Development of motor system dysfunction following whiplash injury

 
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Pain 103 (2003) 65–73
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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 the
early stages following injury and of its progress in those persons who recover and those who develop persistent symptoms. This study
measured prospectively, motor system function (cervical range of movement (ROM), joint position error (JPE) and activity of the superficial
neck flexors (EMG) during a test of cranio-cervical flexion) as well as a measure of fear of re-injury (TAMPA) in 66 whiplash subjects within
1 month of injury and then 2 and 3 months post injury. Subjects were classified at 3 months post injury using scores on the neck disability
index: recovered (,8), mild pain and disability (10–28) or moderate/severe pain and disability (.30). Motor system function was also
measured in 20 control subjects. All whiplash groups demonstrated decreased ROM and increased EMG (compared to controls) at 1 month
post injury. This deficit persisted in the group with moderate/severe symptoms but returned to within normal limits in those who had
recovered 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/severe
group 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                                                                risk of persistent symptoms and facilitate the development
                                                                               of appropriate treatment strategies.
   The development of chronic whiplash associated disorder                        Motor system dysfunction is present in persons with
(WAD) occurs in 12–40% of those who sustain a whiplash                         persistent WAD. Changes observed include reduced cervi-
injury to the cervical spine and contributes substantially to                  cal spine movements, disturbances in cervical kinaesthesia
the economic and social costs related to this condition                        reflected by errors in head and neck repositioning and
(Barnsley et al., 1994; Eck et al., 2001). Previous research                   increased electromyographic (EMG) activity in neck and
has indicated that those persons with persistent symptoms of                   shoulder girdle muscles (Heikkila and Astrom, 1996; Oster-
WAD more than 3 months after injury display changes in                         bauer et al., 1996; Bono et al., 2000; Jull, 2000; Nederhand
cervical motor system function (Heikkila and Astrom, 1996;                     et al., 2000; Dall’Alba et al., 2001; Dumas, 2001; Elert et
Nederhand et al., 2000; Dall’Alba et al., 2001; Dumas,                         al., 2001). Increased EMG activity has been demonstrated
2001; Elert et al., 2001). However, little is known about                      during tasks of high load demand but perhaps more relevant
the early stages following an injury and of the progress in                    to WAD, also with functional low load activities. Neder-
the motor system in those who do or do not recover within 3                    hand et al. (2000), using a single arm task, showed increased
months of the injury. An understanding of these changes                        EMG activity in upper trapezius muscles both during and
early on after injury may enhance identification of those at                   after the movement. Jull (2000) demonstrated increased
                                                                               activity of the superficial neck flexor muscles during a
                                                                               task of supported cranio-cervical flexion in subjects with
                                                                               persistent WAD. These changes in EMG activity have
 * Corresponding author. Tel.: 1 61-7-3365-4568; fax: 161-7-3365-              been interpreted as reflecting altered muscle recruitment
2775.
   E-mail address: m.sterling@shrs.uq.edu.au (M. Sterling).
                                                                               patterns (Nederhand et al., 2000, Jull, 2000).

0304-3959/02/$30.00 q 2002 International Association for the Study of Pain. Published by Elsevier Science B.V. All rights reserved.
PII: S 0304-395 9(02)00420-7
66                                           M. Sterling et al. / Pain 103 (2003) 65–73

   Psychological factors such as beliefs about movement              medical research ethics committee of the University of
induced pain and re-injury may also influence motor                  Queensland, the Royal Australian College of General Prac-
dysfunction observed in patients with persistent WAD                 titioners and from the ethics committee of the Royal Bris-
(Nederhand et al., 2002). Fears of movement and re-injury            bane Hospital.
have been associated with lumbar paraspinal muscle activity
in chronic low back pain (Watson et al., 1997). Similarly,           2.3. Active range of movement
fear of pain (induced experimentally) can alter lumbar spine
                                                                        Range of active cervical movement was measured in
muscle recruitment patterns albeit in asymptomatic subjects
                                                                     three dimensions using an electromagnetic, motion-tracking
(Moseley et al., 2002). Beliefs about fear of movement and
                                                                     device (Fastrak, Polhemius, USA) (Trott et al., 1996;
re-injury (TAMPA) are yet to be investigated in WAD.
                                                                     Dall’Alba et al., 2001). Output from the device was
   Our study addressed the lack of information on changes in
                                                                     converted to Euler angles to describe the motion of sensor
motor system function soon after whiplash injury and the
                                                                     1 (placed on the forehead) relative to sensor 2 (placed over
time course of such changes in those who recover and those
                                                                     C7). A custom computer program was developed to allow
who report persistent pain. The aims of this study were
                                                                     real-time viewing of the motion trace, placement of markers
threefold: to investigate the differences in motor system
                                                                     in the data trace and storage of data. The Fastrak system has
function between those who recover and those who report
                                                                     been used previously to investigate cervical range of move-
persistent symptoms based on their status at 3 months post
                                                                     ments (ROM) in neck pain disorders (Dall’Alba et al., 2001)
whiplash injury; to investigate the prospective longitudinal
                                                                     and has been shown to be accurate to within ^0.28 (Pearcy
development of changes in motor system function following
                                                                     and Hindle, 1989).
whiplash injury; to determine whether TAMPA influences
any observed changes in motor function. Three aspects of             2.4. Cervical joint position error
motor system function were chosen for investigation – range
of cervical movement, kinaesthetic awareness and EMG                    Joint position error (JPE) was measured according to
activity of neck flexor muscles during cranio-cervical flex-         Revel et al. (1994) by using the Fastrak system and set-up
ion.                                                                 described for ROM. The subjects’ ability, whilst blind-
                                                                     folded, to relocate the head to a natural head posture was
                                                                     measured following active cervical left and right rotation
2. Methods
                                                                     and extension.
2.1. Study design                                                    2.5. Superficial neck flexor muscle activity
   A prospective longitudinal design was used to study                   Surface EMG was used to measure the activity of the
persons who sustained a whiplash injury from within 1                superficial neck flexor muscles during the cranio-cervical
month of injury to 3 months post injury. They were assessed          flexion test (CCFT) (Jull, 2000; Sterling et al., 2001). The
at three time frames – within 1 month of injury, 2 and 3             CCFT is a progressively staged test of cranio-cervical flex-
months post injury. An asymptomatic control group was                ion performed in the supine lying position without resis-
assessed at three parallel time frames each 1 month apart.           tance. Subjects are guided to progressively increasing
                                                                     ranges of flexion with use of biofeedback provided by an
2.2. Subjects                                                        air filled pressure sensor positioned behind the neck which
                                                                     monitors the slight flattening of the cervical lordosis which
   Sixty-six volunteers (21 males, 45 females, mean age
                                                                     occurs with the test action (Mayoux-Benhamou et al., 1994;
36.27 ^ 12.69 years) reporting neck pain as a result of a
                                                                     Falla et al., 2002a). To ensure high fidelity feedback, the
motor vehicle crash and 20 healthy asymptomatic volun-
                                                                     pressure sensor was calibrated at regular intervals through-
teers (eight males, 12 females, mean age 40.1 ^ 13.6
                                                                     out the study using a compression tension test device. Pairs
years) participated in the study. The whiplash subjects
                                                                     of standard Ag–AgCl electrodes (Conmed, USA) were posi-
were recruited through hospital accident and emergency
                                                                     tioned along the lower one third of the muscle bellies of both
departments, primary care practices (medical and
                                                                     sternocleidomastoid (SCM) muscles (Falla et al., 2002b).
physiotherapy) and from advertisement within radio and
                                                                     The EMG signals were passed through a 10 Hz high-pass
print media. They were eligible if they met the Quebec
                                                                     filter and amplified to 20,000 units using an AMLAB data
Task Force Classification of WAD II or III (Spitzer et al.,
                                                                     acquisition system (Associated Measurements Pty Ltd,
1995). WAD IV patients were excluded. The asymptomatic
                                                                     Australia).
control group was recruited from the general community
from print media advertisement. The asymptomatic subjects            2.6. Questionnaires
were included, provided they had never experienced any
prior pain or trauma to the cervical spine, head or upper              Self reported pain and disability was measured in all
quadrant.                                                            whiplash subjects using the neck disability index (NDI)
   Ethical clearance for this study was granted from the             (Vernon and Mior, 1991). They also completed the measure
M. Sterling et al. / Pain 103 (2003) 65–73                                          67

of TAMPA questionnaire as an indicator of the fear of                   disability (10–28 NDI) and moderate/severe pain and
movement/re-injury (Kori et al., 1990). As the control                  disability (.30 NDI) (Vernon, 1996).
subjects had never experienced neck pain it was deemed                     Initial analysis was performed using a repeated measures
inappropriate for them to complete the questionnaires.                  mixed model analysis of variance (ANOVA) with a between
                                                                        subjects factor of group (four levels: asymptomatic, recov-
2.7. Procedure                                                          ered, mild, moderate/severe) and a within subjects factor of
                                                                        time (three levels: ,1 month, 2 and 3 months post injury).
   The following measures were undertaken at each of the
                                                                        Age and gender were used as covariates in this analysis.
three time points. The whiplash subjects first completed the
                                                                        Differences between groups were analysed using a priori
NDI and TAMPA questionnaires. Testing of both whiplash
                                                                        contrasts. Where a significant interaction occurred between
and asymptomatic subjects was performed in the following
                                                                        group and time, post hoc tests of simple effects were
sequence ROM, JPE and CCFT. The same examiner (M.S.)
                                                                        performed at entry into the study (,1 month) and exit
performed all tests. This examiner remained blind to the
                                                                        from the study (3 months) to determine where these differ-
subjects’ responses on the NDI and TAMPA questionnaires.
                                                                        ences occurred. A repeated measures mixed model ANOVA
For all tests no verbal cues/feedback were given to the
                                                                        with a time-changing covariate of TAMPA was used to
subjects about their performance.
                                                                        assess the effect of TAMPA on the measures of the whiplash
   After completion of the questionnaires, the subjects were
                                                                        groups. Significance was set at P , 0:01.
seated, the Fastrak sensors applied and ROM was measured.
Subjects were instructed to assume a comfortable position
looking straight ahead, then to perform each movement                   3. Results
three times. They were encouraged to move at a comfortable
speed, as far as possible each time and return to the start             3.1. Subject classification on NDI at 3 months post injury
positioning between each repetition. The order of move-
ments assessed was flexion, left lateral flexion, right lateral            The NDI scores at 3 months post injury improved or
flexion, left rotation, right rotation and extension. Means of          remained the same compared to the initial scores (Fig. 1)
the three trials for each direction of ROM were calculated              and were significantly different between the three whiplash
and used for analysis.                                                  groups (P , 0:01). The NDI of the recovered group was
   Subjects were then blindfolded and kinaesthetic testing              3 ^ 3.1 (mean ^ SD), the mild group 18.5 ^ 5.2 and the
was performed. They were asked to perform the neck move-                moderate/severe group 47.9 ^ 12.2. Thirty eight percent
ments within comfortable limits and return as accurately as             of the whiplash subjects reported recovery by 3 months
possible to the starting position, which they indicated verb-           post injury. Of the remaining whiplash subjects with persis-
ally. This position was recorded electronically. Three trials           tent symptoms at 3 months, 33% reported mild pain and
of each movement direction were performed in the follow-                disability and 29% moderate/severe pain and disability
ing order – left rotation, right rotation and extension. Prior          based on NDI scores at 3 months. Age and gender distribu-
to each new movement direction, the subjects were able to               tion of the four groups is illustrated in Table 1. There was an
re-align their starting position to a visible target before             uneven distribution of males and females and differences in
being blindfolded again. JPE was calculated by using the                ages between the groups approached significance
mean of the absolute errors for the three trials of each move-          (P ¼ 0:03). As a consequence, age and gender were
ment for the primary movement direction.                                included as covariates in the initial analysis.
   The subjects were then positioned supine, EMG electro-
des were applied and the CCFT was performed. Each stage                 3.2. Range of movement
of the test was held for 10 s. For purposes of normalisation
                                                                           There was a significant main effect for group (P ¼ 0:007)
of EMG data, a standard head lift task was performed. This
                                                                        and an interaction between group and time (P ¼ 0:02) for
involved the participant performing cranio-cervical flexion
                                                                        all movement directions except lateral flexion (P . 0:1).
and just lifting the head off the plinth. This method of
                                                                        Due to interaction effects, group differences for flexion,
normalisation of the superficial neck flexors has been used
                                                                        extension, left and right rotation were examined at entry
previously (Sterling et al., 2001). For EMG data, the 1 s of
                                                                        into the study (,1 month) and exit from the study (3
maximum root mean square (RMS) values was calculated
                                                                        months).
for each stage of the test. The maximum RMS was standar-
                                                                           The groups who reported mild symptoms and moderate/
dised against EMG activity in the superficial neck flexor
                                                                        severe symptoms at 3 months had less range of flexion,
muscles during the standard head lift task.
                                                                        extension, left and right rotation when compared to controls
2.8. Data analysis                                                      at the entry point into the study (,1 month post injury),
                                                                        (P , 0:01). There was no difference between these two
  The whiplash subjects were classified into one of three               whiplash groups for any of these movement directions at
groups based on results of the NDI at 3 months post injury.             entry (P . 0:49). The group who recovered showed greater
The groups were recovered (,8 NDI), mild pain and                       range of extension than the other two whiplash groups
68                                                       M. Sterling et al. / Pain 103 (2003) 65–73

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/severe
pain and disability (.30 NDI) and recovered (,8 NDI).

(P , 0:005) at entry but less than that of the control group                      (marginal mean ^ SEM) compared to all other groups
(P , 0:01). Range of movement of the groups who recov-                            (P , 0:01). There were no between group differences in
ered or reported mild symptoms improved with time. At 3                           those who recovered (3.6 ^ 0.58), those with persistent
months post injury, their movement (in all directions) was                        mild symptoms (2.7 ^ 0.48) and the control group
no longer different from controls (P . 0:3). In contrast, the                     (2.8 ^ 0.58) (P . 0:1). There was no effect of age or gender
movement loss at entry persisted in the group with moder-                         on JPE (P . 0:06) (Table 2).
ate/severe symptoms and remained less than that of the
control group at 3 months – the final assessment point                            3.4. EMG activity of superficial neck flexors
(P , 0:01). The marginal means (^SEM) of the four
                                                                                     There was no interaction effect between group and time
groups for the movements of flexion, extension, left and
                                                                                  for the EMG activity measured during the stages of the
right rotation are presented in Figs. 2 and 3. The effect of
                                                                                  CCFT. Analysis of the main effects revealed a significant
age on range of movement was significant only for exten-
                                                                                  difference in EMG activity between the groups
sion, left and right rotation (P , 0:01), with ROM decreas-
                                                                                  (P , 0:0001) and this difference persisted over time (Fig.
ing with increasing age. There was no effect of gender on
                                                                                  5). EMG activity of the superficial neck flexors in the group
any measure of ROM (P . 0:2).
                                                                                  with moderate/severe symptoms was 40 ^ 4% (estimated
                                                                                  mean ^ SEM), which was significantly greater than the
3.3. JPE                                                                          EMG activity recorded for all other groups (P , 0:01).
                                                                                  EMG activity of the groups who recovered (29 ^ 4%) or
   The results of data for JPE are presented in Fig. 4. There
                                                                                  had mild symptoms at 3 months (27 ^ 3%) was also signif-
was no interaction effect between group and time for all
                                                                                  icantly greater than that of the control group (16 ^ 3%)
three measures of JPE, indicating that there was no change
                                                                                  (P , 0:01). There was no effect of age or gender on EMG
over time in any JPE direction. When the main effects were
                                                                                  (P . 0:2).
considered, there was a significant difference between the
groups for JPE (right rotation) (P ¼ 0:002) but no group                          3.5. TAMPA
difference for JPE (left rotation, extension) (P . 0:3). The
group with persistent moderate/severe symptoms had a                                There was a significant difference between the three
significantly greater JPE (right rotation) of 4.8 ^ 0.48                          whiplash groups for the TAMPA score (P ¼ 0:0001). As

Table 1
The 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 ^ 3.1
Mild pain and disability group        22             34.7 ^ 12.6                       64                       10–28                    18.5 ^ 5.2
Moderate/severe pain and              19             41.3 ^ 13.6                       84                       . 30                     47.9 ^ 12.2
  disability group
Control group                         20             40.1 ^ 13.6                       60                       –                        –
M. Sterling et al. / Pain 103 (2003) 65–73                                                       69

                                                                                 percent of our cohort, of volunteers sustaining a whiplash
                                                                                 injury, reported ongoing pain at 3 months post injury, a
                                                                                 similar 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 reported
                                                                                 persistent moderate or severe symptoms. Values obtained
                                                                                 for control subjects for all measures of motor function were
                                                                                 similar 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 in
                                                                                 the group who reported moderate/severe symptoms at 3
                                                                                 months, while movement in the groups who reported mild
                                                                                 symptoms or who had recovered at 3 months improved with
                                                                                 time and returned to ranges that were no longer different
                                                                                 from healthy controls. Most cross-sectional studies investi-
                                                                                 gating ROM in chronic WAD have demonstrated decreased
                                                                                 cervical movement (Osterbauer et al., 1996; Bono et al.,
                                                                                 2000; Dall’Alba et al., 2001; Dumas, 2001). However, a
                                                                                 recent longitudinal study suggested that although ROM
                                                                                 was decreased in the first few weeks after injury, by 3
Fig. 2. Means and standard errors of the mean (SEM) for all groups (control,     months this loss was regained (Kasch et al., 2001) which
recovered, mild pain and moderate/severe pain) over time (1, 2 and 3             seems at odds with our findings. However, Kasch et al.
months post injury) for active range of extension and flexion.                   (2001) did not attempt to differentiate between recovered
                                                                                 and non-recovered subjects as we did. The findings of our
can be seen from the mean values in Fig. 6, the group with                       study reinforce the need to not only differentiate between
persistent moderate/severe symptoms had significantly                            recovered and non-recovered subjects but also between
higher TAMPA scores than the other two groups (marginal                          those who continue to report higher levels of pain and
mean 40.55 ^ 2). In the groups who recovered or reported                         disability from those with mild symptoms.
mild symptoms at 3 months, the TAMPA scores improved
significantly over time (P , 0:05) whereas there was no
change over time in the scores of the moderate/severe
group (P ¼ 0:783).
   When TAMPA scores were included in the analysis of the
three 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 the
time points described above also remained significant
(P , 0:01). There was no interaction between group and
TAMPA for any measure of motor function (P . 0:13)
suggesting that the effect of TAMPA on the motor measures
is similar irrespective of group allocation. The effect size for
TAMPA 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 early
changes in motor system function following whiplash
injury. 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 who
recovered and those with persistent mild symptoms. In all                        Fig. 3. Means and standard errors of the mean (SEM) for all groups (control,
whiplash groups certain specific changes in motor system                         recovered, mild pain and moderate/severe pain) over time (1, 2 and 3
function persisted over the 3 month study period. Sixty-two                      months post injury) for active range of left and right rotation.
70                                                        M. Sterling et al. / Pain 103 (2003) 65–73

Fig. 4. Means and standard errors of the mean (SEM) for all groups (control, recovered, mild pain and moderate/severe pain) over time (1, 2 and 3 months post
injury) for joint position error (JPE) from right rotation.

   Evidence of altered kinaesthetic awareness as measured                         during the CCFT is thought to be indicative of alterations in
using JPE was apparent only in the group of whiplash                              patterns of muscle activation and recruitment and has been
subjects reporting persistent moderate/severe pain at 3                           identified in patients with chronic neck pain of both trau-
months. This occurred in one movement direction – reloca-                         matic and non-traumatic origin (Jull, 2000; Jull et al., 2002).
tion from right rotation, was present within 1 month of                           This study demonstrates that these changes occur soon after
injury and showed no change over time. These results                              injury and persist not only in those reporting ongoing symp-
support our previous research where chronic WAD subjects                          toms at 3 months post injury but also in those whose symp-
with a higher neck disability index (in this case the North-                      toms have resolved during this time. Research into low back
wick Park questionnaire) demonstrated greater JPE (Trelea-                        pain has shown that altered muscle recruitment persists
ven et al., 2002). Whilst only relocation from right rotation                     despite the patient reporting recovery and may be one factor
was affected in this current study, previous researchers have                     involved in high rate of symptom recurrence in this condi-
noted errors in chronic WAD subjects in other movement                            tion (Hides et al., 2001). Whether the whiplash patients who
directions including extension, flexion and left rotation                         recovered in this study continue to demonstrate increased
(Heikkila and Astrom, 1996; Treleaven et al., 2002)                               muscle activity past the 3 month period and whether this
although Treleaven et al. (2002) showed greater JPE with                          group reports recurrence of pain at some later date is
right rotation. The reasons for this discrepancy are unclear.                     presently under investigation.
The majority of subjects (16 of 19) in the moderate/severe                           The contribution of physical and psychosocial factors to
group reported bilateral neck pain discounting the possibi-                       the development of chronic symptoms has been studied
lity that the side of pain is responsible for this finding. Hand                  extensively in chronic low back pain (Fritz et al., 2001),
dominance was not considered in this study and could be                           but very little attention has been paid to their role in cervical
associated with this finding. Additionally, the subjects in                       spine pain. Whilst the moderate/severe group in this study
this study were only 3 months post injury as opposed to                           showed elevated scores on the TAMPA scale – similar to
the above-mentioned studies using chronic WAD subjects                            those seen in chronic low back pain (Crombez et al., 1999),
with longer symptom duration. Whether JPE in other direc-                         differences in motor function between the whiplash groups
tions emerge in time remains to be seen and may require                           remained significant when TAMPA scores were taken into
further investigation.                                                            account. Furthermore the relationship between TAMPA and
   Increased activity in the superficial neck flexor muscles                      the measures of motor function was weak. This would

Table 2
Marginal means (SEM) of joint position error (JPE) right and left rotation and extension for all groups a

Group                                            JPE (right rotation)               JPE (left rotation)                 JPE (extension)
                                                 (mean ^ SEM)                       (mean ^ SEM)                        (mean ^ SEM)

Recovered                                        3.6 ^ 0.3                          3.0 ^ 0.2                           3.3 ^ 0.3
Mild pain and disability                         2.7 ^ 0.3                          2.7 ^ 0.2                           3.4 ^ 0.3
Moderate/severe pain and disability              4.8 ^ 0.3                          3.2 ^ 0.3                           4.1 ^ 0.3
Controls                                         2.7 ^ 0.3                          2.6 ^ 0.3                           2.8 ^ 0.3
 a
     Values in bold are significantly greater than control for P , 0:01.
M. Sterling et al. / Pain 103 (2003) 65–73                                                       71

Fig. 5. Normalised EMG (mean and SEM) of the superficial neck flexors for all groups (control, recovered, mild pain and moderate/severe pain) over time (1,2
and 3 months post injury) during the CCFT.

suggest that ROM loss, increased superficial neck flexor                         recruitment patterns and effects on supraspinal neurons
muscle activity during the CCFT and JPE occurred indepen-                        (Woolf and Wall, 1986; Mense and Skeppar, 1991; Made-
dently of fear of movement/re-injury. The finding that                           leine et al., 1999; Andersen et al., 2000; Ro and Capra,
increased muscle activity occurred in the WAD subjects                           2001; Thurnberg et al., 2001). Most of these studies have
even when controlled for TAMPA beliefs occur is contrary                         used animal models or induced experimental muscle pain as
to findings in chronic low back pain where abnormal para-                        a model for acute pain making it difficult to extrapolate the
spinal muscle activity has shown to be influenced by                             findings to the clinical situation. Furthermore little is known
psychological factors (Watson et al., 1997). Our findings                        about the long-term nature of such changes. Nevertheless
indicate that motor system changes in this population are                        evidence from clinical studies of chronic pain would suggest
not totally explained by the subjects’ TAMPA, confirming                         that certain motor system changes do persist (Hodges and
suggestions that the relationship between fear-avoidance                         Richardson, 1999; Madeleine et al., 1999). The findings of
beliefs and disability in cervical pain may be weaker than                       this study may reflect underlying disturbances in motor
that for lumbar pain (George et al., 2001).                                      function as a consequence of the initial peripheral nocicep-
   Experimental investigations have provided evidence that                       tive input (for example from injured cervical structures
acute musculoskeletal pain is capable of inducing changes                        following whiplash injury) in the acute stage of injury,
in motor system function such as alteration of spinal motor                      which appear to persist over time. Further investigation of
reflexes, effects on the gamma motor system, altered motor                       such potential mechanisms in WAD is required.

Fig. 6. Means and standard errors of the mean (SEM) for three whiplash groups (recovered, mild pain and moderate/severe pain) over time (1,2 and 3 months
post injury) for scores of TAMPA questionnaire.
72                                                        M. Sterling et al. / Pain 103 (2003) 65–73

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