Deteriro Flexores Cervicales (Mt Jull 04)

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www.elsevier.com/locate/mathManual Therapy 9 (2004) 8994

Original article

Impairment in the cervical exors: a comparison of whiplash andinsidious onset neck pain patients

G. Jull a, *, E. Kristjansson b , P. DallAlba aa Department of Physiotherapy, The University of Queensland, Queensland 4072, Australia

b The Faculty of Medicine, The University of Iceland, Reykjav!

k, 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 neckpain of whiplash and insidious origin. This study examined the neck exor synergy during performance of the cranio-cervical exiontest, a test targeting the action of the deep neck exors.

Seventy-ve volunteer subjects participated in this study and were equally divided between Group 1, asymptomatic controlsubjects, Group 2, subjects with insidious onset neck pain and Group 3, subjects with neck pain following a whiplash injury. Thecranio-cervical exion test was performed in ve progressive stages of increasing cranio-cervical exion range. Subjects performancewas guided by feedback from a pressure sensor inserted behind the neck which monitored the slight attening of the cervical lordosiswhich 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 (allP o 0.05) and had signicantly greater shortfalls from the pressure targets in the test stages ( P o 0.05). No signicant differences wereevident between the neck pain groups in either parameter indicating that this physical impairment in the neck exor synergy is

common to neck pain of both whiplash and insidious origin.r 2003 Elsevier Ltd. All rights reserved.

Keywords: Neck exors; Whiplash; Neck pain

1. Introduction

Neck pain is a common condition causing substantialpersonal and nancial costs ( C

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e et al., 1998 ; Holm-strom et al., 1992 ). Broadly, onset may be insidious ormay follow trauma. Pain is often persistent or recurrentin nature. Neck pain of traumatic origin following amotor vehicle crash (whiplash) often poses a particularchallenge in management. There are several inuencesthat may impact on the perception of neck pain anddisability 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, socialfactors and litigation ( C

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e et al., 2001 ; Radanov and

Sturzenegger, 1996 ). There has been little investigationinto whether or not differences exist in the nature of physical impairment associated with neck pain of whiplash and insidious origins which may contributeto the greater difculty often encountered in therehabilitation of patients with WAD.

Changes in cervical exor muscle function have beeninvestigated in neck disorders of both whiplash andinsidious origins. Vernon et al. (1992) in an initialcomparative study of neck isometric strength and exor/extensor strength ratios, found that subjects with bothWAD and insidious onset neck pain had lesser strengththan asymptomatic subjects. There was a progressiveanterior-to-posterior muscle imbalance in the neck painsubjects, with the cervical exors becoming relativelyweaker as compared to the extensors. This was moreapparent in subjects with WAD, suggesting that therecould be a difference in the degree of impairmentbetween these subject groups.

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*Corresponding author. Tel.: +61-7-3365-2275; fax: +61-7-3365-2775.

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


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Cervical exor muscle function has also been exam-ined using the cranio-cervical exion test (C-CFT) ( Jull,2000). The cranio-cervical movement aims to assess theanatomical action of longus capitis in synergy withlongus colli, rather than that of the supercial exors,sternocleidomastoid (SCM) and anterior scalene mus-

cles, which ex the neck but not the head. The longuscolli muscle has a unique role in the support of thecervical segments and curve ( Mayoux-Benhamou et al.,1994). In the C-CFT, the subject performs ve incre-ments of increasingly inner range cranio-cervical exionin a supine lying position ( Falla et al., 2003a ; Jull, 2000 ).Patients are guided to the test level by feedback from apressure unit (Stabilizer, Chattanooga, USA) which isplaced behind the neck to monitor the progressiveattening of the cervical lordosis which results from thecontraction of longus colli ( Mayoux-Benhamou et al.,1994, 1997 ). Performance in the test has been examinedin subjects with WAD ( Jull, 2000 ) and cervicogenicheadache ( Jull et al., 1999 ). The results of these studiesindicated that patients were less able to achieve and holdthe progressive positions of the test as compared to therespective control subjects. These results inferreddysfunction in the deep neck exors, as no directmeasure of these muscles could be made. In the studyof 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) duringthe test, following Cholewicki et al.s (1997) hypothesisthat increased activity of the supercial muscles could be

a measurable compensation for poor segmental stability,or in this case of the C-CFT, poorer activation of thelongus colli. It was shown that both neck pain patientgroups had higher amplitudes of muscle signals in theSCM.

There has not been a direct comparison of perfor-mance in the C-CFT between patients with neck painfrom whiplash and insidious origin. This study wasundertaken to make this comparison. A clinicallyapplicable version of the C-CFT was used.

2. Methods

2.1. Subjects

Seventy-ve volunteer subjects between the ages of 1866 years were enrolled in the study. They comprisedthree groups, each of 25 subjects. Control subjects(Group 1) and insidious onset neck pain subjects(Group 2) were volunteers from the general anduniversity communities who responded to advertising.The control subjects were eligible for the study providedthey had no current or past history of musculoskeletalpain or injury in the neck or upper limb. Insidious onset

neck pain subjects were eligible provided that theircondition had not been caused by trauma from a motorvehicle crash. Subjects with WAD (Group 3) were thoseattending for assessment at a Whiplash Research Unit.Subjects for Groups 2 and 3 were not considered if theyhad a history of neck surgery, previous diseases affecting

the neck or throat, and rheumatic or neurologicaldisorders. Ethical clearance for the study was obtainedfrom the Medical Ethics Committee, The University of Queensland, and all subjects gave informed consent toparticipate in the study.

2.2. Instrumentation and measurements

For Groups 2 and 3, data were collected regarding thelength of history of neck pain and subjects rated theiraverage pain intensity on a visual analogue scale (VAS),anchored with no pain and the worst pain imaginable.

2.2.1. Cranio-cervical exion testThe subjects were positioned in a supine lying

position. The pressure sensor was inserted between thetesting surface and the back of the neck and waspreinated to a baseline of 20 mmHg ( Fig. 1 ). Subjectswere asked to perform progressive repetitions of cranio-cervical exion to increase the pressure by 2 mmHgincremental targets from 22 mmHg to a maximum of 30 mmHg. Each target pressure was held for 5 s with a10 s rest between each task. The pressure sensor wasconnected to a pressure transducer (RS components)and electrical signals from the pressure transducer were

amplied and relayed to a visual feedback device and toan Amlab data acquisition system (Associated Measure-ments Pty Ltd, Australia). The visual feedback deviceconsisted of an electronic voltmeter, marked in 2 mmHgincrements from 20 to 30 mmHg, and calibrated to

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Fig. 1. The cranio-cervical exion test demonstrating the visualfeedback with the pressure sensor and measurement with surfaceEMG.

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display the pressure in the pressure bag, based on thepressure transducer output. Sampling frequency forpressure measures was 1000 Hz. The mean pressure thateach subject achieved over the 5 s holding time of theve test levels was calculated to determine whethersubjects had reached each prescribed level of the test.

The differences between the mean pressure achieved andthe nominated target pressure for each stage werecalculated for each group.

Myoelectric signals were collected from the SCMmuscles using AgAgCl electrodes (Conmed, USA) in abipolar conguration. Electrodes were positioned alongthe lower one-third of the muscle bellies of the SCM(Falla et al., 2002 ). Signals were amplied (Amlab), andpassed through a 20500 Hz bandwidth lter. They weresampled at 1000 Hz. EMG data (amplitude of the signal)were analysed off-line (Matlab). The maximum rootmean squared (RMS) value was identied for each traceusing a 1 s sliding window, incremented in 100 ms steps.RMS values were normalized for each subject, bydividing the 1 s maximum RMS from each level of thecranio-cervical exion test by the 1 s maximum RMSduring a standardized head lift. The normalized RMSdata for the left and right SCMs were averaged foranalysis.

2.3. Procedure

Subjects received written and verbal informationabout test procedures and informed consent wasobtained. Demographic details were obtained from all

subjects and the neck pain subjects rated their pain onthe VAS.

Subjects were positioned in supine lying with the headand neck in a mid position such that the face line washorizontal and an imaginary horizontal line bisected theneck longitudinally. If necessary, layers of towel wereplaced under the head to gain the position. Subjectswere fully familiarized with the C-CFT by the researcherwho was skilled in the clinical test procedure. Theyparticipated in a practice session with the pressurebiofeedback during which time the researcher correctedperformance.

EMG electrodes were applied over the lower one-third of the SCM following skin preparation involvingmild abrasion with ne sandpaper and cleaning with anisopropyl alcohol swab. The subject was rst required toperform a head lift by tucking their chin in and liftingthe head to just clear the bed. A 10 s recording was madefor later normalization procedures. The pressure bagwas placed behind the subjects cervical spine andinated until a stable pressure of 20mmHg wasachieved. The researcher instructed the subject toperform the C-CFT to target 22 mmHg and hold theposition steady. A research assistant operated thecomputer system. A 10 s recording was made for each

stage to capture the 5 s holding time. Subjects thenrested for 10 s. With a similar procedure, the subjectsequentially targeted the other four levels of the test tothe maximum of 30 mmHg.

2.4. Statistical analysis

The analysis of the SCM RMS values required a logtransformation to remove the skewness in the originalmeasure. A saturated design model was tted initiallyand non-signicant terms were removed. A mixed modelANOVA was used to investigate within and betweengroup differences in the normalized RMS values for theSCM muscles for the factors of age, gender and stagesof the C-CFT. Boxplots of the pressure data indica-ted possible differences in the means for the shortfallin pressures from the designated pressure levels of theC-CFT across groups and pressure levels. Variancesbetween measurements within groups indicated thatmodels needed to include terms for this heteroscedacity.The linear effects model used to model target pressureerror included specic variance functions modellingvariance as a power of the pressure level covariate.

3. Results

The demographic details for each subject group aswell as the length of history and VAS scores for the neckpain groups are presented in Table 1 . The only obviousdifference between the groups was the length of history

of the insidious onset neck pain group compared to thewhiplash group. The results of primary analyses forSCM normalized RMS values revealed signicantdifferences between groups P 0:001 and stages of the test P 0:001: There were no signicant effects forgender P 0:51 or age P 0:62: The analysisrevealed a strong positive linear relationship betweenSCM normalized RMS values and stage of the C-CFT,but the relationship levelled off for the whiplash groupat the highest pressure target ( Fig. 2 ). Both the neck painand whiplash groups had signicantly higher SCMnormalized RMS values than the control group at eachstage of the C-CFT (all P o 0:05). However there wereno signicant differences in SCM normalized RMS

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Table 1Characteristics of the subject groups

Controlsn 25

Neck painn 25

Whiplashn 25

Gender (females %) 60 80 68Age (years, mean 7 SD) 39.3 7 14.0 40.3 7 9.2 36.3 7 10.2Length of history (years) 8.5 7 6.0 1.8 7 1.1Average pain (VAS 010) 6.3 7 1.5 6.2 7 2.3

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values between the neck pain and whiplash groups withthe exception of the 22 mmHg stage P 0:02: Theanalysis was repeated for the insidious onset neck painand whiplash groups using length of history of neck painas a covariate and results remained unchanged.

The differences between the target pressure and themean pressure achieved for each stage of the test foreach group are presented in Fig. 3 . Within the teststages, the mean shortfalls in pressure for the neck painand whiplash groups were not signicantly different atany stage of the test P > 0:05; but those of both groupswere signicantly greater than the control groupP o 0:002: The exception was at the 22 mmHg targetwhere the mean for the neck pain group was notsignicantly different from the control group P 0:11:

4. Discussion

Dysfunction in the neck exor muscles has beenfound to be associated with neck pain of both whiplash

and insidious origins ( Jull et al., 1999, 2000 ; Sterlinget al., 2001 ; Vernon et al., 1992 ; Watson and Trott,1993). However there has been little investigation intowhether or not differences exist between the groupswhich might impact on the rehabilitation process.

The results of this study revealed a strong linear

relationship between the magnitude of the SCMnormalized 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 andwhiplash groups in all stages of the C-CFT compared tothe asymptomatic control group. This is in accord withthe ndings of previous studies of subjects with WADand insidious onset neck pain ( Jull, 2000 ; Sterling et al.,2001). No signicant differences were evident betweenthe neck pain and WAD groups indicating that thisphysical impairment or altered pattern of muscle co-ordination is common to neck pain of both whiplashand insidious origin and would not seem to be a reasonwhy patients with chronic WAD often are morechallenging to treat than patients with insidious originneck pain.

Cranio-cervical exion is the action of longus capitisin synergy with longus colli. The presence of progres-sively increasing SCM normalized RMS values in eachtest stage in all subject groups suggests that thesemuscles were recruited to further stabilize the neck asthe contractile demand of the longus capitis increased inthe inner ranges of cranio-cervical exion. The presenceof higher SCM normalized RMS values in the neck paingroups infers that altered patterns of co-ordination may

be present between the deep and supercial exormuscles in patients with neck pain, and this higheractivity may be a measurable compensation ( Cholewickiet al., 1997 ) for poorer active contractile capacity of thelongus colli and capitis muscles. The clinical version of the C-CFT used in this study has the decit of no directmeasure of the activity of longus capitis and colli. Themuscles are deep and not accessible for use of conventional surface EMG. Falla et al. (2003b) used anovel surface EMG electrode in a laboratory version of the C-CFT. A bipolar surface electrode was inbuilt intoa nasopharageal suction catheter and the electrode wasinserted via the nasal passage and suctioned onto theback of the throat adjacent to the uvula, over the longuscapitis and colli. In their study on asymptomaticsubjects, they demonstrated a stronger linear relation-ship between the amplitude of the deep neck exormuscle signal and the increasing incremental stages of the test, which conrms anatomical predictions for thetest. In a further study of 10 neck pain and 10 controlsubjects, Falla et al. (2003c) again demonstrated astrong linear relationship between the EMG amplitudeof the deep neck exor muscles and the incrementalstages of the C-CFT for both control and neck painsubjects. However, the amplitude of deep neck exor

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22mmHg 24mmHg 26mmHg 28mmHg 30mmHg

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

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



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EMG was less in the neck pain group than for thecontrol group and the difference was signicant forthe higher levels of the test. Although not signicant,there was a strong trend for greater EMG activity in theSCM and anterior scalene muscles in the neck paingroup. These ndings lend support to the contention

that the higher levels of SCM normalized RMSvalues measured in all stages of the C-CFT in our studyof neck pain patients as compared to the controlsubjects may reect a compensation strategy for poorercontractile capacity of the deep cervical exors. Furtherstudy on larger sample sizes to better understand thecompensation strategies in the C-CFT as well as theirsensitivity and specicity to neck pain patients iswarranted.

The pressure unit, which is inserted behind the neck inthe C-CFT, monitors the slight attening of the cervicalspine accompanying the contraction of the longus colli(Mayoux-Benhamou et al., 1994 ). The results of thedifferences between the pressure target and that attainedby the subjects in this study revealed that the controlgroup could quite accurately perform and control thecranio-cervical exion action to the designated pressuresof each task ( Fig. 3 ). In contrast, both neck pain groupsdemonstrated larger pressure shortfalls at all stages of the C-CFT. This again would infer poorer activecontractile capacity of the longus colli to atten thecervical curve, particularly in the latter three stages of the test. At the 30 mmHg stage of the test, the WADgroup had a particularly large shortfall indicating thatmany of the subjects could not perform this stage of the

test. This was associated with a levelling off of the EMGnormalized RMS values in the WAD group at the teststage. Thus the results of the study show that the neckpain groups of both insidious and whiplash origin havedifculty attaining the pressure targets of the test and inassociation they both exhibit higher normalized RMSvalues in the SCM, indicating similar impairment in theneck exor synergy.

The neck pain groups were of similar age and genderand reported similar levels of pain associated with theircondition, although the insidious onset neck pain grouphad a longer history of their condition than the whiplashgroup. These differences in length of history did notimpact on results. Similar ndings 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 :77 1:3 years) and patients with chronic non-specic neck pain (6 :77 5:6 years). These authorsconcluded that cervical muscle dysfunction was appar-ently not related to a specic traumatic injury as wasalso found in this study. Thus these changes in musclefunction appear not to be time dependent beyond acertain point and the common factor may be thepresence of pain.

5. Conclusion

This study has determined that altered patternsmuscle co-ordination within the neck exor synergyare present in patients with neck pain of whiplash andinsidious origin as evident in the C-CFT. It appears that

this physical impairment between the two groups issimilar and of itself would not account for the greaterdifculty often encountered in the rehabilitation of patients following whiplash.

Acknowledgements

The authors acknowledge the nancial support forthis research from the Centre of National Research onDisability and Rehabilitation Medicine (CONROD,Queensland, Australia) and from the Association of

Icelandic Insurance Companies.

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