1998; Holmpersonal and financial costs (Cot strom et al., 1992). Broadly, onset may be insidious or may follow trauma. Pain is often persistent or recurrent in nature. Neck pain of traumatic origin following a motor vehicle crash (whiplash) often poses a particular challenge in management. There are several influences that may impact on the perception of neck pain and disability in persons with whiplash associated disorders (WAD) compared to those with an insidious onset of neck pain. These include the magnitude of the injury, psychological responses to injury and pain, social # e! et al., 2001; Radanov and factors and litigation (Cot *Corresponding author. Tel.: +61-7-3365-2275; fax: +61-7-33652775. E-mail address: [email protected] (G. Jull). 1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1356-689X(03)00086-9

Sturzenegger, 1996). There has been little investigation into whether or not differences exist in the nature of physical impairment associated with neck pain of whiplash and insidious origins which may contribute to the greater difficulty often encountered in the rehabilitation of patients with WAD. Changes in cervical flexor muscle function have been investigated in neck disorders of both whiplash and insidious origins. Vernon et al. (1992) in an initial comparative study of neck isometric strength and flexor/ extensor strength ratios, found that subjects with both WAD and insidious onset neck pain had lesser strength than asymptomatic subjects. There was a progressive anterior-to-posterior muscle imbalance in the neck pain subjects, with the cervical flexors becoming relatively weaker as compared to the extensors. This was more apparent in subjects with WAD, suggesting that there could be a difference in the degree of impairment between these subject groups.

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Cervical flexor muscle function has also been examined using the cranio-cervical flexion test (C-CFT) (Jull, 2000). The cranio-cervical movement aims to assess the anatomical action of longus capitis in synergy with longus colli, rather than that of the superficial flexors, sternocleidomastoid (SCM) and anterior scalene muscles, which flex the neck but not the head. The longus colli muscle has a unique role in the support of the cervical segments and curve (Mayoux-Benhamou et al., 1994). In the C-CFT, the subject performs five increments of increasingly inner range cranio-cervical flexion in a supine lying position (Falla et al., 2003a; Jull, 2000). Patients are guided to the test level by feedback from a pressure unit (Stabilizer, Chattanooga, USA) which is placed behind the neck to monitor the progressive flattening of the cervical lordosis which results from the contraction of longus colli (Mayoux-Benhamou et al., 1994, 1997). Performance in the test has been examined in subjects with WAD (Jull, 2000) and cervicogenic headache (Jull et al., 1999). The results of these studies indicated that patients were less able to achieve and hold the progressive positions of the test as compared to the respective control subjects. These results inferred dysfunction in the deep neck flexors, as no direct measure of these muscles could be made. In the study of subjects with WAD (Jull, 2000) and in a study of patients with chronic neck pain (Sterling et al., 2001), amplitudes of muscle signals (electromyography, EMG) were measured in the sternocleidomastoid (SCM) during the test, following Cholewicki et al.’s (1997) hypothesis that increased activity of the superficial muscles could be a measurable compensation for poor segmental stability, or in this case of the C-CFT, poorer activation of the longus colli. It was shown that both neck pain patient groups had higher amplitudes of muscle signals in the SCM. There has not been a direct comparison of performance in the C-CFT between patients with neck pain from whiplash and insidious origin. This study was undertaken to make this comparison. A clinically applicable version of the C-CFT was used.

neck pain subjects were eligible provided that their condition had not been caused by trauma from a motor vehicle crash. Subjects with WAD (Group 3) were those attending for assessment at a Whiplash Research Unit. Subjects for Groups 2 and 3 were not considered if they had a history of neck surgery, previous diseases affecting the neck or throat, and rheumatic or neurological disorders. Ethical clearance for the study was obtained from the Medical Ethics Committee, The University of Queensland, and all subjects gave informed consent to participate in the study. 2.2. Instrumentation and measurements For Groups 2 and 3, data were collected regarding the length of history of neck pain and subjects rated their average pain intensity on a visual analogue scale (VAS), anchored with ‘no pain’ and ‘the worst pain imaginable’. 2.2.1. Cranio-cervical flexion test The subjects were positioned in a supine lying position. The pressure sensor was inserted between the testing surface and the back of the neck and was preinflated to a baseline of 20 mmHg (Fig. 1). Subjects were asked to perform progressive repetitions of craniocervical flexion to increase the pressure by 2 mmHg incremental targets from 22 mmHg to a maximum of 30 mmHg. Each target pressure was held for 5 s with a 10 s rest between each task. The pressure sensor was connected to a pressure transducer (RS components) and electrical signals from the pressure transducer were amplified and relayed to a visual feedback device and to an Amlab data acquisition system (Associated Measurements Pty Ltd, Australia). The visual feedback device consisted of an electronic voltmeter, marked in 2 mmHg increments from 20 to 30 mmHg, and calibrated to

2. Methods 2.1. Subjects Seventy-five volunteer subjects between the ages of 18–66 years were enrolled in the study. They comprised three groups, each of 25 subjects. Control subjects (Group 1) and insidious onset neck pain subjects (Group 2) were volunteers from the general and university communities who responded to advertising. The control subjects were eligible for the study provided they had no current or past history of musculoskeletal pain or injury in the neck or upper limb. Insidious onset

Fig. 1. The cranio-cervical flexion test demonstrating the visual feedback with the pressure sensor and measurement with surface EMG.

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display the pressure in the pressure bag, based on the pressure transducer output. Sampling frequency for pressure measures was 1000 Hz. The mean pressure that each subject achieved over the 5 s holding time of the five test levels was calculated to determine whether subjects had reached each prescribed level of the test. The differences between the mean pressure achieved and the nominated target pressure for each stage were calculated for each group. Myoelectric signals were collected from the SCM muscles using Ag–AgCl electrodes (Conmed, USA) in a bipolar configuration. Electrodes were positioned along the lower one-third of the muscle bellies of the SCM (Falla et al., 2002). Signals were amplified (Amlab), and passed through a 20–500 Hz bandwidth filter. They were sampled at 1000 Hz. EMG data (amplitude of the signal) were analysed off-line (Matlab). The maximum root mean squared (RMS) value was identified for each trace using a 1 s sliding window, incremented in 100 ms steps. RMS values were normalized for each subject, by dividing the 1 s maximum RMS from each level of the cranio-cervical flexion test by the 1 s maximum RMS during a standardized head lift. The normalized RMS data for the left and right SCMs were averaged for analysis.

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stage to capture the 5 s holding time. Subjects then rested for 10 s. With a similar procedure, the subject sequentially targeted the other four levels of the test to the maximum of 30 mmHg. 2.4. Statistical analysis The analysis of the SCM RMS values required a log transformation to remove the skewness in the original measure. A saturated design model was fitted initially and non-significant terms were removed. A mixed model ANOVA was used to investigate within and between group differences in the normalized RMS values for the SCM muscles for the factors of age, gender and stages of the C-CFT. Boxplots of the pressure data indicated possible differences in the means for the shortfall in pressures from the designated pressure levels of the C-CFT across groups and pressure levels. Variances between measurements within groups indicated that models needed to include terms for this heteroscedacity. The linear effects model used to model target pressure error included specific variance functions modelling variance as a power of the pressure level covariate.

3. Results 2.3. Procedure Subjects received written and verbal information about test procedures and informed consent was obtained. Demographic details were obtained from all subjects and the neck pain subjects rated their pain on the VAS. Subjects were positioned in supine lying with the head and neck in a mid position such that the face line was horizontal and an imaginary horizontal line bisected the neck longitudinally. If necessary, layers of towel were placed under the head to gain the position. Subjects were fully familiarized with the C-CFT by the researcher who was skilled in the clinical test procedure. They participated in a practice session with the pressure biofeedback during which time the researcher corrected performance. EMG electrodes were applied over the lower onethird of the SCM following skin preparation involving mild abrasion with fine sandpaper and cleaning with an isopropyl alcohol swab. The subject was first required to perform a head lift by tucking their chin in and lifting the head to just clear the bed. A 10 s recording was made for later normalization procedures. The pressure bag was placed behind the subject’s cervical spine and inflated until a stable pressure of 20 mmHg was achieved. The researcher instructed the subject to perform the C-CFT to target 22 mmHg and hold the position steady. A research assistant operated the computer system. A 10 s recording was made for each

The demographic details for each subject group as well as the length of history and VAS scores for the neck pain groups are presented in Table 1. The only obvious difference between the groups was the length of history of the insidious onset neck pain group compared to the whiplash group. The results of primary analyses for SCM normalized RMS values revealed significant differences between groups ðP ¼ 0:001Þ and stages of the test ðP ¼ 0:001Þ: There were no significant effects for gender ðP ¼ 0:51Þ or age ðP ¼ 0:62Þ: The analysis revealed a strong positive linear relationship between SCM normalized RMS values and stage of the C-CFT, but the relationship levelled off for the whiplash group at the highest pressure target (Fig. 2). Both the neck pain and whiplash groups had significantly higher SCM normalized RMS values than the control group at each stage of the C-CFT (all Po0:05). However there were no significant differences in SCM normalized RMS

Table 1 Characteristics of the subject groups

Gender (females %) Age (years, mean7SD) Length of history (years) Average pain (VAS 0–10)

Controls ðn ¼ 25Þ

Neck pain ðn ¼ 25Þ

Whiplash ðn ¼ 25Þ

60 39.3714.0 — —

80 40.379.2 8.576.0 6.371.5

68 36.3710.2 1.871.1 6.272.3


92 0.9 0.8

Controls Neck Pain

Normalised RMS

0.7

Whiplash

0.6 0.5 0.4 0.3 0.2 0.1 0

22mmHg

24mmHg

26mmHg

28mmHg

30mmHg

Test stages

Fig. 2. The means (se) for the normalized RMS values for sternocleidomastoid in each stage of the cranio-cervical flexion test for control, insidious onset neck pain and whiplash groups.

3.5

Pressure shortfalls mmHg

3

Controls 2.5

Neck Pain Whiplash

2

1.5

1

0.5

0

22mmHg

24mmHg

26mmHG

28mmHg

30mmHg

Test stages

Fig. 3. The means (se) for the shortfall in pressure from the target pressures for each stage of the cranio-cervical flexion test for control, insidious onset neck pain and whiplash groups.

values between the neck pain and whiplash groups with the exception of the 22 mmHg stage ðP ¼ 0:02Þ: The analysis was repeated for the insidious onset neck pain and whiplash groups using length of history of neck pain as a covariate and results remained unchanged. The differences between the target pressure and the mean pressure achieved for each stage of the test for each group are presented in Fig. 3. Within the test stages, the mean shortfalls in pressure for the neck pain and whiplash groups were not significantly different at any stage of the test ðP > 0:05Þ; but those of both groups were significantly greater than the control group ðPo0:002Þ: The exception was at the 22 mmHg target where the mean for the neck pain group was not significantly different from the control group ðP ¼ 0:11Þ:

4. Discussion Dysfunction in the neck flexor muscles has been found to be associated with neck pain of both whiplash

and insidious origins (Jull et al., 1999, 2000; Sterling et al., 2001; Vernon et al., 1992; Watson and Trott, 1993). However there has been little investigation into whether or not differences exist between the groups which might impact on the rehabilitation process. The results of this study revealed a strong linear relationship between the magnitude of the SCM normalized RMS values and each progressive stage of the test for all groups but there were higher levels of SCM normalized RMS values in the neck pain and whiplash groups in all stages of the C-CFT compared to the asymptomatic control group. This is in accord with the findings of previous studies of subjects with WAD and insidious onset neck pain (Jull, 2000; Sterling et al., 2001). No significant differences were evident between the neck pain and WAD groups indicating that this physical impairment or altered pattern of muscle coordination is common to neck pain of both whiplash and insidious origin and would not seem to be a reason why patients with chronic WAD often are more challenging to treat than patients with insidious origin neck pain. Cranio-cervical flexion is the action of longus capitis in synergy with longus colli. The presence of progressively increasing SCM normalized RMS values in each test stage in all subject groups suggests that these muscles were recruited to further stabilize the neck as the contractile demand of the longus capitis increased in the inner ranges of cranio-cervical flexion. The presence of higher SCM normalized RMS values in the neck pain groups infers that altered patterns of co-ordination may be present between the deep and superficial flexor muscles in patients with neck pain, and this higher activity may be a measurable compensation (Cholewicki et al., 1997) for poorer active contractile capacity of the longus colli and capitis muscles. The clinical version of the C-CFT used in this study has the deficit of no direct measure of the activity of longus capitis and colli. The muscles are deep and not accessible for use of conventional surface EMG. Falla et al. (2003b) used a novel surface EMG electrode in a laboratory version of the C-CFT. A bipolar surface electrode was inbuilt into a nasopharageal suction catheter and the electrode was inserted via the nasal passage and suctioned onto the back of the throat adjacent to the uvula, over the longus capitis and colli. In their study on asymptomatic subjects, they demonstrated a stronger linear relationship between the amplitude of the deep neck flexor muscle signal and the increasing incremental stages of the test, which confirms anatomical predictions for the test. In a further study of 10 neck pain and 10 control subjects, Falla et al. (2003c) again demonstrated a strong linear relationship between the EMG amplitude of the deep neck flexor muscles and the incremental stages of the C-CFT for both control and neck pain subjects. However, the amplitude of deep neck flexor


EMG was less in the neck pain group than for the control group and the difference was significant for the higher levels of the test. Although not significant, there was a strong trend for greater EMG activity in the SCM and anterior scalene muscles in the neck pain group. These findings lend support to the contention that the higher levels of SCM normalized RMS values measured in all stages of the C-CFT in our study of neck pain patients as compared to the control subjects may reflect a compensation strategy for poorer contractile capacity of the deep cervical flexors. Further study on larger sample sizes to better understand the compensation strategies in the C-CFT as well as their sensitivity and specificity to neck pain patients is warranted. The pressure unit, which is inserted behind the neck in the C-CFT, monitors the slight flattening of the cervical spine accompanying the contraction of the longus colli (Mayoux-Benhamou et al., 1994). The results of the differences between the pressure target and that attained by the subjects in this study revealed that the control group could quite accurately perform and control the cranio-cervical flexion action to the designated pressures of each task (Fig. 3). In contrast, both neck pain groups demonstrated larger pressure shortfalls at all stages of the C-CFT. This again would infer poorer active contractile capacity of the longus colli to flatten the cervical curve, particularly in the latter three stages of the test. At the 30 mmHg stage of the test, the WAD group had a particularly large shortfall indicating that many of the subjects could not perform this stage of the test. This was associated with a levelling off of the EMG normalized RMS values in the WAD group at the test stage. Thus the results of the study show that the neck pain groups of both insidious and whiplash origin have difficulty attaining the pressure targets of the test and in association they both exhibit higher normalized RMS values in the SCM, indicating similar impairment in the neck flexor synergy. The neck pain groups were of similar age and gender and reported similar levels of pain associated with their condition, although the insidious onset neck pain group had a longer history of their condition than the whiplash group. These differences in length of history did not impact on results. Similar findings of the lack of effect of length of history were reported by Nederhand et al. (2002) in their study of muscle activation patterns of upper trapezius in patients with WAD (mean length of history 1:771:3 years) and patients with chronic nonspecific neck pain (6:775:6 years). These authors concluded that cervical muscle dysfunction was apparently not related to a specific traumatic injury as was also found in this study. Thus these changes in muscle function appear not to be time dependent beyond a certain point and the common factor may be the presence of pain.

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5. Conclusion This study has determined that altered patterns muscle co-ordination within the neck flexor synergy are present in patients with neck pain of whiplash and insidious origin as evident in the C-CFT. It appears that this physical impairment between the two groups is similar and of itself would not account for the greater difficulty often encountered in the rehabilitation of patients following whiplash.

Acknowledgements The authors acknowledge the financial support for this research from the Centre of National Research on Disability and Rehabilitation Medicine (CONROD, Queensland, Australia) and from the Association of Icelandic Insurance Companies.

References Cholewicki J, Panjabi MM, Khachatryan A. Stabilizing function of the trunk flexor-extensor muscles around a neutral spine. Spine 1997;22:2207–12. # e P, Cassidy JD, Carrol L. The Saskatchewan health and back pain Cot! survey: the prevalence of neck pain and related disability in Saskatchewan adults. Spine 1998;23:1689–98. # e P, Cassidy D, Carroll L, Frank J, Bombardier C. A systematic Cot! review of the prognosis of acute whiplash and a new conceptual framework to synthesize the literature. Spine 2001;26:E445. Falla D, Dall’Alba P, Rianoldi 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;113:57–63. Falla D, Campbell C, Fagan A, Thompson D, Jull G. An investigation of the relationship between upper cervical flexion range of motion and pressure change during the cranio-cervical flexion test. Manual Therapy 2003a;8:92–6. Falla D, Jull G, Dall’Alba P, Rianoldi A, Merletti R. An electromyographic analysis of the deep cervical flexor muscles in performance of cranio-cervical flexion. Physical Therapy 2003b; accepted for publication. Falla D, Jull G, Hodges P. Neck pain patients demonstrate reduced EMG activity of the deep cervical flexor muscles during performance of cranio-cervical flexion. 2003c; submitted for publication. Holmstrom EB, Lindell J, Moritz U. Low back and neck/shoulder pain in construction workers: Occupational workload and psychosocial risk factors: Part 2 relationship to neck and shoulder pain. Spine 1992;17:672–7. Jull GA. Deep cervical neck flexor dysfunction in whiplash. Journal of Musculoskeletal Pain 2000;8:143–54. Jull G, Barrett C, Magee R, Ho P. Further characterisation of muscle dysfunction in cervical headache. Cephalalgia 1999;19:179–85. Mayoux-Benhamou MA, Revel M, Vallee C, Roudier R, Barbet JP, Bargy F. Longus colli has a postural function on cervical curvature. Surgical Radiologic Anatomy 1994;16:367–71. Mayoux-Benhamou MA, Revel M, Vallee C. Selective electromyography of dorsal neck muscles in humans. Experimental Brain Research 1997;113:353–60.

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Nederhand MJ, Hermens HJ, Ijzerman MJ, Turk DC, Zivold G. Cervical muscle dysfunction in chronic whiplash-associated disorder grade 2: the relevance of the trauma. Spine 2002;27:1056–61. Radanov B, Sturzenegger M. Predicting recovery from common whiplash. European Neurology 1996;36:48–51. Sterling M, Jull G, Wright A. Cervical mobilisation: Concurrent effects on pain, motor function and sympathetic nervous system activity. Manual Therapy 2001;6:72–81.

Vernon HT, Aker P, Aramenko M, Battershill D, Alepin A, Penner T. Evaluation of neck muscle strength with a modified sphygmomanometer dynamometer: reliability and validity. The Journal of Manipulative and Physiological Therapeutics 1992;15:343–9. Watson DH, Trott PH. Cervical headache: an investigation of natural head posture and upper cervical flexor muscle performance. Cephalalgia 1993;13:272–84.

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Professional issue

Pre-manipulative testing of the cervical spine review, revision and new clinical guidelines Mary E. Magareya,*, Trudy Rebbeckb, Brian Coughlanc,1, Karen Grimmera, Darren A. Rivettd, Kathryn Refshaugee a

Centre for Allied Health Evidence (A Collaborating Centre for the Joanna Briggs Institute), Discipline of Physiotherapy, School of Health Sciences, University of South Australia, North Terrace, Adelaide 5000, South Australia, Australia b School of Physiotherapy, University of Sydney, Australia c Bayside Physiotherapy, 459A Main Street, Mordialloc, VIc 3195, Australia d Discipline of Physiotherapy, Faculty of Health, The University of Newcastle, Callaghan NSW 2308, Australia e School of Physiotherapy, Faculty of Health Sciences, The University of Sydney, East St. Lidcombe, NSW, Australia Received 20 January 2003; received in revised form 24 October 2003; accepted 3 December 2003

Abstract Members of the Manipulative Physiotherapists Association of Australia (now Musculoskeletal Physiotherapy Australia) were surveyed to determine their use of cervical manipulation, compliance with and attitudes to the Australian Physiotherapy Association’s (APA) Protocol for Pre-manipulative Testing of the Cervical Spine, and the incidence of adverse effects from cervical manipulation. The questionnaire was mailed to 740 members and returned by 480 members (65%). Cervical manipulation (84.5%) and passive mobilization (99.8%) were used by a high percentage of respondents. Most were familiar with the protocol with 63% supporting its continued endorsement. Adverse effects were reported at a rate of one per 1000 years of practice (or 0.003/week). The most common effects were symptoms potentially related to VBI (94.4% responses), with no reported major complications. Only 37.1% of respondents always informed the patient about potential dangers of cervical manipulation and consent was sought on every occasion by 33% of respondents. The results suggest that the use and interpretation of the protocol are variable among members of MPA. The risk of adverse effects from manipulative (musculoskeletal) physiotherapy practice, including cervical manipulation, appears to be very low. Recommendations for revision of the protocol were made on the basis of results of the survey and treatment diary, in addition to a review of the literature related to testing for vertebro-basilar insufficiency, adverse incidents related to cervical mobilizing and manipulative technique, differentiating features of VBI related dizzinesss and vertigo related to benign paroxysmal positional vertigo (BPPV) and current issues surrounding informed consent. Finally, a summary of the content of the new Clinical Guidelines for PreManipulative Testing of the Cervical Spine (APA, 2000) is provided. r 2003 Elsevier Ltd. All rights reserved.

1. Introduction The Australian Physiotherapy Association (APA) endorsed the APA Protocol for Pre-Manipulative Testing of the Cervical Spine in, 1988, mandating it for use prior to manipulation of the cervical spine (APA, *Corresponding author. Division of Health Sciences, School of Health Sciences, University of South Australia, North Terrace, Adelaide S.A. 5153, Australia. Tel.: +61-8-8302-2768; fax: +61-88302-2766. E-mail address: [email protected] (M.E. Magarey). 1 On behalf o Musculoskeletal Physiotherapy Australia, National APA Office, PO Box 6465, St. Kilda Road Central, Victoria 8008, Australia. 1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2003.12.002

1988). Over the past decade, advances in research (Grant and Trott, 1991; Refshauge, 1994; Rivett and Milburn, 1996; Rivett et al., 1999; Johnson et al., 2000; Zaina et al., 2003), and changes in the medico-legal system in Australia (Rogers v Whitaker, 1992) have fuelled discussion regarding the validity of the protocol (for example, Grant and Trott, 1991; Rivett, 1995; Grant, 1996a, b). Concerns expressed anecdotally and as part of an APA review included: *

*

The time consuming nature of applying the protocol (Grant, 1994). The provocative nature of the tests themselves (Di Fabio, 1999).

ARTICLE IN PRESS M.E. Magarey et al. / Manual Therapy 9 (2004) 95–108

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The reliability and validity of the test procedures, questioning whether they actually detect alterations in blood flow in the vertebro-basilar system (Assendelft et al., 1996). The lack of validated research underpinning the protocol (Kunnasmaa and Thiel, 1994). Failure to address the legal requirements pertaining to the provision of informed consent.

in writing that they did not wish to participate—their reasons were not recorded (65%). The diary was completed by 287 members (38.7%). The diary was not linked by identification number to the attitudinal survey, and thus represented an independent set of responses.

In response to the expressed opinions, an attitudinal survey and treatment diary were mailed to all members of the Manipulative Physiotherapists’ Association of Australia (now Musculoskeletal Physiotherapy Australia—MPA). The aims of the study were:

Cervical spine HVT techniques were used by 84.5% of currently practising respondents (n ¼ 419), in the upper, middle and lower cervical spine, by 83.4%, 84.7% and 98.3% of respondents, respectively. Of the 287 respondents to the diary, 34.8% performed upper cervical spine HVT techniques and 41.8% performed lower cervical spine HVT techniques in the recording week. We assumed that the physiotherapists who reported using upper and lower cervical manipulations were not mutually exclusive, and we took the higher figure (41.8% respondents used HVT in the cervical spine) to include those who also undertook upper cervical HVTs. Thus, overall, 41.8% used HVTs on the cervical spine. A total of 1002 HVT techniques was performed in the cervical spine by 141 physiotherapists in the diary week using a variety of manipulative techniques. This is an average HVT technique rate of 3.5 manipulations per diary respondent per week. Specific HVT techniques commonly included lateral flexion, longitudinal, postero-anterior (PA) thrust, transverse and rotary techniques.

*

*

*

1. To determine the proportion of members using cervical manipulation (high velocity thrust [HVT] techniques) and the frequency of their use in each region of the cervical spine. 2. To determine the proportion of members using nonthrust techniques (passive mobilization) and cervical traction in each region of the cervical spine. 3. To determine the members’ opinions of, and rate of compliance with, the APA Protocol for Pre-Manipulative Testing of the Cervical Spine. 4. To quantify adverse effects associated with the use of cervical manipulation and other cervical spine procedures. 5. To determine the rate of compliance with the legal requirement to provide information to, and obtain consent from, a patient prior to the use of cervical manipulation.

2. Methods Following granting of ethical approval from the University of South Australia Human Research Ethics Committee, a sample survey was reviewed by a focus group in one Chapter, revised and then trialed in three Chapters of MPA. The survey questions contained multiple set response options plus free text opportunities to express opinions. After revision following this process, a final questionnaire was developed and sent to all 740 members. In addition to the survey, members were requested to prospectively record their use of cervical manipulative techniques and the protocol for one week of clinical practice in a daily diary. Responses to both the survey and diary were anonymous.

3.1. Use of HVT techniques

3.2. Use of non-thrust (passive mobilization) techniques From the survey, passive mobilization (non-thrust) techniques were used by nearly all respondents (99.8%), who applied them on average to 90.4% of their cervical patients. Respondents used a variety of passive mobilization techniques with similar frequency in the upper, middle and lower cervical spine (96.8%, 96.7% and 96.6%, respectively). Cervical traction was used by 94.9% respondents. To determine the most commonly applied HVT and non-thrust techniques, the diary data were used (actual numbers of applications of most commonly used techniques over a standard [1 week] time frame). These figures show that the most commonly practised technique in each region of the cervical spine, and overall, was the passive accessory intervertebral movement (PAIVM). 3.3. Familiarity with the protocol

3. Results The attitudinal survey was returned by 419 members in current clinical practice and 34 members not in current clinical practice. A further 27 members indicated

Ninety-eight per cent of respondents were familiar with the protocol and 85% had read it within the last 4 years. The most common reason for using the protocol was concern that the proposed treatment technique


would stress the vertebro-basilar arterial system. Most respondents (67.4%) considered the protocol valuable in their manipulative/musculoskeletal physiotherapy practice, although 14.2% used it only to satisfy legal requirements. The majority of respondents (63%) supported continued endorsement of the protocol, 25% were unsure, leaving only 12% who definitely felt that endorsement should not be continued. Seventy-five per cent indicated that the protocol was useful to them for other than medico-legal reasons, and 70% would continue to use it even if it were no longer endorsed. About half of the respondents (54.2%) felt that use of the protocol gave them a sense of security prior to the use of HVT techniques, despite being aware of the limitations of the physical test procedures. The respondents who indicated that the APA should not endorse the use of the protocol (n ¼ 54) raised the following issues about its use: *

* *

*

*

It is not clinically relevant (20.3% of this group of respondents). It does not identify patients at risk (37.7%). It places unnecessary restrictions on the use of cervical manipulation (21.9%). It discourages physiotherapists from using cervical manipulation (50%). It places an onerous legal burden on physiotherapists (37.9%).

to the patient’s response, although the majority of techniques contained a component of rotation. Of these respondents, 40% had applied the protocol prior to treatment. Of the patients who had suffered an adverse reaction and for whom the protocol had not been applied, 45% had features for which use of the protocol was indicated. The incidence rate for adverse effects (which is an estimate, as a result of amalgamation of categories of 2–10 and 10+ complications) translates to 168.5 per 1000 manipulative/musculoskeletal physiotherapy years of practice (or 0.003/week). This was calculated by determining the time over which the 447 respondents had practised manipulative/musculoskeletal physiotherapy (average 10.2 years (SD 6.4, range 1–31, median 9), with a sample total of 4601 physiotherapist years of manipulative/musculoskeletal practice, coupled with the estimated number of adverse effects (ever) as reported by this sample. Information on 291 types of effects within the past 2 years was obtained from 211 survey responders (46.6%). Calculations were performed for the rate of adverse effects for HVT, passive physiological intervertebral movements (PPIVMs), PAIVMs, cervical traction and other cervical treatments. Adverse effects were found to occur at a rate of: * *

From the text responses, further comments were noted: * *

*

The time cost of applying the protocol is unrealistic. The questionable validity of the tests themselves and the provocative nature of the protocol tests are of concern. The requirement to provide information and ask for consent prior to use of HVT techniques acts as a deterrent, leading to reluctance on the part of the therapist to request consent and on the part of the patient to provide such consent.

3.4. Adverse effects Adverse effects associated with examination or treatment of the cervical spine were recalled by 447 respondents at some time in their professional career (400 currently practising and 47 not in current practice). The remainder of respondents recalled no adverse effects associated with examination or management of the cervical spine. Of those patients with adverse effects, 15.9% required medical attention, while the remainder resolved without intervention. The most common effects related to passive mobilizing techniques (27.5%), examination techniques (20.4%) and HVT techniques (16.1%). The majority of respondents (77%) could not identify any features that would have alerted them

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* *

*

One per 177.5 therapist weeks for HVT. One per 184 therapist weeks for PPIVMs. One per 180 therapist weeks for PAIVMs. One per 100 therapist weeks for cervical traction and other cervical techniques. A total of 1.38 adverse effects per therapist over the 2 year period (0.01/week).

The rate for HVT translates into an estimate of one effect per 50,000 HVT procedures. This more specific information supported the low rate of adverse effects associated with cervical techniques. The most common complications were symptoms potentially associated with the vertebro-basilar system (accounting for 94.4% responses) [that is, dizziness, diplopia, dysphagia, drop attacks, difficulty in swallowing, nausea]. Specifically, there were no reported major complications in this sample. 3.5. Information and consent Provision of information to the patient about dangers involved with HVT techniques (other than death) was low. Only 37.1% of respondents to the survey always informed the patient about these dangers and 48.1% sometimes did. Dangers discussed included dizziness (29.1%), nausea (22.5%), radiculopathy (12%), stroke (27.7%) and various other complications (8.5%). Death or permanent disability were specifically included as a


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danger by 23.3% of respondents, while some never mentioned either (16%) and 33.1% only introduced the subject if the patient asked for further information. Of those respondents who did not include information regarding death or disability, 33.7% felt uncomfortable about doing so, 30.3% thought that the patient would refuse HVT techniques as a treatment option, 15.4% considered that it was not relevant and 2.9% believed that it was not legally required. The remainder (17.6%) expressed a variety of reasons regarding lack of information exchange. Consent was rarely gained on every occasion of manipulation. Consent was sought by: *

*

*

32.9% respondents for every HVT technique (including multiple techniques on the one occasion); 33.4% respondents at every occasion at which a HVT technique was used; 20.3% respondents only at the first occasion at which a HVT technique was used.

Consent was never sought by 1.9% respondents and 11.5% respondents did not seek consent with every patient. Seeking consent was always linked to the provision of information about the dangers of manipulative therapy techniques by 40.2% respondents, and sometimes by 49.7% respondents. The remaining 10.1% respondents never linked these two issues.

4. Discussion There was a moderate response from the membership (65%), with 61.2% actually completing the survey, and a poor response to the diary (38.7%). However, it appeared that responses were received from members who had a strong positive or negative opinion or experience regarding the use of the protocol. The intensity of responses suggested that few members took a middle ground. Compliance with completing the diary would have been facilitated by clerical assistance in tallying patient and treatment numbers, thus potentially biasing against respondents without such support. Moreover, the weekly diary may not have been completed by those physiotherapists who used cervical manipulation less than once per week as the diary covered a snapshot of a single week’s practice. No other studies were found in which frequency of use of HVT and non-thrust techniques in a national professional association with specialized training in manipulative/musculoskeletal physiotherapy have been reported. Michaeli (1993), Rivett and Milburn (1996) and Grant and Niere (2000) have all undertaken different studies of manipulative/musculoskeletal physiotherapists or those with manipulative therapy training, but in each case, smaller samples were used. In, 1991, Grant and Trott reviewed compliance with the

protocol using a random sample of 10% of members of the APA (n ¼ 727). A return rate of 63% was reported (n ¼ 455) representing a similar sample size and response rate to the present study. However, in Grant and Trott’s (1991) sample, further reported in Grant (1994, 1996a, b), only 18.5% (n ¼ 84) reported using manipulative techniques, even though manipulative physiotherapy was listed as the field of practice by, 198, a much smaller sample than in the current study. Frequency of use of HVT and non-thrust techniques reflects that anticipated from a sample of members of MPA, with virtually 100% use of non-thrust techniques and 84.5% overall use of HVT techniques. Also as anticipated, a higher percentage of members used HVT techniques in the lower cervical spine than in the middle or upper regions, presumably because of the perception of a lower risk of damage to the VA with techniques applied to this area (Klougart et al., 1996a, b). Compliance with the protocol was poor, with only 66% respondents reporting its implementation prior to the first use of HVT techniques and 33.6% using it prior to subsequent HVT procedures. This result reflects a similar level of compliance reported by Grant and Trott (1991) and represents a less than desirable compliance rate for a protocol mandated by the professional body prior to the administration of cervical manipulation. However, despite the poor compliance, only a small percentage (12%) of respondents definitely did not support endorsement of the protocol. Conversely, 63% definitely supported its continued endorsement and 66.7% believed the protocol was of value to their clinical practice, consistent with the findings of Grant and Trott (1991) who reported 66% endorsement. The objections to protocol use reflected similar concerns expressed in Grant and Trott (1991), including its time consuming nature and the need to obtain informed consent reducing opportunities to undertake HVT procedures. The rate of adverse effects from HVT techniques of the cervical spine (1 per 50,000 manipulations) was very low, with no evidence of catastrophic misadventures. The survey instrument precluded collection of data on the precise number of incidents, particularly as the data were retrospective. However, the results do provide a snapshot of the frequency and nature of incidents that have occurred within a large sample of postgraduate educated users of HVT techniques in the cervical spine. The argument could be made that any therapist who had been involved in a catastrophic incident would remember the incident vividly and would therefore report it accurately. However, the counter argument, that such therapists may have chosen not to respond to the survey, could be equally valid. These limitations are acknowledged and reflected in interpretation of the results of this study.


Interestingly, adverse responses were reported with non-thrust (27.5%) and examination techniques (20.4%) in addition to HVT techniques (16.1%). Techniques associated with the highest frequency of adverse responses were those involving some component of rotation, consistent with previous research (Klougart et al., 1996a, b). Examination techniques included various types of examination procedures—active and passive physiological movements and PAIVMs. In a review of the reported incidence of mishaps related to cervical manipulation, Rivett and Milburn (1996) highlighted the limitations in the information currently available. Estimated rates of mishap varied from less than one in 5,000,000 in a chiropractic study (Jaskoviak, 1980) to one in 50,000 in a medical report (Gutmann, 1981). However, all studies were, like the present one, retrospective with consequent inherent recall bias, and most involved medical practitioners and chiropractors. A single published retrospective study (Michaeli, 1993) of cervical manipulation by physiotherapists was highlighted by Rivett and Milburn (1996). The sample population (n ¼ 88) had only 100 h postgraduate education in manipulative physiotherapy, thus not reflecting the education levels of MPA members—formal postgraduate qualifications in manipulative physiotherapy. However, a risk of minor or transient complications of approximately one in 1756 manipulations was reported. In the present study, the rate of adverse effects from HVT techniques was one in 50,000—considerably lower, perhaps reflecting the higher level of formal manipulative physiotherapy education in the present sample. Rivett and Reid (1998) investigated the incidence of neurovascular insult attributed to cervical manipulation by physiotherapists in New Zealand, reporting at least four cases in a 7 year period (1991–1997). These authors also provided an estimate of the number of cervical manipulations performed by manipulative/musculoskeletal physiotherapists in the same timeframe, calculating an approximate incidence rate of one cerebrovascular accident (CVA) for every 163,371 manipulations. It is impossible to provide direct comparison from this study to the present one, as no CVAs were reported in the present study. Clearly, the results of this study do not provide the answers to the question of incidence of complications because of the limitations of the study design. Until a large prospective study is completed, the risk is likely to continue to be under-estimated. There is increasing emphasis on the teaching of short lever HVT techniques as alternatives to the more traditional techniques (Gross et al., 1996; College of Physical Therapists of Alberta, 2000; Gibbons and Tehan, 2000; Monaghan, 2000; Hing et al., 2003). These techniques are perceived to place less end-range rotary stress on the upper cervical spine. Continuation of this

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direction of teaching would appear to be appropriate at this stage in light of the findings of the present study. Following review of the results of the survey, the following changes were recommended: *

*

*

*

Review and modification of the protocol in the light of the most recent research available on the effect of cervical movement on blood flow in the vertebrobasilar system and its relation to provocation of symptoms. Shortening and simplification of the protocol for use with cervical manipulation and techniques involving end-range rotation of the cervical spine. Facilitation of the provision of information to patients prior to cervical manipulation. Development of a protocol for provision of information, obtaining consent to cervical manipulation and recording of the process.

To achieve these aims, the following steps were undertaken: *

*

*

*

An extensive review of the literature and evaluation of work in progress was undertaken, related to: * measurement of vertebro-basilar blood flow and the effect on flow of cervical movements; * provocation of symptoms associated with alteration of vertebro-basilar blood flow; * the incidence and possible causes of complications associated with manipulation of the cervical spine; * differentiation of symptoms of VBI from those of other sources. Medico-legal experts and physiotherapists with expertise on informed consent for therapeutic intervention were consulted, to help determine the optimal way to facilitate this process within a clinical practice setting. The structure and content of the protocol were reviewed. A draft set of clinical guidelines for pre-manipulative procedures for the cervical spine was developed and distributed to members of the professional body for comment, focus groups were held throughout the profession and, on the basis of feedback from this process, a new set of clinical guidelines produced.

4.1. The effect of cervical movement on blood flow in the vertebro-basilar system and its relation to provocation of symptoms The effect of cervical movement on VA blood flow has been investigated in vivo using Doppler ultrasound. The findings of these studies are conflicting, leading some researchers to question the validity of pre# e! manipulative testing (Kunnasmaa and Thiel, 1994; Cot

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M.E. Magarey et al. / Manual Therapy 9 (2004) 95–108

Table 1 Studies demonstrating altered flow parameters of the VA Study

Instrumentation and measurements

Sample population

Results

Arnetoli et al. (1989)

Cw Doppler US VA flow in rotation/extension

190 healthy volunteers 60 patients with VBI

Either diastolic flow loss or absent Doppler signal of contralateral VA in 6% of volunteers and 33% of patients

Dan#ek (1989)

Cw Doppler US VA flow in sustained rotation/ extension

25 symptomatic patients

Flow changes in 12 of 25

Stevens (1991)

Cw Doppler US VA flow at C1–C2 during positional testing

250 patients with an identified abnormal flow velocity pattern

Velocity in contralateral rotation reduced in 62%, increased in 20% Decreased flow velocity in extension in 18%

Refshauge (1994)

Duplex US Flow velocity at C2–C3 in 45 & end-range contralateral rotation

20 healthy volunteers

Flow changes (usually increase) in 45 , significant trend for decreased velocity in full rotation 2 subjects had no flow at 45 rotation but no symptoms

Haynes (1996)

Cw Doppler US Maximum contralateral rotation

290VAs

Cessation of Doppler signal in 5%

Rivett et al. (1999)

Colour duplex US Peak systolic & end diastolic velocities & resistance index at C2-C3 in extension, 45 & end-range contralateral rotation & combined rotation/extension

16 patients and 4 volunteers (10 positive, 10 negative to premanipulative testing)

Significant changes in flow velocity in end-range positions of rotation and rotation/extension No meaningful significant differences found between positive and negative subjects

CW=continuous wave; US=ultrasound; VA=vertebral artery; VBI=vertebro-basilar insufficiency.

et al., 1996; Grant, 1996a, b, Johnson et al., 2000). The earlier studies are summarized in Tables 1 and 2. The results of many of these investigations are questionable as preceding reliability studies were not conducted or were, at best, limited in nature (Stevens, 1991; Refshauge, 1994), despite the well-known operator dependency of ultrasonographic examination (Johnson et al., 2000). Vessel identification error and inaccurate sampling due to non-visualization of the target vessel with continuous wave ultrasound and sampling at different parts of the artery, often upstream to the area potentially affected, may also have affected the results of some studies. In response to this problem, Zaina et al. (2003) reported on an investigation of the effect on cervical rotation on VA flow using a reliable experimental protocol proposed by Johnson et al. (2000) and following an initial test–retest reliability study. Neither peak velocity nor volume flow rate was found to be significantly changed in a group of, 20 asymptomatic volunteers at both 45 and end-range contralateral rotation. However, the effects of pre-manipulative testing on a symptomatic population cannot be determined from this small study. In a larger investigation on a patient population, Rivett et al. (2000) evaluated the effects of pre-

manipulative testing on VA haemodynamics and whether these effects differed between patients demonstrating positive and negative clinical test responses. Colour duplex ultrasound with power Doppler imaging was used to measure haemodynamic parameters at C1– C2 during testing. Good reliability was shown (n ¼ 20) for sampling of selected flow parameters at C1–C2 in various cervical positions. Patients were classified as either positive (n ¼ 51) or negative (n ¼ 49) to premanipulative testing, and then underwent an ultrasonographic examination in positions involving rotation and extension. While there were statistically significant haemodynamic changes during pre-manipulative testing, these changes were generally unlikely to be clinically significant. There were no meaningful significant differences in flow changes in any of the cervical positions between the two groups. Notably, 20 patients had total or partial vessel occlusion during testing, however only two of these displayed possible VBI symptoms at the time. It was concluded that pre-manipulative testing alone is clinically unlikely to distinguish between patients with varying degrees of flow impedance. Thus, within our current knowledge and given the apparently questionable clinical value of physical premanipulative testing, it is clear that greater emphasis should be placed on detecting potential indicators of risk


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Table 2 Studies in which no change in VA flow was found Study

Instrumentation and measurements

Sample population

Results

Weingart & Bischoff (1992)

Cw Doppler US Flow velocity at C1in various positions of rotation & extension

30 normal volunteers

No significant changes

Thiel et al. (1994)

Duplex US Flow velocity during sustained (30 sec) extension, rotation & combined extension/rotation

30 control volunteers 12 patients with symptoms &/or signs of VBI on clinical testing

No abnormal flow patterns No meaningful significant differences in mean velocity ratios

# e et al. (1996) Cot! Secondary analysis of data from Thiel et al. (1994)

Duplex US VA flow during extension/rotation testing

30 control volunteers 12 patients with symptoms &/or signs of VBI on clinical testing

For increased impedance to flow: Sensitivity 0% Specificity 67–90%

Licht et al (1998, 1999)

Colour duplex US Contraleral & ipsilateral rotation (45 & end-range) on peak flow velocity

20 healthy university students

Both test positions: * Significant but modest decrease with contralateral rotation * Significant increase with ipsilateral rotation Volume flow data demonstrated no change, therefore hindbrain perfusion unaffected

Haynes & Milne (2000)

Colour duplex US Peak systolic & end diastolic flow velocities at 10 increments of contralateral rotation

20 patients (39 VAs) with neckrelated symptoms

No significant change in group mean flow velocity Marked changes in flow velocities in 7 VAs toward end-range rotation

Licht et al. (2000)

Colour duplex US Peak & mean flow velocities at 45 rotation, end-range rotation & rotation/extension

15 patients with positive premanipulative test response

No significant change in flow velocities of contralateral or ipsilateral arteries in any test position

CW=continuous wave; US=ultrasound; VA=vertebral artery; VBI=vertebro-basilar insufficiency.

in the patient history (Grant, 2002; Rivett, 1995, 1997). It also appears that, often, the symptoms detected during clinical pre-manipulative testing may be unrelated to alterations in blood flow in the VA. 4.2. Differentiation of symptoms of VBI from those of other sources Clinical experience of vestibular rehabilitation physiotherapists indicates that VBI is rare and the majority of patients who present with dizziness do not suffer from VBI (Clements, 2001). Although only anecdotal, this observation may change the perspective on this condition. Some distinction between dizziness/vertigo related to VBI and that from other sources is possible within a clinical examination. Multiple sensory systems contribute to the body’s balance function (Shepard and Telian, 1996). The central nervous system is responsible for integration and modulation of the information required for balance and if integration of input from

the different sources is disrupted, symptoms of disequilibrium may develop. In a pathological situation, visual, vestibular or neurological disease may alter the perception of motion and the environment, as the sensory inputs no longer match those anticipated (Luxon, 1997). Vertebro-basilar insufficiency is evidenced by symptoms of ischaemia of the areas of the brain supplied by the basilar artery—the pons, medulla and cerebellum, in addition to the central and peripheral vestibular system. When investigating clinical features in 84 subjects with vascular origin vertigo, Grad and Baloh (1989) (cited by Clendaniel, 2000) found that vertigo may be an initial isolated symptom of VBI, but its presence without other symptoms associated with posterior circulation ischaemia for greater than 6 months would imply a different cause. Other symptoms are those traditionally screened for in the subjective examination: visual hallucinations (spots in front of the eyes), drop attacks, dysarthria, dysphagia, visual field defects (narrowing of the visual



field), diplopia, visceral sensations (nausea with or without vomiting) and headaches. Benign Paroxysmal Positional Vertigo (BPPV) is the most common cause of vertigo of peripheral origin and is more common than vertigo of central origin (Brandt and Daroff, 1980; Herdman, 1997; van der Velde, 1999). BPPV is characterized by brief intense, but often severe, rotational vertigo when the head is moved into particular positions. These movements typically include rolling onto one side in bed, lying down or getting up from supine, looking or reaching upwards, turning the head into the combined position of extension/rotation such as when reversing the car, with reversal of the provoking movement causing a reversal in the nystagmus and recurrence of the vertigo (Brandt & Daroff, 1980; Herdman, 1997; Van Der Velde, 1999; Herman and Tusa, 2000). Symptoms such as postural instability, generalized disequilibrium, unsteadiness of gait, sensitivity to head movements and falls may also be reported. There are two postulated causes of BPPV, with the most common being canalithiasis, where degenerative debris from the utricle floats freely within the endolymph of, most commonly, the posterior semi-circular canal. When the head is moved into a provoking position, the otoconia (debris) move, as a result of gravity, to the most dependent position in the semicircular canal, causing movement within the endolymph which pulls on the cupula, causing the neurons to fire. The typical delay in onset of symptoms relates to the time required for deflection of the cupula by the endolymph, the characteristic nystagmus is caused by the relative deflection of the cupula and the fatigue of the symptoms occurs because the endolymph stops moving when the position is sustained (Herman and Tusa, 2000). BPPV occurs spontaneously but may also follow a bout of labyrinthitis or head trauma, such as whiplash or head injury. Cervical vertigo or dizziness has also been described, but its mechanisms remain controversial (Clendaniel, 2000). Symptoms typically associated with cervical dizziness appear related more to altered balance than oculomotor or vestibular function. Typical presentation includes dysequilibrium or light-headedness, ataxia or unsteadiness combined with cervical pain and restricted movements, with symptoms provoked by movements of the head, in no particular direction. However, other disease processes can present with similar symptoms. At present, since there is no definitive test for cervical dizziness, the presence of cervical signs on examination and prompt favourable response to their treatment would appear the optimal initial differential diagnostic pathway. Failure to respond to cervical treatment suggests referral for investigation of vestibular or neurological function would be appropriate.

Vertigo from VBI may resemble BPPV. The key features of each are provided in Table 3. Physical diagnosis of BPPV involves a series of provocative positioning and movement tests, part of which is not dissimilar to those used for VBI testing. If VBI testing of cervical rotation/extension undertaken in supine appears positive, BPPV may be the cause as the position is similar to the final stage of the Dix–Hallpike test (Herman and Tusa, 2000). VBI testing should be repeated in sitting, particularly with hips in flexion, so that the final cervical position is the same but the head remains in a vertical position, thus preventing the symptoms of BPPV, which are provoked by changes in head position relative to gravity (Clendaniel, 2000). Other causes of vertigo and nystagmus should also be considered in differential diagnosis and the presence of other background conditions may also facilitiate differentiation: ear disease, cardiovascular disease, migraine, epilepsy, stroke, head injury or a family history of BPPV may provide clues to the current presenting disorder. These cues may be helpful during examination to determine the source of vertigo, thus facilitating decisions related to the safety of cervical manipulation. The revised guidelines enable the physiotherapist the latitude to evaluate the most likely cause for the presenting ‘dizziness’ symptoms based on clinical reasoning and guided by the above research. However, if a physiotherapist is unsure of a diagnosis related to dizziness of VBI, BPPV or other origin, referral to an otolaryngologist, neurologist or vestibular rehabilitation physiotherapist is recommended. 4.3. Provision of information and gaining consent The rate of compliance of provision of information and obtaining consent was poor overall. The fact that fewer than half the respondents complied with this component of the protocol and that such strong opinion was expressed against obtaining consent is of great concern. There are clear legal arguments stating that provision of information and obtaining consent from a patient prior to use of techniques over which the patient has no control and which potentially involve a degree of risk is no longer a recommendation but law (for example, Dunn, 1993; Parry, 1994; Delany, 1996; Haswell, 1996; Sim, 1996). There has been extensive comment in both the popular and legal press about the implications for the health professions of the Rogers v Whitaker (1992) judgement (for example, McSherry, 1993; Nisselle, 1993; Balding, 1995; Grant, 1996a, b, 2002; Nagree, 1997), supporting the need to develop a new protocol that can be applied appropriately and consistently by all. In addition to the legal requirement, the emphasis of care within musculoskeletal physiotherapy now includes the patient more in decision making (Gifford, 1998;


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Table 3 Differentiating BPPV from VBI (Based on Davies, 1997; van der Velde, 1999; Clendaniel, 2002) BPPV

VBI

Head vs. neck position used to elicit vertigo and nystagmus

Specific head movement in relation to gravity, but not when head is immobile. Typically, movements include: Lying down Rolling onto one side Looking up Hallpike manoeuvre is classically positive

Relative head movement while neck immobile

Latency

Few seconds (average 3–4 s to 1 min)

Abrupt in onset and of short duration (several minutes)

Nystagmus behaviour

Decrease in nystagmus within less than 20 s if position is sustained

Continuation of nystagmus with maintenance of position

Pattern of nystagmus

Torsional (fast phase towards the affected ear) More vertical (upbeating) when looking away from the affected ear Can be stabilized by visual fixation

Usually vertical

Fatiguability

Intensity of vertigo decreases with continued testing

Intensity of vertigo increases with continued testing

Additional symptoms/ signs

Postural instability Disequilibrium Nausea/vomiting

Disturbances in vision Diplopia Nausea/vomiting Ataxia

Harding, 1998), as this process has been shown to enhance patient response to management (Strong, 1995). The comment that requesting the patient’s consent to manipulate their neck would mean fewer patients agreeing to the technique fails to reflect this changing philosophy within health care generally. Health professionals have both an ethical and legal obligation to provide information and gain consent for techniques such as cervical manipulation. Failure to provide the opportunity for consent undermines the moral principle of respect for an individual’s essential human dignity (Sim, 1996). A suit for assault or battery may be brought by a patient against a health practitioner, significantly, with no need to show actual physical harm (Dimond, 1995)—battery if the patient is touched, assault where the patient fears they will be touched. Under the tort of negligence, if a breach of duty of care can be proved, with the direct result that the patient undergoes some foreseeable harm, negligence on the part of the therapist is said to have occurred (Brazier, 1992). A duty of care covers the provision of information and obtaining consent as well as the treatment itself. Therefore, providing information and gaining consent for cervical manipulation protects the therapist from legal action in addition to respecting the patient’s right to self-determination.

Sustained cervical or head posture No effect of gravity identified

Cannot be stabilized by visual fixation

Dysarthria Dysphagia Hemiparesis/hemiplegia Drop attacks

In law, consent takes different forms. ‘Express consent’ occurs when an individual explicitly indicates agreement, either orally or in writing; ‘implied consent’ occurs when an individual does not specifically indicate agreement but performs some action that suggests consent, such as following instructions prior to administration of any particular procedure; and ‘tacit’ consent is where consent is inferred from the patient’s failure to dissent (Sim, 1996). Express consent is considered essential prior to techniques over which the patient has no control, such as cervical manipulation and should be re-established prior to every individual manipulative technique. Implied or tacit consent is sufficient for the majority of physiotherapy procedures. Informed consent is a form of express consent and has been defined as ‘the voluntary and revocable agreement of a competent individual to participate in a therapeutic or research procedure, based on an adequate understanding of its nature, purpose, and implications’ (Sim, 1996). The judgement made in Rogers v Whitaker (1992) changed the view of the courts from one where mistakes were accepted as part of the risk inherent in medical treatment, to one where failure to provide information and warnings about treatment was no longer ‘misadventure’ but negligence (Delany, 1996). The key feature in this case was that the court decided what



was acceptable and reasonable, not the profession. ‘The general legal principle which underpins the (Rogers and Whitaker) finding is one which asserts that the paramount consideration is that a person is entitled to make decisions about his or her own life, and the duty to disclose the information takes its precise content from the needs, concerns and circumstances of the patient’ (Retsas and Forrester, 1995, cited by Delany, 1996). Since this judgement, medico-legal practitioners have urged the health professions, including physiotherapy, to change their practice in this area (Delany, 1996; Haswell, 1996; Kee, 1996; Nagree, 1997). A survey of APA members (Grant and Trott, 1991; Grant, 1996a, b), a straw poll conducted by Delany (1996) and the present survey all reported poor compliance among physiotherapists with the requirement to provide information and obtain consent prior to cervical manipulation. Text responses to the MPA survey demonstrated strong opinion by some respondents that this requirement was inappropriate. Such an approach to patient information and consent is not acceptable in law (Delany, 1996). Expert medico-legal advice was sought prior to development of the new clinical guidelines. The key feature of this advice was that the health practitioner was required to provide adequate information to the patient concerning the procedure for the patient to be able to make a judgement about the choices offered. Such information must include the benefits and risks associated with the procedure and alternatives to that procedure, together with their benefits and risks. The information must be provided in a form that the patient can understand. In addition, the health practitioner must provide the patient with the opportunity to ask questions about the procedure and to have those questions answered to their satisfaction prior to the request for consent. Such information may be provided in a brochure format but without adequate face to face follow-up, a brochure does not fulfil the legal requirement. It is acknowledged that this process is time-consuming, but the negative impact must be weighed against the potential consequences of litigation should the process not be followed. Such a process is also considered essential to patient involvement in decision making related to their management. The need to inform the patient of the potential risk of death associated with cervical manipulation was also addressed. While accepting that there has been no legal precedent to help the decision process, the legal opinion was that, on available evidence from the literature and the results of the current survey, there was no need to inform the patient routinely of the risk of death. The consideration was that, if the risk is lower than those taken as part of normal daily life, it fails to constitute a

• • • • • • • •

The procedure involved Discussion/information Alternatives Benefits/risks Information sheets given or the method by which information provided Questions asked by patient Consent obtained Date Time:

Fig. 1. Recommended format for recording provision of information and obtaining consent.

substantial danger. However, if during questioning, concern about the risk of death were expressed by the patient, the therapist would be required to mention it and discuss the degree of risk with that particular patient. Finally, the need to record consent was considered. The legal advice was that, to fulfil all legal requirements, evidence must be shown that information has been given, that the patient has had the opportunity to ask questions and receive satisfactory answers, that consent was sought and given without coercion, with the time and date of consent recorded. Verbal consent is considered equivalent to written consent in this context, although this opinion differs among legal practitioners. The recommendation was made that a standard form of recording this process be implemented (see Fig. 1).

5. Clinical guidelines for pre-manipulative procedures for the cervical spine The new Clinical Guidelines differ substantially from the APA Pre-Manipulative Protocol. The somewhat rigid format of the protocol has been modified to allow a degree of clinical reasoning in patient examination and management. In all other aspects of manipulative/ musculoskeletal physiotherapy, clinical reasoning is strongly emphasized. A set of Clinical Guidelines rather than a formal protocol more appropriately reflects current practice of manipulative/musculoskeletal physiotherapy within Australia. The final document, while providing guidelines to clinical practice, leaves the ultimate decision on appropriate action to the therapist in the context of any particular individual patient presentation. The specific changes within the new guidelines from the previous Protocol include: *

Inclusion of an introductory explanatory preamble. This preamble includes mention of the provocative nature of the test procedures; mixed results from research in relation to alteration of blood flow within the vertebro-basilar system (Rivett et al., 1999;


*

*

Johnson et al., 2000; Zaina et al., 2003); that indicative factors appear to include trauma and/or neurological changes (Haldeman et al., 1999) and that there is no known method for testing the intrinsic anatomy of the vertebral artery. The screening tests will not identify all patients at risk of suffering an adverse reaction to manipulation. Inclusion of nausea within routine screening; inclusion of a range of symptoms that have been reported as associated with vertebro-basilar insufficiency (VBI) or vertebral artery dissection. Also included are differentiating features related to these symptoms to facilitate distinction of VBI related symptoms from those related to vestibular disorders or BPPV (Davies, 1997; van der Velde, 1999). In addition, the emphasis on the importance of the subjective screening is raised. Inclusion of routine questioning about provocation of VBI related symptoms during standard physical testing of the cervical spine of any patient. For patients who report provocation of VBI related symptoms, reduction of the specific requirements in the physical examination section. Minimum testing recommended now includes sustained end-range rotation only, performed either in supine or sitting, with the actual testing procedure unchanged from the previous protocol. Additional testing procedures are suggested but are not required by the guidelines, other than routine questioning during examination of active movements for the provocation of VBI related symptoms. Inclusion of additional testing procedures should be guided by the clinical reasoning of the physiotherapist in the context of any particular patient presentation.

The mandate was to reduce the protocol in length, but to base this reduction on research evidence. As discussed, the research is inconclusive in determining the most valid screening test. However, given that a change in blood flow related to rotation was detected in the majority of studies and that the present survey highlighted more incidents related to rotation than any other movement, sustained rotation was reasoned to be the most appropriate test to include as mandatory. *

Inclusion of a specific section outlining recommendations for assessment during and following treatment and interpretation of the results of the examination procedures. The specific recommendations are that if there is evidence of symptoms potentially associated with VBI from both the subjective and physical components of the examination, cervical manipulation or high velocity thrust techniques (HVTT) or end-range rotation techniques (ERRT) should not be undertaken. Also, if there is evidence at any time that symptoms are clearly associated with VBI,

*

105

HVTT or ERRT should not be undertaken. In all other situations, the final decision depends on the therapist’s reasoning in any particular patient presentation. Inclusion of a substantially revised section on provision of information and obtaining consent for cervical manipulation (HVT techniques). This section includes essential information to be provided to any patient prior to undertaking cervical manipulation. Differences in types of consent as recognized in law are included to assist physiotherapists to determine the situations in which consent should be gained. Guidelines for gaining consent from patients for cervical manipulation (HVTT) and recording that consent are also included (Fig. 5). A flow chart of the processes to be followed during examination of a patient with cervical symptoms is provided (Fig. 2).

6. Conclusion This study suggests that the use and interpretation of the APA Protocol for Pre-Manipulative Testing of the Cervical Spine (APA, 1988) is variable among members of MPA. There is a need to continue with definitive investigations regarding the appropriateness, sensitivity and specificity of the protocol in detecting patients at risk of complications from manipulative/musculoskeletal physiotherapy techniques and the effect of cervical movement on vertebral artery blood flow. This research is ongoing (Rivett et al., 1999; Johnson et al., 2000; Grant, 2002; Zaina et al., 2003). The risk of complication from physiotherapy practice, including HVT techniques, appears to be low and none of the reported incidents in this study involved serious or permanent compromise to the vertebrobasilar system. A large number of the reported minor incidents were elicited by examination procedures involving rotation, including those related to the protocol, rather than manipulative physiotherapy treatment, arguably supporting the value of the protocol as a screening tool. While the new guidelines will never satisfy all members of the profession, the majority of the feedback has been positive. The principal criticism relates to the informed consent section, with some members resentful of the apparent imposition of this requirement. In reality, the imposition has come from the changing perception of the individual’s place and rights in society rather than the profession and the guidelines have been developed to protect physiotherapists in addition to their patients. Most MPA members providing informal feedback appreciate the relative freedom allowed in the new guidelines to make their own decisions.


106

Patient presents with problem OR need to cervical spine is recognised

cervical examine

Subjective vertebro-basilar (VBI) screening questions asked

No VBI symptoms identified

Presence of potential VBI symptoms identified

Cervical physical examination includes

Cervical physical examination includes

Screening for VBI symptoms with every active physiological movement tested

Screening for VBI symptoms with every active physiological movement tested Screening for VBI symptoms throughout PAIVM examination advisable

Refer for further investigation? Treat gently as appropriate No cervical manipulation

No VBI symptoms identified:

VBI symptoms identified: Refer for further investigation?

Treat as appropriate Monitor carefully during treatment Treatment choice = cervical manipulation:

No end-range rotation techniques

Recheck subjective VBI screening Evaluate sustained cervical rotation bilaterally (supine/sitting)

No cervical manipulation

No evidence of VBI Provide information about cervical manipulation Obtain consent to manipulation Manipulate with appropriate localised technique Reassess subjective VBI screening Reassess relevant physical signs Reassess sustained cervical rotation

Evidence of VBI Do NOT manipulate Refer for further investigation? Non-manipulative treatment as appropriate

Fig. 2. Flow chart for examination of the cervical spine using guidelines for pre-manipulative testing of the cervical spine.

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ARTICLE IN PRESS M.E. Magarey et al. / Manual Therapy 9 (2004) 95–108 Clements A. The dizzy patient: VBI or BPPV? In: Magarey ME, editor. Proceedings, More than Skin Deep, Proceedings of the 13th Conference of Musculoskeletal Physiotherapy Australia, Melbourne, Australian Physiotherapy Association: www.physiotherapy.asn.au, 2001. Clendaniel RA. Cervical vertigo. In: Herdman SJ, editor. Vestibular Rehabilitation, 2nd ed. Philadelphia: FA Davis; 2000. p. 494–509 [Chapter 21]. College of Physical Therapists of Alberta. Competencies required to safely perform spinal manipulation as a physical therapy intervention. rCollege of Physical Therapists of Alberta, Edmonton, 2000. # e P, Kreitz BG, Cassidy JD, Thiel H. The validity of the extension– Cot! rotation test as a clinical screening procedure before neck manipulation: a secondary analysis. Journal of Manipulative and Physiological Therapeutics 1996;19:159–64. Dan#ek V. Haemodynamic disorders within the vertebro-basilar arterial system following extreme positions of the head. Journal of Manual Medicine 1989;4:127–9. Davies RA. Disorders of balance. In: Luxon LM, Davies RA, editors. Handbook of vestibular rehabilitation. San Diego: Singular Publishing Group Inc.; 1997. p. 33–6. Delany C. Should I warn the patient first? Australian Journal of Physiotherapy 1996;42(3):249–56. Di Fabio RP. Manipulation of the cervical spine: risks and benefits. Physical Therapy 1999;79:50–65. Dimond B. Legal aspects of nursing, 2nd ed. London: Prentice-Hall; 1995. p. 88. Dunn I. What should doctor tell you? Law Institute Journal 1993;April:268–271. Gibbons P, Tehan P. Manipulation of the spine, thorax and pelvis: an osteopathic perspective. Edinburgh: Churchill Livingstone; 2000. Gifford L. Topical issues in pain: Whiplash: Science and management. Fear-avoidance beliefs and behaviour. In: Gifford L, editor. Physiotherapy Pain Association yearbook, 1998–1999. Falmouth, Adelaide: NOI Press; 1998. Grant R. Vertebral artery insufficiency: a clinical protocol for premanipulative testing of the cervical spine. In: Boyling JD, Palastanga N, editors. Grieve’s modern manual therapy. The vertebral column, 2nd ed. Edinburgh: Churchill Livingstone; 1994. p. 371–80. Grant R. Vertebral artery testing—the Australian Physiotherapy Association Protocol after 6 years. Manual Therapy 1996;1(3):149–54. Grant R. Vertebral artery concerns: premanipulative testing of the cervical spine. In: Grant R, editor. Physical therapy of the cervical and thoracic spine, 2nd ed. New York: Churchill Livingstone; 1996. p. 145–67 [Chapter 8]. Grant R. Pre-manipulative testing of the cervical spine: reappraisal and update. In Grant R, editor. Physical therapy of the cervical and thoracic spine, 3rd ed. New York: Churchill Livingstone; 2002. p. 138–58 [Chapter 8]. Grant R, Trott P. Pre-manipulative testing of the cervical spine—the APA protocol three years on. Proceedings of the 7th Biennial Conference Manipulative Physiotherapists Association of Australia, Blue Mountain’s, NSW, 1991. Grant T, Niere K. Techniques used by manipulative physiotherapists in the management of headaches. Australian Journal of Physiotherapy 2000;46:215–22. Gross AR, Aker PD, Quartly C. Manual Therapy in the treatment of neck pain. Rheumatic Disease Clinics of North America 1996;22(3):579–98. Gutmann G. Functional pathology, clinical picture of the spine, vol. 1. Stuttgart: IG Fischer; 1981. Haldeman S, Kihlbeck FJ, McGregor M. Risk factors and precipitating neck movements causing vertebrobasilar artery dissection after cervical trauma and spinal manipulation. Spine 1999;24: 785–94.

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Parry S. Aspects of law relating to cervical spine manipulation. Unpublished Master of Applied Science (Manipulative Physiotherapy) Treatise, Sydney University, 1994. Refshauge K. Rotation: a valid premanipulative dizziness test? Does it predict safe manipulation? Journal of Manipulative and Physiological Therapeutics 1994;17(1):15–9. Retsas A, Forrester K. Consent implications for health care practitioners. Journal of Law and Medicine 1995;2:317–26. Rivett DA. The premanipulative vertebral artery testing protocol: a brief review. New Zealand Journal of Physiotherapy 1995;23(1): 9–12. Rivett DA. Preventing neurovascular complications of cervical spine manipulation. Physical Therapy Reviews 1997;2:29–37. Rivett DA, Milburn PD. A prospective study of complications of cervical spine manipulation. Journal of Manual and Manipulative Therapy 1996;4:166–70. Rivett DA, Reid D. Risk of stroke for cervical spine manipulation in New Zealand. New Zealand Journal of Physiotherapy 1998;26:14–7. Rivett DA, Sharples KJ, Milburn PD. Effect of pre-manipulative tests on the vertebral artery and internal carotid artery blood flow: a pilot study. Journal of Manipulative and Physiological Therapeutics 1999;22:368–75. Rivett D, Sharples K, Milburn P. Vertebral artery blood flow during pre-manipulative testing of the cervical spine. In: Singer, K.P. (Ed.), Proceedings of the International Federation of Orthopaedic and Manipulative Therapists Conference, Interna-

tional Federation of Orthopaedic and Manipulative Therapists, Perth, 2000. Rogers v Whitaker. 175 CLR, 1992. p. 479–94. Shepard NT, Telian SA. Practical management of the balance disorder patient. San Diego: Singular Publishing Group; 1996. p. 1–24, 33–50, 163–85. Sim J. Informed consent and manual therapy. Manual Therapy 1996;2:104–6. Stevens A. Functional Doppler sonography of the vertebral artery and some considerations about manual techniques. Journal of Manual Medicine 1991;6:102–5. Strong J. Self-efficacy and the patient in chronic pain. In: Shacklock M, editor. Moving in on pain. Chatswood: Butterworth Heinemann; 1995. p. 97. Thiel HW, Wallace K, Donat J, Yong-Hing K. Effect of various head and neck positions on vertebral artery blood flow. Clinical Biomechanics 1994;9:105–10. Van der Velde GM. Benign paroxysmal positional vertigo. Part 1: background and clinical presentation. Journal of the Canadian Chiropractic Association 1999;43(1):31–40. Weingart JR, Bischoff H-P. Doppler sonography of the vertebral artery with regard to head positions appropriate to manual medicine. Journal of Manual Medicine 1992;30:62–5. Zaina C, Grant R, Johnson C, Dansie B, Taylor J, Syropoulos P. The effect of cervical rotation on blood flow in the opposite vertebral artery. Manual Therapy 2003;8(2):103–109, doi:10.1016/S1356689X(02)00155-8.

ARTICLE IN PRESS



Case Report

The presence and utilization of psoas musculature despite congenital absence of the right hip J.M. Elliott*, E.D. Zylstra, C.J. Centeno 11080 Circle Point Road, Suite 140, Westminster, CO 80020, USA Received 26 February 2003; received in revised form 9 July 2003; accepted 14 July 2003

1. Introduction All muscles that traverse the lumbar region have the potential to provide stability to the lumbar spine. In the last decade it has been reported that some muscles, including transversus abdominus and lumbar multifidus are more specific than others. These muscles have a functional role in enhancing spinal segmental support and control (Panjabi, 1992; O’Sullivan et al., 1995; Hodges and Richardson, 1996; Quint et al., 1998; Hides et al., 2001). Recently, the psoas major muscle has been implicated in its role as a muscle suited to stabilize the lumbar spine (Anderson et al., 1995; Penning, 2000). Additionally, there is evidence for a strong relationship between psoas muscle dysfunction in patients with documented herniated nucleus pulposus (HNP) and ipsilateral sciatica pain (Dangaria and Naesh, 1998). Traditional anatomical resources describe the psoas major as originating from the ventral surfaces of the transverse processes of L1–L5, the sides of the vertebral bodies and the annular fibres of the intervertebral discs of T12–L5. The psoas inserts into the lesser trochanter of the femur and it receives its nerve supply from the lumbar plexus, L1–L4. The actions of the psoas, with the origin fixed, are vast and include primary hip flexion with assistance in external rotation and abduction of the hip joint. Acting bilaterally and with the insertion fixed, the psoas flexes the trunk e.g. abdominal ‘‘sit-up.’’ In addition, while acting bilaterally, the psoas will increase the lumbar lordosis and will unilaterally act to assist in lateral flexion of the trunk towards the same side (Kendall, 1993). This case report suggests that, based on this patient’s congenital absence of specific anatomy, the psoas may have a more specific purpose than the aforementioned global movements involving the lumbar spine and hip *Corresponding author. Tel.: +1-303-429-6448x112; fax: +1-303429-6373. E-mail address: [email protected] (J.M. Elliott). 1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1356-689X(03)00128-0

joints. In particular, this purpose may be one of dynamic stabilization and support of the lumbar spine. This stabilizing function may be supported by the presence of multiple psoas muscle fascicles that attach to all lumbar spine levels (Penning, 2000). Further, electromyographic studies have provided evidence that, during relaxed upright stance, activity of the back muscles is restricted to the continuous minimal activity of the psoas muscle (Nachemson, 1966; Andersson et al., 1977; Hadjipavlou et al., 1996).

2. Patient history The patient was a 27-year-old female with congenital absence of both upper and lower extremities with the exception of a left acetabulum and underdeveloped left femur. It is duly noted that she is a highly motivated, fully independent member of her community in that she has recently finished a master’s level degree in communications at a local university in Norfolk, Virginia and continues to drive her own specially engineered automobile designed to her specific disabilities. She lives in an accessible apartment with her mother and vigorously demonstrates her ability to perform stand-by transfers with seemingly little difficulty. She does, despite her renowned enthusiasm and remarkable independence, suffer from ongoing low back and left lower extremity pain and this required further evaluation in our Westminster, Colorado pain clinic while she was visiting family in the Rocky Mountain region. The patient described her pain as being primarily located in the upper right lumbar spine and secondarily in the left gluteal region, left ischial tuberosity and the distal portion of her left femoral remnant. The pain in her left gluteal region and ischial tuberosity was qualitatively described as being intermittent, burning in nature and made worse with forward movement of her right-sided pelvis and trunk. Conversely, her right


J.M. Elliott et al. / Manual Therapy 9 (2004) 109–113

upper lumbar pain was dull and constant and made worse with movement of her left hip joint.

3. Examination findings A physiatrist evaluated her for her long-standing history of low back pain. Standard neurological examination utilizing a Wartenburg wheel revealed decreased sensation in the right T12–L1 dermatomes with a positive straight-leg raise (SLR) on the left. The SLR maneuver on the left increased concordant right upper lumbar pain. Additional radiological investigations were warranted and this included lumbar spine X-rays and a lumbar spine MRI to rule out an upper lumbar spine HNP. Standard lumbar spine series X-rays revealed the presence of a left-sided acetabulum with a 10-in femoral remnant, which was measured radiographically. The right-sided acetabulum and femoral complex were congenitally absent. Further, the presence of a well-developed left-sided ilium was present on X-ray whereas the right-sided ilium was grossly deformed with an antero-medially directed ilial bone. Coronal, sagittal and axial fast spin echo (FSE) T1 and T2 weighted (WI) MR images were unremarkable for an upper lumbar spine HNP, facet arthropathy or any other significant pathology. However, MR coronal scans revealed the presence of a bilateral psoas muscle despite the absence of a right-sided hip joint and femur (see Fig. 1). The origin of the right psoas muscle was visible on the L1–L3 vertebral levels while its insertion was visually appreciated in the distal pelvic fascia on the ventral surface of the right ilial bone. Further, bilateral grade IV lumbar multifidus atrophy and fatty infiltration were observed on the axial FSE T2WI at L5–S1 (see Figs. 2 and 3) (Danneels et al., 2000; Kader et al., 2000). In view of the musculoskeletal nature of the patient’s complaints and the copious amount of literature supporting specific lumbar stabilization exercises for

Fig. 1. FSE T2WI coronal MR image. The presence of bilateral psoas is visible.

Fig. 2. FSE T2WI axial MR scan of L3, demonstrating bilateral psoas musculature (small arrows), atrophy and fatty infiltration of bilateral multifidus (large arrows).

Fig. 3. FSE T2WI axial MR scan of L5 demonstrating absence of psoas on the right (arrow).

patients with low back pain, the physiatrist requested physical therapy evaluation and treatment as well as stabilization exercises with the aide of real-time ultrasound imaging. The physical therapy (PT) examination included gait evaluation, passive intervertebral motion testing (PIVM) in the lower thoracic and lumbar spines and standard neurological testing. The neurological portion of the PT evaluation revealed hypoesthetic response to pinwheel testing in the T11–L1 dermatomes on the right when compared to the ipsilateral and contralateral dermatomal fields above and below. The gait evaluation identified that the patient propelled her trunk in a ‘‘shuffling’’ type manner, which, secondary to body habitus, increased the weight bearing force on the left distal femoral remnant and the left ischial tuberosity while she propelled her right-sided trunk and pelvis forward. PIVM testing revealed point tenderness with posterior–anterior (PA) pressure on the spinous processes of T12–L2. PA pressure at those levels revealed an abnormal quality of movement through a restricted

ARTICLE IN PRESS J.M. Elliott et al. / Manual Therapy 9 (2004) 109–113

range and did increase concordant right upper lumbar spine pain. The quality of the movement was ‘‘stiff’’ and was accompanied by increased muscular spasm, which was interpreted to be stemming from protective muscular spasm (Maitland, 1986). All other caudal levels were considered normal with regard to PA pressure testing and pain provocation. The patient was also asked to perform an active SLR maneuver on the left while lying supine and this increased concordant right upper lumbar spine pain at approximately 10 of left SLR. There was a subjective report of decreased pain in the right upper lumbar spine when compression was provided by the physical therapist to the pelvic joints during the left SLR maneuver, suggestive of impaired pelvic joint mobility (Mens et al., 1999).

4. Treatment The patient was seen for a total of three visits over the course of her 1-week holiday in Colorado. The first treatment session began with PA mobilizations of the ‘‘stiff’’ motion segments in the lower thoracic and upper lumbar spine, T12–L2. This consisted of PA oscillatory mobilizations of grade IV, one set of 30 repetitions. However, due to an increased complaint of pain, as well as surrounding muscular spasm during mobilizations and limited time with respect to follow-up treatment, we decided to abandon this approach and focus strictly on the education of specific low-load therapeutic exercises e.g. transversus abdominus, lumbar multifidus and psoas musculature. Education and training of these specific exercises were performed with real-time ultrasound imaging with a hand-held 2.5 MHz curvilinear head. The patient spent the remainder of the first treatment session performing ‘‘abdominal hollowing’’ exercises for transversus abdominus and demonstrated a strong awareness of low load effort and isometric contraction of transversus abdominus. The patient was instructed to practice ‘‘abdominal hollowing’’ exercises over the next two days with each contraction to last approximately 10 s. We encouraged her to practice every time the telephone rang, as she stated that occurred frequently in her home in Virginia. It was agreed that this would be an appropriate prompt for her to develop and continue with an exercise routine. The second treatment session, 2 days later, consisted of a review session with ultrasound imaging of transversus abdominus. The patient continued to demonstrate an appropriate independent isometric contraction but denied relief with regards to her right upper lumbar spine pain. The treatment was then advanced to include educating the patient on the performance of lumbar multifidus ‘‘swelling’’ exercises.

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The patient was positioned prone and provided gentle manual pressure over the individual spinous processes of L1–L5 in a caudal direction to help facilitate multifidus contraction. Ultrasound imaging in the axial and sagittal planes were utilized to provide the patient with visual feedback of muscular contraction at each level. However, despite numerous attempts of performing lumbar multifidus exercises and attempting co-contractions of transversus abdominus, the patient was unable to demonstrate a contraction of her lumbar multifidus at any lumbar level. It is likely that the patient was unable to consciously contract her multifidus secondary to the significant amount of atrophy and fatty infiltration of the multifidi musculature, which was appreciated, on her axial MR images. The second treatment session ended with education on specific exercises of the left and right psoas muscle as psoas has been implicated in its role as a muscle suited to stabilize the lumbar spine (Anderson et al., 1995; Penning, 2000). Further, the authors were intrigued to determine whether or not the patient could even contract her right psoas given the absence of her right hip joint complex. More importantly, we were interested to determine if contraction of her right psoas, if possible, could provide her with some relief from her right upper lumbar pain, which was constant and dull and made worse with movement of her left hip joint. The patient’s body habitus dictated the positions utilized to image the psoas muscle (Fig. 4). The clinicians utilized the theorized mechanism of isometric psoas facilitation exercises described by Comerford (Kinetic Control, 2001). This technique involves instructing the patient to gently approximate the unilateral femur into the acetabulum, with particular attention given to possible substitution of the mobilizing hip musculature including rectus femoris, sartorius and quadratus lumborum. In addition, it has been theorized

Fig. 4. Patient being imaged with diagnostic ultrasound with handheld 2.5 MHz curvilinear head at the L2 segmental level using an axial scan.


J.M. Elliott et al. / Manual Therapy 9 (2004) 109–113

that manual long-axis distraction of the ipsilateral lower extremity may assist the patient by providing tactile feedback, which, in turn, may help the patient perform an independent contraction of the psoas. (Kinetic Control, 2001). An established procedure of obtaining real-time ultrasound images of psoas musculature was utilized (King et al.,1993; Kirchmair et al., 2001). Psoas musculature was identified on ultrasound by location of the kidney as the lateral border and the L2 transverse process medially (Figs. 4 and 5) (King et al., 1993; Kirchmair et al., 2001). The patient was asked to utilize the previously mentioned technique to facilitate independent isometric contractions of the right and left psoas while sonographic images were obtained. In order to verify specific contraction of the right and left psoas muscle, particular attention was given to the local superficial musculature to reduce and/or eliminate possible compensation during isometric psoas facilitation. The physical therapist provided gentle manual long-axis distraction to the distal portion of the patient’s left femoral remnant. The patient, after numerous attempts and with the aide of visual ultrasound imaging feedback and long-axis distraction, was able to independently contract her left psoas. However, she was unable to contract her right psoas without large substitutions of the more superficial mobilizing musculature e.g. quadratus lumborum. The patient was asked to continue practicing her right psoas contractions with the same effort that was needed to create an independent left psoas contraction over the next 2 days. Upon returning 2 days later, we reviewed her exercises and she continued to demonstrate independent contractions of transversus abdominus and left psoas and stated that she was encouraged by her progression on the rightsided psoas exercise. Interestingly enough, the patient was able to demonstrate an appropriate independent

contraction of psoas on the right side and this was evident on ultrasound imaging (Fig. 5). She continued to utilize the theorized mechanism for psoas contraction of gently approximating the unilateral femur into the acetabulum despite the absence of this anatomical complex on her right side, possibly suggesting that this may be an appropriate technique for performing an independent psoas contraction. Lastly, during psoas facilitation on the right, the patient performed a left SLR and reported a significant decrease in right upper lumbar spine pain, which was previously documented.

5. Discussion It has been reported that impairment of an active SLR correlates with mobility of the pelvic joints (Mens et al., 1999). It remains plausible, given this particular patient’s decreased complaint of pain with right psoas contraction, that she may have been utilizing the remaining fascicles of her right psoas muscle to provide dynamic stability in the upper lumbar spine while functionally moving her left femoral remnant. Further, this finding may suggest that psoas may be related to control of the lumbar spine and trunk during lower extremity movement. Since the patient was able to contract the right psoas despite the absence of her right hip anatomy and that this provided her with subjective relief from her pain, it is proposed that this muscle plays another, possibly more important role than global mobility of the lumbar spine and hip joints. Perhaps, this role is one as an adjuvant to lumbar multifidus and transversus abdominus, which provide dynamic stability, and control to the lumbar spine (Panjabi, 1992; Anderson et al., 1995; O’Sullivan et al., 1995; Hodges et al., 1996; Hides et al., 2001).

6. Conclusion

Fig. 5. Right: Psoas relaxed (top) and contracted (bottom).

This particular patient was seen in our Colorado clinic for a total of three visits prior to returning to her Virginia residence. It is noted that, despite her significant disability, she continues to manage her right upper lumbar spine pain with the performance of these specific isometric contractions of the right psoas and transversus abdominus musculature. In light of the aforementioned clinical and treatment findings with this exceptional patient and the particular characteristics of segmental spinal stability therapeutic exercises, it seems quite reasonable that psoas muscle, based on its segmental attachment to the lumbar vertebrae, could in fact be considered a lumbar spine stabilizer. Consequentially, psoas appears to be a muscle

ARTICLE IN PRESS J.M. Elliott et al. / Manual Therapy 9 (2004) 109–113

that may warrant careful attention when educating low back pain patients on specific exercise therapy. In this regard, however, because of the paucity of available similar documentation in the professional literature with regards to psoas muscle and stability exercises for patients with low back pain, more specific clinical research is warranted to further substantiate this theory.

References Anderson E, Oddsson L, Grundstrom H. The role of psoas and iliacus muscles for stability and movement of the lumbar spine, pelvis and hip. Scandinarian Journal of Medicine & Science in Sports 1995;5(1):10–16. Andersson GBJ, Ortengren R, Herberts P. Quantitative electromyographic studies of back muscle activity related to posture and loading. Orthopedic Clinics of North America 1977; 8:85–96. Dangaria TR, Naesh O. Changes in cross-sectional area of psoas major muscle in unilateral sciatica caused by disc herniation. Spine 1998;23(8):928–931. Danneels LA, Vanderstraeten GG, Cambier DC. CT imaging of trunk muscles in chronic low back pain patients and healthy control subjects. European Spine Journal 2000;9(4):266–272. Hadjipavlou AG, Farfan HF, Simmons JW. The functioning spine In: Farfan HF, Simmons JW, Hadjipavlou AG, editors. The sciatic syndrome, Slack, Thorofare, NJ, USA. Slack, 1996. p. 41–73. Hides J, Jull G, Richardson C. Long-term effects of specific stabilizing exercises for first-episode low back pain. Spine 2001;26(11): E243–E248. Hodges P, Richardson C. Inefficient muscular stabilization of the lumbar spine associated with low back pain: a motor control evaluation of Transverse Abdominis. Spine 1996;21:2640–2650.

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Kader D, Wardlaw D, Smith F. Correlation between the MRI changes in the lumbar multifidus muscles and leg pain. Clinical Radiology 2000;55:145–149. Kendall FP. Muscles—testing and function, 4th ed. Baltimore: Williams & Wilkins: 1993. p. 214 [Chapter 7]. Kinetic Control Course Notes. Dynamic stability and muscle balance of the lumbar spine and trunk. Southampton, Hants, UK: Kinetic Control; 2001. King AD, Hine AL, McDonald C, Abrahams P. The ultrasound appearance of the normal psoas muscle. Clinical Radiology 1993;48(5):316–318. Kirchmair L, Entner T, Wissel J. A study of the paravertebral anatomy for ultrasound-guided posterior lumbar plexus block. Anesthesia and Analgesia 2001;93:477–481. Maitland GD. Vertebral manipulation, 5th ed., Oxford: ButterworthHeinemann; 1986. p. 74 [Chapter 4]. Mens JM, Vleeming A, Snijders CJ, Stam HJ, Ginai AZ. The active straight leg raising test and mobility of the pelvic joints. European Spine Journal 1999;8(6):468–474. Nachemson A. Electromyographic studies on the vertebral portion of the psoas muscle. Acta Orthopaedica Scandinarica 1996;37: 177–190. O’Sullivan P, Twomey L, Allison G. Evaluation of specific exercise in the treatment of chronic low back pain with radiological diagnosis of spondylolysis or spondylolisthesis. In: Proceedings of Manipulative Physiotherapists Association of Australia Biennial Conference, Gold Coast; 1995. p. 113–4. Panjabi M. The stabilizing system of the spine. Part I. Function, dysfunction, adaptation and enhancement. Journal of Spinal Disorders 1992;5:383–389. Penning L. Psoas muscle and lumbar spine stability: a concept uniting existing controversies; critical review and hypothesis. European Spine Journal 2000;9(6): 577–585. Quint U, Wilke H-J, Shirazi A. Importance of the intersegmental trunk muscles for the stability of the lumbar spine: a biomechanical study in vitro. Spine 1998;23(18):1937–1945.

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Obituary

Brian Clifford Edwards Born Perth Western Australia—January 1941 Died Perth Western Australia—November 2003

Brian Edwards was born and grew up in Perth, Western Australia. In his early years, Brian had wanted to become a physician, but instead found his true and lasting vocation as a specialist in manual orthopaedic physiotherapy. He completed a diploma in physiotherapy at the WA School of Physiotherapy in 1963, worked briefly as a physiotherapist for the Repatriation Department in Perth and attended the first 3 month manual/manipulative therapy course run in Adelaide by Geoffrey Maitland in 1965. On his return to Perth he set up a private practice and began to develop his knowledge, skills and ability in joint manipulation by discriminating reading, careful observation and continual practice. He soon developed a wonderful reputation as a successful practitioner and a charismatic teacher. doi:10.1016/j.math.2004.01.007

When the Western Australian Institute of Technology (later Curtin University of Technology) took over the WA School of Physiotherapy in 1969, Brian began to teach undergraduate students the skills of manipulation, on a part-time basis, while continuing to run a busy city practice. Short duration, part-time courses for graduates soon followed by 1972/1973. Brian worked with Maureen Lissiman, Jack Gilbert and myself in preparing the curriculum for a full-time, 1 year post-graduate diploma in manipulative therapy. This began in February 1974 and a similar course also started in South Australia a little later in the same year. These were the first fully-accredited post-graduate courses in manipulative physiotherapy in the world. The first program consisted of 12 students; six from Western Australia, three from Eastern Australia and three from overseas. It is true to say that we ran the first year of the program very much by ‘‘the seat of our pants’’, remaining just in front of the students as we developed our own understanding of how to go about this demanding new work. While the theory was important, the practice and application was everything and in this regard, Brian Edwards was clearly the star. He was a great instinctive teacher and an exacting task master who demanded a great deal from his students, but gave of himself very freely in return. It is true to say that Brian had struggled in his own undergraduate studies, but in this specialised post-graduate field he flourished and became first a national figure and then an international personality in this new and very rapidly developing field of manual/manipulative physiotherapy. Brian also completed a Bachelor of Science in Anatomy at the University of Western Australia in 1975. Through this time, Brian was instrumental in forming a national specialist interest group, the Manipulative Therapists’ Association (MTA), which over time developed into the Manipulative Therapists’ Association of Australia (MTAA) and in 2000 became Musculoskeletal Physiotherapy Australia (MPA). He represented the MTA in the Canary Islands in 1973 when physiotherapists from around the world gathered to promote manipulative therapy education and to form the International Federation of Orthopaedic Manipulative Therapists (IFOMT). Brian was a leading figure in all of these associations, an individual who became a much

ARTICLE IN PRESS Obituary / Manual Therapy 9 (2004) 114–115

sought after keynote speaker, a role model and a wonderfully skilled practitioner much loved by his huge list of patients. He continued to teach generations of post-graduate students from all around the world until the mid 1990s, when he began to concentrate a little more on his business, Brian Edwards and Associates, his family, and on developing a major winery in the Margaret River area of Western Australia. Brian Edwards, along with his mentor Geoff Maitland and Pat Trott, became the first specialist manipulative therapists (by examination) in Australia and were awarded their fellowships in the mid 1980s. As one of his examiners, I’m not sure just who was under the most pressure during this exacting process. In 1996 Brian was honoured with an Honorary Doctorate in Science from Curtin University of Technology. In more recent times he provided advice to Notre Dame University (WA) in helping them set up their physiotherapy undergraduate program, and was made Professor of Physiotherapy. Brian had a most distinguished career. However, there was a great deal more to the man than just physiotherapy. He was an excellent sportsman and Australian rules football was his passion. He played amateur football at the highest level within the University Club in WA, and in this environment made a group of firm friends with whom he maintained contact for the rest of his life. He was part of the medical team for the West Coast Eagles football team which joined the Australian Football League in 1987, and an integral part of their 1992 and 1994 AFL Premiership winning combinations. Brian was also a swimmer of some note and participated in the annual 12 km ocean swim to Rottnest Island on a number of occasions. Thirteen years ago, in March 1990, Brian Edwards flew his bright yellow Tiger Moth aircraft ‘‘Matilda’’ from Binbrook in the United Kingdom to Perth. This extraordinary feat was performed in an elderly oneengined bi-plane, with no advanced navigation technology. His initial problems (a broken crankshaft on the first leg of the trip before leaving England) were soon over and Brian set off to Australia. Thirty-three legs, 47 days and very many adventures later he finally arrived in Perth. This trip honoured the memory of his father Clifford who died in July 1943, when he flew out from

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Binbrook in a Lancaster bomber during the second world war and never returned. A major reason which prompted Brian to do this was to return something to Legacy, the Australian organisation which supports the children of ex-service men and women. They supported Brian through his school and university days and he saw this flight, the attendant publicity and the funding he was able to attract, as one way of saying thank you. More than $40 000 was passed on to Legacy as a result of his flight. In the mid 1990s, Brian, with his close friend, orthopaedic surgeon and fellow footballer Tim Keenan, made several trips to the Pakistan–Afghanistan border to treat patients and train doctors who would treat the refugees in the area. Brian was both a brave man and a considerable humanitarian. Brian’s greatest partnership was with his wife, Jenny. She was the stable element, especially in his early years, as Brian was a fairly wild young man, and together they formed a great team. They had three children, Michael, Christopher and Susie, formed a very close family and in recent years have worked together in building the large Edwards vineyard and winery at Margaret River. There they have produced wonderful award winning quality wines. Their two sons both work at the winery, as does Christo’s wife Bianca. In 1992 Brian was awarded the Order of Australia Medal (OAM) for his services to physiotherapy and to aviation. Over the last 2 years Brian battled leukaemia with great courage and strength. His funeral service was attended by many hundreds of people from all phases of his life, his family and friends, professional colleagues, public identities, sporting associates and of course a considerable number of his very grateful patients. The service was a celebration of his life, his humanity and his great love for his family and friends. Brian was taken from us much too soon, but his own legacy lives on in his family, his professional and personal achievements, and in his award winning red wine.

Lance Twomey Vice-Chancellor Curtin University of Technology, Australia

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Letter to the Editor

Quantitative analysis of traction in the glenohumeral joint: in vivo radiographic measurements. By Gokeler A, van Paridon-Edauw GH, DeClercq S, Matthijs O, Dijkstra U. Manual Therapy 8 (2) (2003) 97–102. What do we feel—if we feel? There is no doubt that research is necessary in physiotherapy, and therefore I congratulate the authors for their radiographic exploration of traction in the glenohumeral joint. Finding no joint separation they state: ‘‘Our results indicate that it is unlikely that joint distraction occurs in a clinical situation in healthy glenohumeral joints’’ (p. 101). Doubt is at the beginning of progress and, therefore, I would like to add a question to their conclusion. Mennell’s publications are one origin of today’s Manual Therapy. In his publications, Mennell has shown two different pairs of radiographs without and with traction, where the separation of the head of humerus from the glenoid fossa is clearly visible (Mennell, 1945, p. 186 (Fig. 1); 1949, p. 127 (Fig. 2)). He wrote ‘‘Miss Catherine Lamb, who so kindly acted as a model during the tedious process of preparing these photographs, was

Fig. 1. 1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1356-689X(03)00102-4

in no way selected for the unusual mobility of her joints. The choice fell on her as a matter of pure accident and the movements shown are merely those that can be performed through a similar, or wider, range in any normal youthful adult’’ (Mennell, 1945, p. 186). Of course, at that time scientific guidelines were not what they are today, but Mennell’s descriptions did not include any mention of an excessive amount of traction force.

Why did the authors not find what Mennell was able demonstrate? What might have been the reasons of their failure to demonstrate joint separation? The authors have referred to Kaltenborn for their technique. He defines traction as a movement at a right angle away from the treatment plane, i.e. laterally for the shoulder joint (Kaltenborn,

ARTICLE IN PRESS Letter to the Editor / Manual Therapy 9 (2004) 116–117

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Fig. 2.

2002, p. 33, 193). In Fig. 1 (p. 99) however, the direction of traction seems to be at a 45 angle to the horizontal plane. The shoulder girdle elevation visible in Fig. 1 might be an explanation for this, but this is neither part of the standard technique nor explained in the study. Fixation was perhaps not as it should have been and the authors admit that it ‘‘was not possible to fixate the scapula entirely during testing’’ (p. 101). The fixation belt does not seem to be near to the infraglenoid tubercle and not directed horizontally opposite to the traction direction (Schomacher, 2001, p. 404). In the study the fixation belt was wrapped diagonally over the shoulder, held by an assistant and not attached to a table as it should have been (Kaltenborn, 2002, p. 193). The authors give ‘‘the impression that it is mainly soft tissues that are moved during traction and that in spite of the therapist’s feeling of joint separation, no such separation occurs’’ (p. 101). Their results however are limited to the technique modalities used in the study and

are questioned at least by radiographs from Mennell cited above. Further research is necessary before making general statements on shoulder joint traction.

References Kaltenborn FM. Manual mobilisation of the joints: the Kaltenborn method of joint examination and treatment, Oslo: Olaf Norlis Bokhandel; 2002. p. 33, 193. Mennell JB. Physical treatment by movement, manipulation and massage, 5th ed. London: J&A Churchill Ltd; 1945. p. 186. Mennell JB. The science and art of joint manipulation, vol. 1, The Extremities 2nd ed. London: J&A Churchill Ltd; 1949. Schomacher J. Diagnostik und Therapie des Bewegungsapparates in der Physiotherapie, Stuttgart, NY: Thieme Verlag; 2001.

Jochen Schomacher PT-OMT (Germany), MCMK (France), DPT (USA) Feldergstr, 16a, Willstatt 77731, Germany

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Correspondence

Author’s reply We would like to thank Mr. Schomacher for reading our paper carefully and for his useful critical comments. We would like to address the points of critique. First, Mr. Schomacher suggests that in Mennell’s paper, separation of the humeral head from the glenoid fossa is clearly visible after application of a traction force. We have some reservations about these observations. As one may see on the radiographs, the shoulder girdle in its totality has moved laterally in the direction of the traction force applied. Thus, the position of the scapula and the humerus has been changed. However, this has not been accounted for during the radiographic projection. When traction is applied the shoulder girdle is pulled laterally and the anterior posterior projection changes. This lateral position changes suggests a larger joint space compared to the position without traction. In fact, we encountered the same problem in our experiment, but we solved it by adjusting the X-ray beam during traction accordingly to get the same approfile compared to the situation without traction force applied. This correction was necessary to allow for a valid comparison between no-traction and traction. This correction was not mentioned in Mennell’s study. Second, Mr. Schomacher raises a question about the direction of traction force applied in our study. We followed the lateral orientation of the scapular spine and used then the instruction mentioned in the textbooks (Kaltenborn, 1985; Mink et al., 1990; Frisch, 1996) on manual therapy regarding the direction of traction. As the scapula had taken a slightly more vertical orientation we had to adjust the direction of traction force accordingly to keep it perpendicular to the treatment plane as can be seen in Fig. 1 of our paper. Third, we do not agree with Mr. Schomacher regarding the lack of appropriate fixation. We fixated the scapula with a belt and the assistant pulled with maximal force as traction was applied to the glenohumeral joint. The fixation force exceeds the one used clinically.

1356-689X/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1356-689X(03)00103-6

Our study was designed to analyse the change in distance between the humeral head and the glenoid fossa during maximally loose-packed position (MLPP) and the maximally closed-packed position (MCPP) under rigidly standardized research conditions in six cases whereas Mennell’s publication is an anecdotal illustration of a clinical impression (one case). We do agree with Mr. Schomacher that reservations have to be made in generalizing our results to the clinical situation. Further research with different positions of humerus relative to the scapula, applying different traction forces with regard to magnitude and direction and applying different techniques for fixation are needed before the results can be generalized to the clinical practice.

References Kaltenborn FM. Mobilization of the extremity joints, 3rd ed. Oslo, Norway: Olaf Norlis Bokhandel; 1985. Mink AJF, Veer ter HJ, Vorselaars JAC. Extremiteiten. Functieonderzoek en manuele therapie, 6th ed. Utrecht/Antwerpen: Bohn, Scholtema en Holkema; 1990. Frisch H. Programmierte Therapie am Bewegungsapparat. Chirotherapie, 2nd ed. Berlin: Springer; 1996.

Alli Gokeler Medisch Centrum Zuid, Van Ketwich-Verschuurlaan 287, Groningen 9271 SM, Netherlands E-mail address: [email protected] Pieter U. Dijkstra Department of Rehabilitation, Department of Oral and Maxillo Facial Surgery, University Hospital Groningen, Groningen, Netherlands

ARTICLE IN PRESS



Book reviews Chronic fatigue syndrome and the body’s immune defense system Roberto Patarca-Montero: The Haworth Medical Press, New York, 2002, price d19.95, ISBN 0789015307

This book is a comprehensive and concise overview of the available literature data on extracellular immune (dys)function in patients with Chronic Fatigue Syndrome (CFS). The author, who has served as the Editor for both the ‘Journal of Chronic Fatigue Syndrome’ and ‘Critical Reviews in Oncogenesis’, has done a superb job in summarizing, and most importantly organizing this body of literature in nine successive chapters. The chapters succeed one another like they do in a novel. Chapter 1 addresses the basics of immunology, enabling each caregiver, regardless of their background, to devour this book. CFS represents the combination of both physiologic and psychological impairments. Chapters 2–7 provide knowledge and insight into these physiologic impairments, and how the different body systems affected by the disease (the immune system, the nervous system, and the endocrine system) cross-talk in both healthy subjects and patients with CFS. Special emphasizes is given to the increased autoimmune manifestations and associated TH1 (T helper type 1)/ TH2 imbalance of the immune system, immune activation, and poor cellular immune function (characterized

by the low natural killer cell cytotoxicity, etc.). At several places in the book, similarities and differences with other disorders (depression, fibromyalgia syndrome, gulf warr illness, rheumatoid arthritis, etc.) are explored. Although remaining purely hypothetical, much of the available evidence on immunopathology in CFS, as described in Patarca’s book, may have damaging consequences for the musculoskeletal system. The book, however, does not address the practical implications of the current understanding of CFS immunopathology for the manual therapy profession. Additionally, insufficient emphasis is given to the body of literature addressing the intracellular immune deregulations in patients with CFS. Nevertheless, this book is relevant and highly recommended to each health-care worker treating patients with CFS.

Jo Nijs Department of Human Physiology, Faculty of Physical Education and Physical Therapy, Vrije Universiteit Brussel (V.U.B), 1090 Brussel, Belgium Division of Occupational and Physical Therapy, Department of Health Sciences, Hogeschool Antwerpen, Belgium E-mail address: [email protected]

doi:10.1016/S1356-689X(03)00091-2

Rehabilitation of the hand and upper limb Rosemary Prosser and W. Bruce Conolly (Eds.); Butterworth-Heinemann, Stoneham, MA, 2003, Price d35, - ISBN 0750622636 This comprehensive book on disorders of the hand and upper limb covers numerous surgical, sport and work injury conditions. Chapter one starts with an overview of the healing process, principles of assessment and a wide range of modalities and treatment approaches. In Chapters 2,3,5 and 6 the functional anatomy, detailed assessment, possible dys-

functions and applicable therapy options for the hand, wrist, elbow and shoulder are discussed. Arthritic and nerve conditions, and sport and work injuries are extensively discussed, each in a separate chapter. Acknowledged experts in the field contributed to the book under the editorship of an experienced hand surgeon and hand therapist. It is a book for surgeons and therapists at all levels of experience and training who might be treating patients with a disorder of their hand or upper limb. Surgical interventions (including some ideas on rehabilitation afterwards), as well as


Book reviews / Manual Therapy 9 (2004) 119–120

conservative management of conditions, are described. Although not covered extensively, the clear and practical approach, numerous illustrations, biochemical and pathological discussion allow manual therapists to decide which manual therapy techniques are best practice for each condition. A useful questionnaire (American Shoulder and Elbow Score) is included as an appendix, to assess the outcome of intervention after shoulder and/or elbow injury.

doi:10.1016/j.math.2004.01.002

The book contributes to a multi-professional approach in management of hand and upper limb disorders. Ina Dienera,b Stellenbosch, South Africa Departments of Physiotherapy University of the Western Cape South Africa b Stellenbosch University, South Africa a

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Book review Rehabilitation of the hand and upper limb Rosemary Prosser and W. Bruce Conolly (Eds.); Butterworth-Heinemann, Stoneham, MA, 2003, Price d35, - ISBN 0750622636 This comprehensive book on disorders of the hand and upper limb covers numerous surgical, sport and work injury conditions. Chapter one starts with an overview of the healing process, principles of assessment and a wide range of modalities and treatment approaches. In Chapters 2,3,5 and 6 the functional anatomy, detailed assessment, possible dysfunctions and applicable therapy options for the hand, wrist, elbow and shoulder are discussed. Arthritic and nerve conditions, and sport and work injuries are extensively discussed, each in a separate chapter. Acknowledged experts in the field contributed to the book under the editorship of an experienced hand surgeon and hand therapist. It is a book for surgeons and therapists at all levels of experience and training who might be treating patients with a disorder of their

doi:10.1016/j.math.2004.01.002

hand or upper limb. Surgical interventions (including some ideas on rehabilitation afterwards), as well as conservative management of conditions, are described. Although not covered extensively, the clear and practical approach, numerous illustrations, biochemical and pathological discussion allow manual therapists to decide which manual therapy techniques are best practice for each condition. A useful questionnaire (American Shoulder and Elbow Score) is included as an appendix, to assess the outcome of intervention after shoulder and/or elbow injury. The book contributes to a multi-professional approach in management of hand and upper limb disorders. Ina Dienera,b Stellenbosch, South Africa Departments of Physiotherapy University of the Western Cape South Africa b Stellenbosch University, South Africa a

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Manual Therapy Journal - Volume 9, Issue 3, Pages 123-182 (August 2004)

Manual Therapy Journal - Volume 9, Issue 4, Pages 183-246 (November 2004)

Manual Therapy Journal - Volume 9, Issue 1, Pages 1-58 (February 2004)

Manual Therapy Journal - Volume 8, Issue 2, Pages 63-128 (May 2003)

Manual Therapy Journal - Volume 12, Issue 2, Pages 85-198 (May 2007)

Manual Therapy Journal - Volume 11, Issue 2, Pages 91-166 (May 2006)

Manual Therapy Journal - Volume 10, Issue 2, Pages 93-174 (May 2005)

Manual Therapy Journal - Volume 14, Issue 2, Pages 117-240 (April 2009)

Manual Therapy Journal - Volume 13, Issue 2, Pages 91-180 (April 2008)

Manual Therapy Journal - Volume 14, Issue 5, Pages 461-584 (October 2009)

Manual Therapy Journal - Volume 13, Issue 4, Pages 277-372 (August 2008)

Manual Therapy Journal - Volume 14, Issue 4, Pages 353-460 (August 2009)

Manual Therapy Journal - Volume 12, Issue 4, Pages 297-396 (November 2007)

Manual Therapy Journal - Volume 8, Issue 1, Pages 1-62 (February 2003)

Manual Therapy Journal - Volume 10, Issue 4, Pages 239-304 (November 2005)

Manual Therapy Journal - Volume 8, Issue 3, Pages 129-192 (August 2003)

Manual Therapy Journal - Volume 8, Issue 4, Pages 193-270 (November 2003)

Manual Therapy Journal - Volume 13, Issue 1, Pages 1-90 (February 2008)

Manual Therapy Journal - Volume 12, Issue 3, Pages 199-296 (August 2007)

Manual Therapy Journal - Volume 10, Issue 1, Pages 1-92 (February 2005)

Manual Therapy Journal- Volume 13, Issue 6, Pages 475-564 (December 2008)

Manual Therapy Journal - Volume 12, Issue 1, Pages 1-84 (February 2007)

Manual Therapy Journal - Volume 14, Issue 1, Pages 1-116 (February 2009)

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

Manual Therapy Journal - Volume 11, Issue 1, Pages 1-90 (February 2006)

Manual Therapy Journal - Volume 13, Issue 3, Pages 181-276 (June 2008)

Manual Therapy Journal - Volume 10, Issue 3, Pages 175-238 (August 2005)

Manual Therapy Journal - Volume 14, Issue 3, Pages 241-352 (June 2009)

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

Manual Therapy Journal - Volume 11, Issue 4, Pages 241-358 (November 2006)

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