|
THE LATE WHIPLASH
SYNDROME: A PSYCHOPHYSICAL STUDY
Martina Moogc, John
Quintnerb, Toby Halla and Max
Zusmana
a School
of Physiotherapy, Curtin University of Technology, Shenton Park WA
6008 (Australia), bWyllie Arthritis Centre, Shenton Park
WA 6008 (Australia)
cCorresponding Author:
Martina Moog, University of Sydney, Pain
Management and Research Centre, Royal North Shore Hospital, St.
Leonards NSW 2065, Australia, Tel: +61-2-9926 7990, Facsimile:
+61-2-9926 6548, Email: mmoog@doh.health.nsw.gov.au
Category: Clinical
article
Keywords: Whiplash
injury, Allodynia, Secondary Hyperalgesia, Psychophysics,
SCL-90-R
ABSTRACT
Some patients
who have sustained whiplash injuries present with chronic widespread
pain and mechanical allodynia. This single blind, case control matched
study of 43 chronic whiplash patients sought to examine
psychophysical responses to non-noxious stimuli and their
relationship to psychological profiles.
Symptom Check List-90-R, Neck
Disability Index and Shortform McGill Questionnaire were completed
prior to testing. Qualitative stimuli comprised light-touch,
punctate pressure, moderate heat and cold. Additionally, sustained
vibration was administered using a vibrameter which allowed ramping
of either frequency or amplitude.
Twenty-eight
patients reported vibration-induced pain. No control subject
experienced pain in response to vibration. No significant
differences in perception threshold to vibration were noted between
patients and control group. Twenty-three patients and ten control
subjects reported painful responses to cold. Eleven patients and
nine control subjects experienced pain in response to moderate heat.
Four patients rated punctate pressure and one patient rated
light-touch as painful.
SCL-90-R
profiles revealed an overall elevated level of distress in the
whiplash group. No significant difference was found between patients
with and without vibration-induced pain for any dimension of the
SCL-90-R.
Pain
in response to non-noxious stimulation over presumably healthy
tissues suggests that central mechanisms are responsible for ongoing
pain in at least some whiplash patients. The additional findings of
pain on punctate pressure and hyperalgesic responses to heat and
cold stimuli are consistent with enhanced central responsiveness to
nociceptor input. These results have important therapeutic and
prognostic implications.
INTRODUCTION
In
Western societies motor vehicle insurance claims due to
‘whiplash-type’ injuries have been described as reaching ‘epidemic’
proportions (Spitzer et
al., 1995; Ratcliff, 1997). Those who become chronically
disabled impose a major social and financial burden upon society
(Barnsley et al., 1994;
Gargan et al., 1997,
Ferrari and Russel, 1999a).
The
pathogenesis of the so-called ‘late whiplash syndrome’ (Pearce,
1989) is poorly understood (Koelbaek Johansen et al., 1999). Some maintain
that chronic pain and disability reflect the influence of such
‘environmental’ factors as management interventions by health care
professionals and the medico-legal process (Schmand et al., 1998; Ferrari and
Russell, 1999b; Obelieniene et al., 1999; Pearce 1999;
Cassidy et al., 2000).
Others argue that ongoing
pain is likely to have a somatic basis and that any associated
physical and psychological disability are secondary, in so far as
they resolve coincidentally with pain relief (Radanov et al., 1995, Radanov et al. 1999; Wallis et al., 1998). Cervical
zygapophyseal joints have been proposed as a possible anatomical
source of chronic pain in at least 50% of these patients (Wallis et al.,
1997).
Animal
experimental studies have shown that tissue injury causing prolonged
noxious input can produce functional changes within the central
nervous system which are maintained long after nociceptive input has
disappeared or has become minimal (Woolf and Doubell, 1994). This
state, which is known as central sensitization, is manifested as an
increased response or reduced threshold to afferent input, prolonged
after-discharges to repeated stimulation, an expansion of the
receptive fields of dorsal horn neurones and an increase in their
spontaneous activity (Coderre et al., 1993; Devor, 1994;
Koltzenburg et al.,
1994).
The clinical correlates of central
sensitization are likely to be hyperalgesia (an increased response
to a noxious stimulus) (Merskey and Bogduk 1994), allodynia (pain in
response to a non-noxious stimulus) (Merskey and Bogduk 1994),
widespread pain, and stimulus-independent pain (Coderre et al., 1993). There is an
emerging body of evidence derived from psychophysical testing which
is consistent with an underlying state of hypersensitivity in the
central nervous system of patients presenting with chronic neck pain
(including some with pain following whiplash injury) (Hagström and
Carlsson, 1996; Sheather-Reid and Cohen, 1998; Koelbak Johansen et al., 1999).
The aim of this
study was to determine whether such a condition is present in a
larger group of patients fulfilling the criteria for ‘late whiplash
syndrome’. As one of the authors had previously observed that
sustained vibration at 100 Hz (delivered by a commercially available
appliance) was perceived as a painful stimulus by some sufferers of
chronic neck pain, it was decided to use this modality of sensory
testing, in addition to standard tests of cutaneous sensory
function.
MATERIALS AND
METHODS
Subjects
The inclusion
criteria were based on the classification adopted by the Quebec Task
Force (Spitzer et al 1995). Patients in Classes I and II with
symptoms of more than six months duration subsequent to a
motor-vehicle accident (MVA) were selected for the study. Patients
with discernible musculoskeletal disorders, objective neurological
deficits, or obvious psychopathology were not included in the study.
The patient sample was not biased to either age or sex. A control
group consisted of age and sex-matched healthy volunteers with no
complaints of spinal, upper or lower limb pain or of injuries to the
head, shoulder or knee regions necessitating medical treatment or
time off work in the 12 months prior to
testing.
All participants
in the study were unpaid volunteers, living within the Perth
metropolitan area and unconnected with this study. They had been
referred from pain clinics and selected private practices in
rheumatology and physiotherapy. All had given their informed written
consent to a protocol approved by the Ethics Committee of Curtin
University. Patients were allowed to continue taking their usual
medication. It was not considered ethical or practicable to insist
on a “wash-out” period of 24 hours before sensory testing, as many
patients complained of pain that interfered with their ability to
carry out normal daily activities.
Data Collection
Prior to
psychophysical testing, demographic and health-related
questionnaires were administered to all participants. In addition,
specific accident-related information and symptomatology as
recollected from acute phase were collected from the whiplash group.
The Symptom Check List-90-R (SCL-90-R) (Derogatis, 1994) was used to
assess psychological status of all participants. The Neck Disability
Index (NDI) (Vernon, 1996) was used to provide an assessment of the
extent of perceived functional disability in the whiplash
patients.
All sensory
tests were performed by a single individual. Blinding of the
investigator had been considered during the design of the study.
However, it was decided to simulate, as far as possible, the normal
clinical situation. Instructions given to each participant
were standardized and care was taken not to provide information
about expected test outcomes or about the research
hypothesis.
Experiment 1: Qualitative psychophysical
testing
In each participant, four standard
cutaneous stimuli were used (Asbury, 1998). The aim was to stimulate
different types of peripheral receptors using light-touch, punctate
pressure, non-noxious cold and heat and to obtain a descriptive
interpretation of stimulus quality by the participants. The stimuli
were applied in a random order to the skin over the belly of the
upper trapezius muscle on either side and over the central sternum.
Each participant was asked to identify the presence and the quality
of the stimulus for each area. Any differences in reported sensation
between the areas were noted. For the thermal stimuli the
participants were also instructed to rate the intensity of any
painful sensation on a numerical rating scale from 0 to 100.
To elicit a
sensation of light-touch, a cotton ball was fixed to a clamp and
gently stroked four times across each test site. Touch pressure was
applied over each site through a hand held Semmes-Weinstein
monofilament (size 6.45). Two metal probes were used to assess
thermal sensibility (Hot/Cold Discrimination kit with calibrated
thermometers, Smith & Nephew Roylan Inc.). The cold probe was
placed in ice and water (0°C) and the heat
probe in warm water (40-41°C). The
respective probes were maintained at a constant temperature. During
application of heat and cold stimuli, the skin was touched obliquely
with the rounded end of the metal probe for five seconds. The
pressure applied was insufficient to indent the underlying
skin.
Experiment 2: Quantitative psychophysical
testing
Measurements were performed using a
purpose built vibrameter with adjustable frequency (0-100Hz) and
amplitude (0-2.5mm - peak to peak). The vibrating element
produces pure sine waves that are transmitted by a small element,
emerging from a supporting base. The possible influence of different
application pressures on the accuracy of the readings is thereby
minimised when the instrument is gently placed over soft tissues. A
LED display indicates the frequency and amplitude of the delivered
vibratory stimuli. The device was calibrated prior to testing and it
was found to be accurate between 0.02-0.04mm for amplitude and between 1-2Hz for
frequency. The resolution of the instrument was specified as being
below 0.04mm for amplitude and ± 1Hz for frequency.
The vibration device was clamped to the end of
an articulated arm, which was fixed to a portable trolley, thus
ensuring stable application of the stimulus. Vibration was applied
to skin over three test sites on each side of the body: the belly of
the upper trapezius, the belly of the deltoid muscle, and the belly
of the quadriceps muscle.
Different pre-determined test patterns were
used to ensure that the stimulation sequence over the six test sites
was conducted in a random manner. Randomization was necessary to
exclude any potential reporting bias due to testing within or
outside the area of described pain. From the available literature,
it was unclear whether greater mechanical stimulation would result
from increases in vibration frequency or in amplitude. Therefore,
stimulation at each test site commenced alternately either with
increasing frequency or amplitude in an ascending manner.
Vibration perception threshold (VPT) was
determined by the subject operating a buzzer when first becoming
aware of the stimulus. Amplitude or frequency readings were then
recorded. The stimulus was further increased, either to a frequency
of 100Hz, or to an amplitude of 1.0mm, whilst the other modality was kept constant
at 0.2mm or 20Hz respectively. The participants were
instructed to again sound the buzzer at the onset of any
vibration-induced pain (VIP), thus providing an assessment of pain
threshold. The location and the character of this pain were recorded
on a body chart. If the participant was in pain prior to
commencement of vibration testing, the buzzer was to be sounded if
the intensity of pain increased or if pain spread into a ‘new’ body
area. Unless there had been intolerance to submaximal stimulation,
maximum vibration frequency or amplitude was maintained for 30
seconds at each test site.
Statistical methods
Descriptive statistics, normality testing
(Lilliefors statistic) and Mann-Whitney-U test or 2-tail unpaired
t-test were applied to cutaneous and vibration test results, and to
the questionnaire. Pearson’s correlation coefficient or Spearman’s
rank order correlation (rho) were used to assess the relationship
between functional, psychological and pain scores. The significance
level for all parametric/non-parametric tests was set at p<0.05.
A logistic regression model evaluated the prognostic value of
post-injury symptomatology, self-reported pain intensity with
thermal stimuli and questionnaire scores in order to predict the
presence of VIP in the patient group.
Reliability testing (Wilcoxon Signed Rank test
and Spearman Rank Correlation) was conducted for the VPT/VIP in a
subset of 16 healthy control participants and in the first 11
whiplash patients who had responded with VIP and agreed to undergo
repeat testing.
RESULTS
Demographic details
Forty-three patients, comprising 15 males and
28 females, of mean age 37 years (range 12-66 years), complained of
neck and upper back pain of more than 6 months duration (median 18
months) following their involvement in a MVA. The commonest type of
MVA were rear-end collisions (56%), followed in frequency by frontal
(16%) and side-on (16%) collisions. Forty-three control subjects who
were age and gender matched with the whiplash sample participated in
the study.
At the time of their accident, 34 patients had
been employed. Of these, 25 had taken on average 12-13 days off
work, 6 had changed their occupation as a result of the accident and
8 had not returned to work. All had received ongoing medical
treatment, which consisted mainly of analgesics, non-steroidal
anti-inflammatory drugs and various modalities of physical
treatment. Twenty-eight patients were involved in ongoing
litigation, ten had settled their claims and five had never sought
compensation for personal injury.
Comparing the subjective reports, the intensity
of neck pain and the presence of concentration problems appear to
have remained constant since the accident. The incidence of headache
tended to have declined, whereas that of referred pain (into
shoulders and arms) to increase slightly with the passage of time.
Other symptoms were rated as being less frequent with the passage of
time (Table 1).
|
Table 1. –
Self-reported symptoms acute (<2 weeks) and chronic (>6
months) |
|
SYMPTOM |
ACUTE |
VAS
scores |
CHRONIC |
VAS
scores |
|
|
n |
% |
Mean |
SD |
n |
% |
Mean |
SD |
|
Neck Pain |
43 |
100% |
82 |
15 |
43 |
100% |
67 |
15 |
|
Headache |
43 |
100% |
77 |
21 |
38 |
88.4% |
74 |
19 |
|
Shoulder Pain |
38 |
88.4% |
64 |
32 |
41 |
95.3% |
61 |
18 |
|
Arm Pain |
26 |
60.5% |
39 |
37 |
25 |
58.1% |
59 |
22 |
|
Pins and Needles |
22 |
51.2% |
- |
- |
19 |
44.2% |
- |
- |
|
Numbness |
17 |
39.5% |
- |
- |
10 |
23.3% |
- |
- |
|
Dizziness |
23 |
53.5% |
- |
- |
4 |
9.5% |
- |
- |
|
Blurred vision |
15 |
34.8% |
- |
- |
6 |
14.3% |
- |
- |
|
Tinnitus |
13 |
30.9% |
- |
- |
1 |
2.4% |
- |
- |
|
Concentration |
24 |
55.8% |
- |
- |
24 |
55.8% |
- |
- |
|
|
|
|
|
|
|
|
|
|
Pain distribution
At the time of testing, patients most commonly
reported pain in the neck, shoulders, scapulae, and head. Next, in
descending order of frequency, were the dorsal upper arms, lumbar
region, interscapular region, thoraco-lumbar junction, and posterior
thigh. Leg pain only occurred in those complaining of widespread
spinal pain. Twenty-three patients reported either continuous or
intermittent paraesthesiae, described as numbness and/or ‘pins and
needles’, most frequently felt in their hands (dermatomes
C6/7/8).
Qualitative psychophysical
testing
All participants were able to perceive and
correctly identify each of the four cutaneous stimuli. One patient
reported that light touch over the pain-dominant shoulder was
painful. Four patients rated punctate pressure applied in the region
of their shoulder pain as painful. Eleven patients described a
painful response to heat and twenty-three to cold stimulation. In
the control group no participant reported pain in response to
light-touch or punctate pressure, but ten experienced cold
stimulation as painful and nine reported heat as painful. However
pain felt on thermal stimulation was self-rated on a numerical scale
as being 2-3 times higher in the whiplash patients (34/100 for heat,
29/100 for cold) than in the controls (14/100 for heat, 10/100 for
cold).
Quantitative psychophysical
testing
In all participants VPT was reported in the
first 10-15% of available frequency and in the first 9-14% of
available amplitude range. Normality testing was conducted on all
perception threshold data collected from each individual test site.
The results were positively skewed. Mann-Whitney U-tests showed no
significant difference in vibration perception threshold between
patients and control participants at the p<0.05 level. No
significant differences in VPT were found between pre-test painful
and non-painful test sites (Table 2).
|
Table 2. -
Comparisons for VPT between whiplash and
control group |
|
Groups° |
n 1
W |
n 2
C |
Test
point |
Mann-Whitney
U |
Significance
2-tailed p |
|
Frequency measurements |
|
W vs C |
43 |
43 |
Knee |
886 |
0.73 |
|
|
43 |
43 |
Trapezius |
817.5 |
0.35 |
|
|
43 |
|
Deltoid |
870 |
0.63 |
|
Amplitude
measurements |
|
W vs C |
43 |
43 |
Knee |
762.5 |
0.16 |
|
|
43 |
43 |
Trapezius |
764 |
0.16 |
|
|
43 |
43 |
Deltoid |
729.5 |
0.09 |
°Groups: W=Whiplash patients, C= Control
participants,
Twenty-eight whiplash patients (19 females and
9 males) reported VIP. In 13 patients the stimulus had to be removed
before the predetermined maximal intensity and time of application
were reached. Although the onset of both VIP and pain intolerance
was reported through a wide range, the median of responses occurred
in the last quarter of available amplitude and frequency stimulus
intensity at all three test sites (Table 3). Most patients reported
VIP with an increase in both modalities at the same test site. Two
patients reported pain only with an increase in frequency, whilst
one patient only to an increase in amplitude. No control subject
reported VIP or any discomfort due to vibration.
The majority of pain responses in the patients
occurred at the trapezius test site, when frequency (n=25) or
amplitude (n=26) was increased. Stimulation over the deltoid muscle
belly produced painful responses, both with increases in amplitude
(n=23) and in frequency (n=18). In these patients, vibration over
both regions reproduced their pre-existing pain. Fourteen patients
reported pain spreading into ‘new’ areas. Some patients reported VIP
at the knee test site (10 with increasing amplitude and 8 with
increasing frequency). In these patients, vibration evoked
pre-existing pain, presumably referred from the low back into the
lower limb. In eight patients VIP was recorded at all three test
sites. Onset of vibration induced pain at any one site was
considered a positive response.
The non-painful responses to vibration elicited
from 16 healthy controls and the VIP in 11 patients were
reproducible in a test/retest context, with at least two weeks
separating the two tests.
|
Table 3.
Vibration induced pain threshold and tolerance |
|
|
n |
Knee
median (range) |
Trapezius
median (range)
|
Deltoid
median (range) |
Amplitude |
|
|
|
|
Pain
Threshold |
28 |
|
|
|
|
Pain Tolerance |
11 |
|
|
0.91 (0.68-1.0) mm |
|
Frequency |
|
|
|
|
Pain
Threshold |
26 |
|
|
82 (28-100) Hz |
|
Pain Tolerance |
12 |
72 (42-100) Hz |
|
83 (56-100) Hz |
Scores on self-reported
questionnaires
The patients presented with high scores in all
five components of the Shortform McGill pain questionnaire.
Mann-Whitney U-test results showed that those who reported VIP
selected significantly more affective pain descriptors than those
without VIP.
As a group, the patients scored a mean of 44.8%
(SD 14.9%) of functional impairment on the NDI, which is rated as a
‘severe’ level of disability (40-60%) (Vernon 1996). Pain was the
dominant problem, but travelling, activities of social life,
personal care, sexual activity and sleep were also disrupted. No
significant difference in the NDI was found between patients who
were involved in litigation and those who had settled their claims
or had never claimed compensation for personal injury. No
significant difference in NDI was found between patients with and
without VIP.
Forty-one patients and 42 control subjects
completed the psychological questionnaire. As two of the
participants were under 14 years of age, the adult questionnaire
could not be used. One whiplash patient declined to complete the
questionnaire. The SCL-90-R results revealed an overall elevated
level of distress in the patients compared to the controls.
Significant differences between patients and controls were found in
the dimensions of somatisation, obsessive-compulsive, depression,
anxiety, hostility and the three global indexes (GSI, PSDI, PSI)
(Figure 1). The presence of VIP was not predictive of higher levels
of psychological distress.
Fig.1 –
SCL-90-R Clinical profile for study groups
SOM= somatisation, 0-C= obsessive-compulsory,
I-S= interpersonal sensitivity, DEP=
depression, ANX= anxiety,
HOS= hostility, PHO= phobic-anxiety, PAR=
paranoid ideation, PSY= psychoticism
Correlations
All nine primary symptom dimensions and three
global indexes on the SCL-90-R were analysed for correlation with
the NDI and the Shortform McGill pain questionnaire in the whiplash
group (n=41), using Pearson’s and Spearman’s Rank Order Correlation.
In the whiplash group, there was high positive correlation for the
NDI with most variables of the Shortform McGill pain questionnaire
(Table 4). There was no significant correlation between any of the
psychological dimensions of the SCL-90-R and the NDI. Spearman’s
Rank Order Correlation showed significant correlation between the
VAS of the McGill pain questionnaire with the scores in the
psychological dimension ‘somatisation’ (r=0.32, p=0.02) and the
‘PSDI-global index’ (Positive Symptom Distress Index) (r=0.35,
p=0.02) of the SCL-90-R.
Regressions
A logistic regression analysis was conducted to
identify the variables that might predict either the presence or
absence of VIP in a patient with chronic pain following a whiplash
injury. Due to the small sample size, different combinations of
variables were tested with regression models. Only the intensity of
arm pain post-injury appeared to be significant (p<0.05). Factors
which tended to correctly predict group membership were the presence
of paraesthesiae post-injury, high affective pain descriptor scores
(Shortform McGill pain questionnaire) and self-reported pain
intensity with heat stimuli (Table 5).
|
Table 4.
Nonparametric Correlations - Spearman’s rho (n=43) |
|
|
|
|
MG-S |
McG-A |
McG-T |
VAS |
|
NDI |
CC |
-- |
.27 |
0.36 b |
0.34 b |
0.61 a |
|
|
Sig. |
-- |
.08 |
0.02 |
0.03 |
0.00 |
CC= Correlation Coefficient, Sig.= Significance
(2-tailed)
McG-S = sensory dimension; McG-A = affective
dimension;
McG-T = total pain descriptors; VAS = visual
analogue scale
a significant (p<0.01)
b significant (p<0.05)
|
Table 5.
Backward Stepwise (LR) regression analysis |
Variable |
B |
SE |
Sig |
Exp (B) |
95% CI |
Predictive Power % |
|
Arm pain |
0.03 |
0.01 |
0.03* |
1.03 |
1.00-1.05 |
70.3 |
McGill
affective |
0.25 |
0.14 |
0.06 |
1.29 |
0.99-1.68 |
72.1 |
|
Heat mean |
1.51 |
0.89 |
0.09 |
4.51 |
0.78-25.96 |
72.1 |
|
Paraesthesiae |
0.96 |
0.71 |
0.18 |
2.61 |
0.65-10.56 |
70.0 |
|
Depression |
0.25 |
0.13 |
0.05 |
1.28 |
0.99 - 1.65 |
72.9 |
|
|
|
|
|
|
|
|
The principal
findings
The principal finding was that 65% of patients
in the sample reported VIP. Those with VIP were more likely to
report referred pain and paraesthesiae into the upper limb, both
soon after the MVA, as well as at time of testing. Furthermore,
stimulation with cold and heat elicited a proportionately higher
number of pain responses in these patients. Although this group used
affective pain descriptors more frequently, neither a significantly
higher NDI nor higher psychological scores were found compared to
the other patients.
DISCUSSION
Although the information collected regarding
accidents was retrospective, the demographic and clinical
characteristics of the patient sample were similar to those reported
by others (Barnsley et al., 1994; Radanov et al.,
1995; Panjabi et al., 1998). The relatively high
proportion of patients with upper limb pain (58%) and paraesthesiae
(44%) was unexpected. There is clinical evidence suggesting that
these are referred symptoms of cervical neural origin (Quintner,
1989).
Experimental findings
Cutaneous vibration sense is mediated through
specialised mechanoreceptors which respond to different frequencies
- Merkel’s discs respond to frequencies between 5-15 Hz, Meissner’s
corpuscles to frequencies between 20-50 Hz and Pacinian corpuscles
to frequencies between 60-400 Hz (Kandel et al.,
2000). The vibration parameters used in this study were sufficient
to elicit responses from each type of receptor. There were no
significant differences in VPT between the patients and the control
subjects. Furthermore, testing conducted within an area of pain did
not appear to have any significant influence on VPT. The unimpaired
VPT in the patients is indicative of normal mechanoreceptor and
large sensory fibre function. Our findings confirm that VPT tends to
occur early in the available stimulus range (first 20-25%) and that
skewed results are to be expected (Bloom et al.,
1984; Yarnitsky, 1996). The applied ‘method of limits’ for threshold
detection does show large inter-sessional bias as discussed by
Yarnitsky (1996) and may to some extent be dependent on subject’s
attentional and cognitive factors (Snodgrass et al.,
1985; Schwartz and Klima 1995).
A region
of secondary hyperalgesia is characterised by a change in the
modality of the sensation evoked by low threshold mechanoreceptors,
from touch to pain, and an increase in the magnitude of pain
sensations evoked by mechanically sensitive nociceptors (Lamotte et al.,
1991; Cervero et al., 1994). In the majority of patients,
VIP occurred in the last quarter of available stimulus range.
Increasing the amplitude of the vibration stimulus, is known to
increase the total number of active sensory neurons in a linear
fashion (Kandel et al., 2000). Presumably, the resulting
spatial summation of spike trains was sufficient to discharge
sensitized second order sensory neurones. The similar response seen
when the frequency of vibration was increased can be explained by
the phenomenon of temporal summation of afferent impulses. These
findings imply that VIP following whiplash injury is a clinical
correlate of central sensitization. Furthermore, the spread of VIP
into ‘new’ areas, as observed in 14 patients, is consistent with
such a state of heightened sensibility of the central nervous system
(Coderre et al., 1993; Woolf and Mannion,
1999).
The
distribution of chronic pain was diverse in the patient population
and does seem to have influenced the responses to vibration at the
different test sites. Increased stimulus intensity also means an
increase in the length of application time. Further research will be
necessary to determine whether the test body site, the duration of
application or its intensity that are critical factors determining
response to vibration.
Because of the proximity of the trapezius test
site to the cervical spine, cutaneous vibration over this region
might have been conducted to receptors located in putative occult
injuries of deep cervical spinal structures, one candidate being
zygapophyseal
joints (Wallis et al.,
1997). In this scenario, VIP could reflect peripheral sensitization
of nociceptors related to these joints.
VIP occurring in eight patients at all three
test sites raises the possibility of hypervigilance, manifested by a
generalised increase in sensitivity to experimentally induced
stimulation (McDermid et al., 1996). The negative cognitive and
emotional experiences of individual patients might have amplified
vibration at the supraspinal level to the extent that it became an
aversive stimulus. However, as the cognitions and beliefs of
individual patients were not explored in this study, this
possibility cannot be refuted.
The
number of patients reporting pain to mechanical cutaneous stimuli
was low and no conclusion can be drawn from it. However, it was of
interest that in the same patients, vibration was also reported as
painful. While both findings demonstrate mechanically induced pain
(allodynia or hyperalgesia), it is possible that different
underlying pain mechanisms may exist amongst the group of positive
responders to vibration. As such, four patients rated punctate
pressure exerted by the Semmes-Weinstein monofilament in the area of
their shoulder pain as painful. Three of them also reported pain in
response to heat and cold over the same site. In these patients, all
stimuli appear to have been of sufficient intensity to activate
polymodal small diameter fibres (Ochoa and Yarnitsky, 1993; Magerl
et
al., 1998, Pederson and Kehlet, 1998).
Mechanical stimulation caused by the
application pressure of the thermal probes was considered to have
been minimal. Moderate heat, expected to elicit a sensation of
‘warmth’ rather than pain, was rated as being painful by 9 of 43
control participants. Such responses were difficult to explain.
However, the evoked pain intensity ratings were significantly lower
than those of 11 patients, whose reported ratings could therefore be
classed as hyperalgesic and mediated by a small group of polymodal
high-threshold afferents (Cesare and McNaughton, 1997; Morin and
Bushnell, 1998). The blinding to the heat stimulus might have
resulted in heightened awareness in all participants???, causing
them to be unduly hypervigilant in this situation.
The short duration of application of the cold
stimulus appears to have activated both innocuous cold receptors
(Ad-fibres) and polymodal nociceptors (Davis,
1998). Ten control participants reported pain in response to cold,
implying a normal discharge response of some polymodal units (Davis,
1998). Five out of those 10 responses were recorded at the sternal
test site where lack of subcutaneous fat the site might have
contributed to the responses. The painful responses to cold in 23
patients can be attributed to responses from the same receptor
types. Cold hyperalgesia is prevalent in patients with neuropathic
pain (Ochoa, 1996; Davis, 1998). The higher proportion of painful
responses seen in the whiplash group is consistent with this
phenomenon.
The patients exhibited an enhanced level of
psychological distress across all dimensions of the SCL-90-R, when
compared to the controls. The finding of significantly elevated
scores for the dimensions of somatisation, obsessive-compulsive
behaviour, depression, anxiety and hostility is consistent with the
findings of others (Wallis et al., 1996; Wallis et al.,
1997; Wallis et al., 1998; Kessels et al.,
1998). This relatively homogeneous psychological profile is thought
to be the result of the chronic pain state and not a reflection of
primary psychopathology (Wallis et al.,
1996). The significant positive correlation found in this study
between the VAS pain intensity scale (Shortform McGill pain
questionnaire) and both the somatisation dimension and ‘positive
symptom distress index’ of the SCL-90-R, supports there being a
relationship between ongoing pain and distress arising from bodily
dysfunction.
Patients
who reported VIP had significantly higher affective but not sensory
pain descriptor scores on the Shortform McGill pain questionnaire.
Affective pain descriptor scores were also significantly correlated
with scores on the NDI. Other studies have shown that high affective
scores tend to correlate with higher ratings of distress, and that
there is a positive association between distress and self-reported
functional disability (REF!!)
It has been suggested that psychosocial factors
may be major risk factors for development of the late whiplash
syndrome (Smed, 1997). The medico-legal process has been identified
as one such factor that can reinforce and perpetuate maladaptive
pain behaviour (Shapiro and Roth, 1993; Swartzman et al.,
1996; Schmand et al., 1998; Cassidy et al.,
2000). Therefore, as mentioned above, some patients with outstanding
medico-legal claims and/or with high levels of psychological
distress may be biased in favour of reporting painful responses
during quantitative sensory testing (McDermid et al.,
1996). In this study, no significant difference was found between
patients with and without VIP for any dimension of the SCL-90-R. The
28 patients with VIP (13 being intolerant to the stimulus) did not
differ from the 15 without VIP with respect to the status of their
personal injury claims. Furthermore, patients pursuing personal
injury claims did not rate themselves as being significantly more
disabled (NDI) than those without ongoing litigation. Although the
numbers are small, these findings suggest that the reported
responses to vibratory stimuli were independent of the psychological
and litigation status of the patients.
CONCLUSIONS
Patients presenting with the late whiplash
syndrome appear to be a heterogeneous group in terms of underlying
pain mechanisms. This cross-sectional sample contained those who
processed vibratory stimuli in a manner consistent with the
phenomenon of central sensitization. Areas of widespread pain
reported by these patients are therefore likely to represent regions
of secondary hyperalgesia, raising a number of important clinical
implications.
Firstly, the clinical features can be
rationally explained in a neurobiological framework. This has not
proved possible when using the standard ‘injury’ model, nor with the
model of primary psychogenesis. Secondly, it predicts that
mechanical forms of passive therapeutic intervention will be
ineffective, and possibly harmful. Thirdly, the increased level of
psychological distress, a higher tendency to use affective pain
descriptors and a high level of perceived disability in the whiplash
group, predicates that the approach to pain management in such
chronic pain patients should be multidimensional.
Acknowledgments
The authors wish to thank Mr. P. Kolb
(Bioengineering Division, Royal Perth Hospital), who designed and
constructed the vibration device for this study, Mr. K. Sussenbach
for technical assistance, Ms L. Lester and Dr. J. Sommer for
statistical advice, Dr. P. Siddall and Prof. M. Cousins for their
helpful suggestions.
References
Asbury A. Numbness, tingling, and sensory loss.
In: Fauci AS, Braunwald E, Isselbacher KJ, Wilson JD, Martin JB,
Kasper DL, Hauser SL, Longo DL, editors. Harrison’s
Principles and Practice of Medicine. 14th ed. New York: McGraw Hill, 1998:
122-125.
Barnsley L, Lord SM, Bogduk N. Whiplash injury.
Pain
1994;58:283-307.
Bloom S, Till S, Soenksen P, Smith S. Use of
biothesiometer to measure individual vibration thresholds and their
variation in 519 non-diabetic subjects. Brit Med
J 1984; 288:1793-1795.
Cassidy JD, Carroll LJ, Cote P, Lemstra M,
Berglund A, Nygren A. Effect of eliminating compensation for pain
and suffering on the outcome of insurance claims for whiplash
injury. NEJM 2000; 342:1179-1186.
Cervero F, Meyer RA, Campbell JN. A
psychophysical study of secondary hyperalgesia: evidence for
increased pain to input from nociceptors. Pain
1994;58:21-28.
Cesare P, McNaughton P. Peripheral pain
mechanisms. Curr Opin Neurobiol 1997;7:493-499.
Coderre TJ, Katz J, Vaccarino AL, Melzack R.
Contribution of central neuroplasticity to pathological pain. Pain
1993;52:259-285.
Davis KD. Cold-induced pain and prickle in the
glabrous and hairy skin. Pain 1998;75:47-57.
Derogatis LR. Symptom Checklist-90-R.
Administration, scoring and procedures manual. Minneapolis, National
Computer Systems Inc,1994.
Devor M. The pathophysiology of damaged
peripheral nerves. In: Wall PD, Melzack R, editors. Textbook of
Pain. Edinburgh: Churchill Livingstone, 1994. pp.
79-100.
Ferrari R, Russell AS. Epidemiology of whiplash: an international
dilemma.
Ann Rheum Dis 1999a;58:1-5.
Ferrari R, Russell AS. Development of persistent neurologic symptoms
in patients with simple neck sprain. Arthritis
Care Res 1999b;12:70-76.
Gargan M, Bannister G, Main C, Hollis S. The
behavioural response to whiplash injuries. J Bone
Joint Surg 1997;79B:523-526.
Hagström Y, Carlsson J. Prolonged functional
impairments after whiplash injury. Scand J
Rehab Med 1996;28:139-146.
Kandel ER, Schwartz JH, Jessell TM, editors. Principles
of Neural Science. 4th ed. New
York: McGraw Hill, 2000: 430-450.
Kessels RP, Keyser A, Verhagen WI and van
Luijtelaar EL. The whiplash syndrome: a psychophysical and
neuropsychological study towards attention. Acta Neurol
Scand 1998;97:188-193.
Koelbaek Johansen M, Graven-Nielsen T, Schou
Olesen A, Arendt-Nielsen L. Generalised muscular hyperalgesia in
chronic whiplash syndrome. Pain 1999;83: 229-234.
Koltzenburg M, Lundberg LE, Torebjoerk HE.
Dynamic and static components of mechanical hyperalgesia in human
hairy skin. Pain 1992;51:207-219.
Koltzenburg M, Torebjoerk HE, Wahren LK.
Nociceptor modulated central sensitization causes mechanical
hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain
1994;117:579-591.
Lamotte RH, Shain CN, Simone DA, Tsai E-FP.
Neurogenic hyperalgesia: psychophysical studies of underlying
mechanisms. J Neurophysiol 1991; 66: 190-211.
Magerl W, Wilk SH, Treede RD. Secondary
hyperalgesia and perceptual wind-up following intradermal injection
of capsaicin in humans. Pain 1998;74:257-268.
McDermid AJ, Rollman GB, McCain GA. Generalized
hypervigilance in fibromyalgia: evidence of perceptual
amplification. Pain 1996;66:133-144.
Melzack R. Neurophysiological foundations of
pain. In: Sternbach RA, editor. The psychology of pain. 2nd ed. New York: Raven Press, 1986:
1-23.
Melzack R. The short-form McGill pain
questionnaire. Pain 1987;30:191-197.
Merskey H, Bogduk N, editors. Classification of
chronic pain. Description of chronic pain syndromes and
definitions of pain terms. 2nd
ed. Seattle: IASP Press, 1994: 209-213.
Morin C, Bushnell MC. Temporal and qualitative
properties of cold pain and heat pain: a psychophysical study. Pain
1998;74:67-73.
Obelieniene D, Schrader H, Bovim G, Miseviciene
I, Sand T. Pain after whiplash: a prospective controlled inception
cohort study. J Neurol Neurosurg Psychiatry
1999;66:279-283.
Ochoa JL, Yarnitsky D. Mechanical hyperalgesia
in neuropathic pain patients: dynamic and static subtypes. Ann
Neurol 1993;33:465-472.
Ochoa JL. Human polymodal receptors in
pathological conditions. In: Kumazawa T, Krueger L, Mizumura K,
editors. Progress in Brain Research. Amsterdam:
Elsevier Science BV, 1996.113:185-197.
Panjabi MM, Cholewicki J, Nibu K, Babat LB,
Dvorak J. Simulation of whiplash trauma using whole cervical spine
specimens. Spine 1998;23:17-24.
Pearce JM. Whiplash injury: a reappraisal. J Neurol
Neurosurg Psychiatry 1989;52:1229-1231.
Pearce JM. A critical appraisal of the chronic
whiplash syndrome. J Neurol Neurosurg Psychiatry
1999;66:273-276.
Pederson JL, Kehlet H. Secondary hyperalgesia
to heat stimuli after burn injury in man. Pain
1998;76:377-84.
Quintner JL. A study of upper limb pain and
paraesthesiae following neck injury in motor vehicle accidents: an
evaluation of the brachial plexus tension test of Elvey. Brit J
Rheumatol 1989;28:528-533.
Radanov BP, Sturzenegger M, Di Stefano G.
Long-Term outcome after whiplash injury. A 2-year follow-up
considering features of injury mechanism and somatic, radiologic,
and psychological findings. Medicine (Baltimore) 1995;74:281-297.
Radanov BP, Bicik I, Dvorak J, Antinnes J, von
Schulthess GK, Buck A. Relationship between neuropsychological and
neuroimaging findings in patients with late whiplash syndrome. J Neurol
Neurosurg Psychiatry
1999;66:485-89.
Ratcliff AH. Whiplash injuries. J Bone
Joint Surg 1997;79:517-519.
Schmand B, Lindebloom J, Schagen S, Heijt R.,
Koene T, Hamburger HL. Cognitive complaints in patients after
whiplash injury: the impact of malingering. J Neurol
Neurosurg Psychiatry 1998;64:339-343.
Schwartz B, Klima RR. Vibration sensation:
measurement techniques and applications. Critical
Reviews in Physical and Rehabilitation Medicine 1995;7:113-130.
Shapiro AP, Roth R. The effect of litigation on
recovery from whiplash injury. Spine:
State of the Art Reviews. Philadelphia: Hanley & Belfus,
Inc. 1993;7:531-556.
Sheather-Reid RB, Cohen ML. Psychophysical
evidence for neuropathic components of chronic neck pain. Pain
1998;75:341-347.
Smed A. Cognitive function and distress after
common whiplash injury. Acta Neurol Scand 1997; 95:73-80.
Snodgrass JG, Levy-Berger G, Haydon M. Human
Experimental Psychology. New York: Oxford University Press,
1985. pp: 56-87.
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;20:8S:10S-20S.
Swartzman LC, Teasell RW, Shapiro AP, McDermid
AJ. The effect of litigation status on adjustment to whiplash
injury. Spine 1996;21:53-58.
Vernon H. The neck disability index: patient
assessment and outcome monitoring in whiplash. J
Musculoskel Pain 1996;4:95-104.
Wallis BJ, Lord SM, Barnsley L, Bogduk N. Pain
and psychologic symptoms of Australian patients with whiplash. Spine
1996;21:804-810.
Wallis BJ, Lord SM, Bogduk N. Resolution of
psychological distress of whiplash patients following treatment by
radiofrequency neurotomy: a randomised, double-blind,
placebo-controlled trial. Pain 1997;73:15-22.
Wallis BJ, Lord SM, Barnsley L, Bogduk
N. The psychological profiles of patients with
whiplash-associated headache. Cephalalgia 1998;18:101-105.
Woolf CJ, Doubell TP. The patho-physiology of
chronic pain - increased sensitivity to low threshold Aß-fibre
input. Curr Opin Neurobiol 1994;4:525-534.
Woolf CJ, Mannion RJ. Neuropathic pain:
aetiology, symptoms, mechanisms, and management. Lancet
1999;353:1959-1964.
Yarnitsky D. Quantitative sensory testing. Muscle
Nerve 1996;20:198-204. |