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Development of motor system dysfunction following whiplash injury

Development of motor system dysfunction following whiplash injury
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  Development of motor system dysfunction following whiplash injury Michele Sterling a, *, Gwendolen Jull a , Bill Vicenzino a , Justin Kenardy b , Ross Darnell c a The Whiplash Research Unit, Department of Physiotherapy, The University of Queensland, 4072 Brisbane, Australia b  Department of Psychology, The University of Queensland, 4072 Brisbane, Australia c School of Health and Rehabilitation Sciences, The University of Queensland, 4072 Brisbane, Australia Received 1 July 2002; accepted 7 October 2002 Abstract Dysfunction in the motor system is a feature of persistent whiplash associated disorders. Little is known about motor dysfunction in theearly stages following injury and of its progress in those persons who recover and those who develop persistent symptoms. This studymeasured prospectively, motor system function (cervical range of movement (ROM), joint position error (JPE) and activity of the superficialneck flexors (EMG) during a test of cranio-cervical flexion) as well as a measure offear of re-injury (TAMPA) in 66 whiplash subjects within1 month of injury and then 2 and 3 months post injury. Subjects were classified at 3 months post injury using scores on the neck disabilityindex: recovered ( , 8), mild pain and disability (10–28) or moderate/severe pain and disability ( . 30). Motor system function was alsomeasured in 20 control subjects. All whiplash groups demonstrated decreased ROM and increased EMG (compared to controls) at 1 monthpost injury. This deficit persisted in the group with moderate/severe symptoms but returned to within normal limits in those who hadrecovered or reported persistent mild pain at 3 months. Increased EMG persisted for 3 months in all whiplash groups. Only the moderate/ severe group showed greater JPE, within 1 month of injury, which remained unchanged at 3 months. TAMPA scores of the moderate/severegroup were higher than those of the other two groups. The differences in TAMPA did not impact on ROM, EMG or JPE. This study identifies,for the first time, deficits in the motor system, as early as 1 month post whiplash injury, that persisted not only in those reporting moderate/ severe symptoms at 3 months but also in subjects who recovered and those with persistent mild symptoms. q  2002 International Association for the Study of Pain. Published by Elsevier Science B.V. All rights reserved. Keywords : Whiplash; Motor dysfunction; Fear of movement/re-injury 1. Introduction The development of chronic whiplash associated disorder(WAD) occurs in 12–40% of those who sustain a whiplashinjury to the cervical spine and contributes substantially tothe economic and social costs related to this condition(Barnsley et al., 1994; Eck et al., 2001). Previous researchhas indicated that those persons with persistent symptoms of WAD more than 3 months after injury display changes incervical motor system function (Heikkila and Astrom, 1996;Nederhand et al., 2000; Dall’Alba et al., 2001; Dumas,2001; Elert et al., 2001). However, little is known aboutthe early stages following an injury and of the progress inthe motor system in those who do or do not recover within 3months of the injury. An understanding of these changesearly on after injury may enhance identification of those atrisk of persistent symptoms and facilitate the developmentof appropriate treatment strategies.Motor system dysfunction is present in persons withpersistent WAD. Changes observed include reduced cervi-cal spine movements, disturbances in cervical kinaesthesiareflected by errors in head and neck repositioning andincreased electromyographic (EMG) activity in neck andshoulder girdle muscles (Heikkila and Astrom, 1996; Oster-bauer et al., 1996; Bono et al., 2000; Jull, 2000; Nederhand et al., 2000; Dall’Alba et al., 2001; Dumas, 2001; Elert et al., 2001). Increased EMG activity has been demonstratedduring tasks of high load demand but perhaps more relevantto WAD, also with functional low load activities. Neder-hand et al. (2000), using a single arm task, showed increasedEMG activity in upper trapezius muscles both during andafter the movement. Jull (2000) demonstrated increasedactivity of the superficial neck flexor muscles during atask of supported cranio-cervical flexion in subjects withpersistent WAD. These changes in EMG activity havebeen interpreted as reflecting altered muscle recruitmentpatterns (Nederhand et al., 2000, Jull, 2000). Pain 103 (2003) 65–730304-3959/02/$30.00 q  2002 International Association for the Study of Pain. Published by Elsevier Science B.V. All rights reserved.PII: S0304-3959(02)00420-7www.elsevier.com/locate/pain* Corresponding author. Tel.: 1 61-7-3365-4568; fax:  1 61-7-3365-2775. E-mail address:  m.sterling@shrs.uq.edu.au (M. Sterling).  Psychological factors such as beliefs about movementinduced pain and re-injury may also influence motordysfunction observed in patients with persistent WAD(Nederhand et al., 2002). Fears of movement and re-injuryhave been associated with lumbar paraspinal muscle activityin chronic low back pain (Watson et al., 1997). Similarly,fear of pain (induced experimentally) can alter lumbar spinemuscle recruitment patterns albeit in asymptomatic subjects(Moseley et al., 2002). Beliefs about fear of movement andre-injury (TAMPA) are yet to be investigated in WAD.Our study addressedthe lackof informationon changes inmotor system function soon after whiplash injury and thetime course of such changes in those who recover and thosewho report persistent pain. The aims of this study werethreefold: to investigate the differences in motor systemfunction between those who recover and those who reportpersistent symptoms based on their status at 3 months postwhiplash injury; to investigate the prospective longitudinaldevelopment of changes in motor system function followingwhiplash injury; to determine whether TAMPA influencesany observed changes in motor function. Three aspects of motor system function were chosen for investigation –rangeof cervical movement, kinaesthetic awareness and EMGactivity of neck flexor muscles during cranio-cervical flex-ion. 2. Methods 2.1. Study design A prospective longitudinal design was used to studypersons who sustained a whiplash injury from within 1month of injury to 3 months post injury. They were assessedat three time frames – within 1 month of injury, 2 and 3months post injury. An asymptomatic control group wasassessed at three parallel time frames each 1 month apart. 2.2. Subjects Sixty-six volunteers (21 males, 45 females, mean age36.27 ^ 12.69 years) reporting neck pain as a result of amotor vehicle crash and 20 healthy asymptomatic volun-teers (eight males, 12 females, mean age 40.1 ^ 13.6years) participated in the study. The whiplash subjectswere recruited through hospital accident and emergencydepartments, primary care practices (medical andphysiotherapy) and from advertisement within radio andprint media. They were eligible if they met the QuebecTask Force Classification of WAD II or III (Spitzer et al.,1995). WAD IV patients were excluded. The asymptomaticcontrol group was recruited from the general communityfrom print media advertisement. The asymptomatic subjectswere included, provided they had never experienced anyprior pain or trauma to the cervical spine, head or upperquadrant.Ethical clearance for this study was granted from themedical research ethics committee of the University of Queensland, the Royal Australian College of General Prac-titioners and from the ethics committee of the Royal Bris-bane Hospital. 2.3. Active range of movement  Range of active cervical movement was measured inthree dimensions using an electromagnetic, motion-trackingdevice (Fastrak, Polhemius, USA) (Trott et al., 1996;Dall’Alba et al., 2001). Output from the device wasconverted to Euler angles to describe the motion of sensor1 (placed on the forehead) relative to sensor 2 (placed overC7). A custom computer program was developed to allowreal-time viewing of the motion trace, placement of markersin the data trace and storage of data. The Fastrak system hasbeen used previously to investigate cervical range of move-ments (ROM) in neck pain disorders (Dall’Alba et al., 2001)and has been shown to be accurate to within ^ 0.2 8 (Pearcyand Hindle, 1989). 2.4. Cervical joint position error  Joint position error (JPE) was measured according toRevel et al. (1994) by using the Fastrak system and set-updescribed for ROM. The subjects’ ability, whilst blind-folded, to relocate the head to a natural head posture wasmeasured following active cervical left and right rotationand extension. 2.5. Superficial neck flexor muscle activity Surface EMG was used to measure the activity of thesuperficial neck flexor muscles during the cranio-cervicalflexion test (CCFT) (Jull, 2000; Sterling et al., 2001). The CCFT is a progressively staged test of cranio-cervical flex-ion performed in the supine lying position without resis-tance. Subjects are guided to progressively increasingranges of flexion with use of biofeedback provided by anair filled pressure sensor positioned behind the neck whichmonitors the slight flattening of the cervical lordosis whichoccurs with the test action (Mayoux-Benhamou et al., 1994;Falla et al., 2002a). To ensure high fidelity feedback, thepressure sensor was calibrated at regular intervals through-out the study using a compression tension test device. Pairsof standard Ag–AgCl electrodes (Conmed, USA) were posi-tioned alongthe lower one third of the muscle bellies of bothsternocleidomastoid (SCM) muscles (Falla et al., 2002b).The EMG signals were passed through a 10 Hz high-passfilter and amplified to 20,000 units using an AMLAB dataacquisition system (Associated Measurements Pty Ltd,Australia). 2.6. Questionnaires Self reported pain and disability was measured in allwhiplash subjects using the neck disability index (NDI)(Vernon and Mior, 1991). They also completed the measure  M. Sterling et al. / Pain 103 (2003) 65–73 66  of TAMPA questionnaire as an indicator of the fear of movement/re-injury (Kori et al., 1990). As the controlsubjects had never experienced neck pain it was deemedinappropriate for them to complete the questionnaires. 2.7. Procedure The following measures were undertaken at each of thethree time points. The whiplash subjects first completed theNDI and TAMPA questionnaires. Testing of both whiplashand asymptomatic subjects was performed in the followingsequence ROM, JPE and CCFT. The same examiner (M.S.)performed all tests. This examiner remained blind to thesubjects’ responses on the NDI and TAMPA questionnaires.For all tests no verbal cues/feedback were given to thesubjects about their performance.After completion of the questionnaires, the subjects wereseated, the Fastrak sensors applied and ROM was measured.Subjects were instructed to assume a comfortable positionlooking straight ahead, then to perform each movementthree times. They were encouraged to move at a comfortablespeed, as far as possible each time and return to the startpositioning between each repetition. The order of move-ments assessed was flexion, left lateral flexion, right lateralflexion, left rotation, right rotation and extension. Means of the three trials for each direction of ROM were calculatedand used for analysis.Subjects were then blindfolded and kinaesthetic testingwas performed. They were asked to perform the neck move-ments within comfortable limits and return as accurately aspossible to the starting position, which they indicated verb-ally. This position was recorded electronically. Three trialsof each movement direction were performed in the follow-ing order – left rotation, right rotation and extension. Priorto each new movement direction, the subjects were able tore-align their starting position to a visible target beforebeing blindfolded again. JPE was calculated by using themean of the absolute errors for the three trials of each move-ment for the primary movement direction.The subjects were then positioned supine, EMG electro-des were applied and the CCFT was performed. Each stageof the test was held for 10 s. For purposes of normalisationof EMG data, a standard head lift task was performed. Thisinvolved the participant performing cranio-cervical flexionand just lifting the head off the plinth. This method of normalisation of the superficial neck flexors has been usedpreviously (Sterling et al., 2001). For EMG data, the 1 s of maximum root mean square (RMS) values was calculatedfor each stage of the test. The maximum RMS was standar-dised against EMG activity in the superficial neck flexormuscles during the standard head lift task. 2.8. Data analysis The whiplash subjects were classified into one of threegroups based on results of the NDI at 3 months post injury.The groups were recovered ( , 8 NDI), mild pain anddisability (10–28 NDI) and moderate/severe pain anddisability ( . 30 NDI) (Vernon, 1996).Initial analysis was performed using a repeated measuresmixed model analysis of variance (ANOVA) with a betweensubjects factor of group (four levels: asymptomatic, recov-ered, mild, moderate/severe) and a within subjects factor of time (three levels: , 1 month, 2 and 3 months post injury).Age and gender were used as covariates in this analysis.Differences between groups were analysed using a prioricontrasts. Where a significant interaction occurred betweengroup and time, post hoc tests of simple effects wereperformed at entry into the study ( , 1 month) and exitfrom the study (3 months) to determine where these differ-ences occurred. A repeated measures mixed model ANOVAwith a time-changing covariate of TAMPA was used toassess the effect of TAMPA on the measures of the whiplashgroups. Significance was set at  P , 0 : 01. 3. Results 3.1. Subject classification on NDI at 3 months post injury The NDI scores at 3 months post injury improved orremained the same compared to the initial scores (Fig. 1)and were significantly different between the three whiplashgroups ( P , 0 : 01). The NDI of the recovered group was3 ^ 3.1 (mean ^ SD), the mild group 18.5 ^ 5.2 and themoderate/severe group 47.9 ^ 12.2. Thirty eight percentof the whiplash subjects reported recovery by 3 monthspost injury. Of the remaining whiplash subjects with persis-tent symptoms at 3 months, 33% reported mild pain anddisability and 29% moderate/severe pain and disabilitybased on NDI scores at 3 months. Age and gender distribu-tion of the four groups is illustrated in Table 1. There was anuneven distribution of males and females and differences inages between the groups approached significance( P ¼ 0 : 03). As a consequence, age and gender wereincluded as covariates in the initial analysis. 3.2. Range of movement  There was a significant main effect for group ( P ¼ 0 : 007)and an interaction between group and time ( P ¼ 0 : 02) forall movement directions except lateral flexion ( P . 0 : 1).Due to interaction effects, group differences for flexion,extension, left and right rotation were examined at entryinto the study ( , 1 month) and exit from the study (3months).The groups who reported mild symptoms and moderate/ severe symptoms at 3 months had less range of flexion,extension, left and right rotation when compared to controlsat the entry point into the study ( , 1 month post injury),( P , 0 : 01). There was no difference between these twowhiplash groups for any of these movement directions atentry ( P . 0 : 49). The group who recovered showed greaterrange of extension than the other two whiplash groups  M. Sterling et al. / Pain 103 (2003) 65–73  67  ( P , 0 : 005) at entry but less than that of the control group( P , 0 : 01). Range of movement of the groups who recov-ered or reported mild symptoms improved with time. At 3months post injury, their movement (in all directions) wasno longer different from controls ( P . 0 : 3). In contrast, themovement loss at entry persisted in the group with moder-ate/severe symptoms and remained less than that of thecontrol group at 3 months – the final assessment point( P , 0 : 01). The marginal means ( ^ SEM) of the fourgroups for the movements of flexion, extension, left andright rotation are presented in Figs. 2 and 3. The effect of age on range of movement was significant only for exten-sion, left and right rotation ( P , 0 : 01), with ROM decreas-ing with increasing age. There was no effect of gender onany measure of ROM ( P . 0 : 2). 3.3. JPE  The results of data for JPE are presented in Fig. 4. Therewas no interaction effect between group and time for allthree measures of JPE, indicating that there was no changeover time in any JPE direction. When the main effects wereconsidered, there was a significant difference between thegroups for JPE (right rotation) ( P ¼ 0 : 002) but no groupdifference for JPE (left rotation, extension) ( P . 0 : 3). Thegroup with persistent moderate/severe symptoms had asignificantly greater JPE (right rotation) of 4.8 ^ 0.4 8 (marginal mean ^ SEM) compared to all other groups( P , 0 : 01). There were no between group differences inthose who recovered (3.6 ^ 0.5 8 ), those with persistentmild symptoms (2.7 ^ 0.4 8 ) and the control group(2.8 ^ 0.5 8 ) ( P . 0 : 1). There was no effect of age or genderon JPE ( P . 0 : 06) (Table 2). 3.4. EMG activity of superficial neck flexors There was no interaction effect between group and timefor the EMG activity measured during the stages of theCCFT. Analysis of the main effects revealed a significantdifference in EMG activity between the groups( P , 0 : 0001) and this difference persisted over time (Fig.5). EMG activity of the superficial neck flexors in the groupwith moderate/severe symptoms was 40 ^ 4% (estimatedmean ^ SEM), which was significantly greater than theEMG activity recorded for all other groups ( P , 0 : 01).EMG activity of the groups who recovered (29 ^ 4%) orhad mild symptoms at 3 months (27 ^ 3%) was also signif-icantly greater than that of the control group (16 ^ 3%)( P , 0 : 01). There was no effect of age or gender on EMG( P . 0 : 2). 3.5. TAMPA There was a significant difference between the threewhiplash groups for the TAMPA score ( P ¼ 0 : 0001). As  M. Sterling et al. / Pain 103 (2003) 65–73 68Table 1The age, gender and classification of subject groups at 3 months according to the NDI scores (Vernon, 1996)Group Number Age (years) (mean ^ SD) Gender % female NDI classification NDI (mean ^ SD)Recovered group 25 33.5 ^ 10.2 60  , 8 3.0 ^ 3.1Mild pain and disability group 22 34.7 ^ 12.6 64 10–28 18.5 ^ 5.2Moderate/severe pain anddisability group19 41.3 ^ 13.6 84  . 30 47.9 ^ 12.2Control group 20 40.1 ^ 13.6 60 – –Fig. 1. Initial (1 month) and final (3 months) classification of whiplash subjects based on NDI scores. Mild pain and disability (10–28 NDI), moderate/severepain and disability ( . 30 NDI) and recovered ( , 8 NDI).  can be seen from the mean values in Fig. 6, the group withpersistent moderate/severe symptoms had significantlyhigher TAMPA scores than the other two groups (marginalmean 40.55 ^ 2). In the groups who recovered or reportedmild symptoms at 3 months, the TAMPA scores improvedsignificantly over time ( P , 0 : 05) whereas there was nochange over time in the scores of the moderate/severegroup ( P ¼ 0 : 783).When TAMPA scores were included in the analysis of thethree whiplash groups, group differences remained signifi-cant for JPE (right rotation) ( P ¼ 0 : 01) and EMG( P , 0 : 01). With respect to ROM, group differences at thetime points described above also remained significant( P , 0 : 01). There was no interaction between group andTAMPA for any measure of motor function ( P . 0 : 13)suggesting that the effect of TAMPA on the motor measuresis similar irrespective of group allocation. The effect size forTAMPA on the measures of motor activity was small(partial eta squared ranged from 0.00006 to 0.02). 4. Discussion The results of this study provide the first evidence of earlychanges in motor system function following whiplashinjury. These changes were apparent within 1 month of injury and occurred not only in those reporting moderate/ severe symptoms at 3 months but also in subjects whorecovered and those with persistent mild symptoms. In allwhiplash groups certain specific changes in motor systemfunction persisted over the 3 month study period. Sixty-twopercent of our cohort, of volunteers sustaining a whiplashinjury, reported ongoing pain at 3 months post injury, asimilar figure to data from previous longitudinal studies(Radanov et al., 1995; Mayou and Bryant, 1996; Gargan et al., 1997). Twenty-nine percent of the cohort reportedpersistent moderate or severe symptoms. Values obtainedfor control subjects for all measures of motor function weresimilar to those previously reported (Revel, 1991; Jull,2000; Dall’Alba et al., 2001).Deficits in cervical ROM were present within 1 month of injury in all whiplash subjects. The loss in ROM persisted inthe group who reported moderate/severe symptoms at 3months, while movement in the groups who reported mildsymptoms or who had recovered at 3 months improved withtime and returned to ranges that were no longer differentfrom healthy controls. Most cross-sectional studies investi-gating ROM in chronic WAD have demonstrated decreasedcervical movement (Osterbauer et al., 1996; Bono et al.,2000; Dall’Alba et al., 2001; Dumas, 2001). However, arecent longitudinal study suggested that although ROMwas decreased in the first few weeks after injury, by 3months this loss was regained (Kasch et al., 2001) whichseems at odds with our findings. However, Kasch et al.(2001) did not attempt to differentiate between recoveredand non-recovered subjects as we did. The findings of ourstudy reinforce the need to not only differentiate betweenrecovered and non-recovered subjects but also betweenthose who continue to report higher levels of pain anddisability from those with mild symptoms.  M. Sterling et al. / Pain 103 (2003) 65–73  69Fig.2. Meansandstandarderrorsofthe mean(SEM)forall groups(control,recovered, mild pain and moderate/severe pain) over time (1, 2 and 3months post injury) for active range of extension and flexion.Fig. 3.Meansandstandarderrorsofthe mean (SEM)forall groups(control,recovered, mild pain and moderate/severe pain) over time (1, 2 and 3months post injury) for active range of left and right rotation.
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