original article
Wien Klin Wochenschr
https://doi.org/10.1007/s00508-020-01631-y
Can measuring passive neck muscle stiffness in whiplash
injury patients help detect false whiplash claims?
Jure Aljinović · Igor Barišić · Ana Poljičanin · Sandra Kuzmičić · Katarina Vukojević · Dijana Gugić Bokun ·
Tonko Vlak
Received: 4 July 2019 / Accepted: 3 March 2020
© Springer-Verlag GmbH Austria, part of Springer Nature 2020
Summary
Background Whiplash injury of the cervical spine is
the most common injury after a car accident and in
25% of patients it progresses into chronic neck pain.
Aim of the study To investigate the difference in neck
muscle stiffness using shear wave ultrasound elastography between subjects who suffered an uncomplicated whiplash injury and a control group. Possible
recognition of patients who insist on physical therapy
in order to support their false whiplash injury claims.
Methods This study included 75 whiplash injury patients and 75 control subjects. Trapezius, splenius
capitis and sternocleidomastoid muscles were examined by ultrasound shear wave elastography.
Results Increased muscle stiffness was noticed in
trapezius muscle bilaterally in the whiplash group
when compared to the control group (p < 0.001;
J. Aljinović and I. Barišić equally contributed to this paper as
first authors.
J. Aljinović () · A. Poljičanin · S. Kuzmičić · T. Vlak
Institute of Physical and Rehabilitation Medicine
with Rheumatology, University Hospital of Split,
Šoltanska 1, 21000 Split, Croatia
[email protected]
I. Barišić
Clinical Department of Diagnostic and Interventional
Radiology, University Hospital of Split, Split, Croatia
K. Vukojević
Department of Anatomy, Histology and Embryology,
University of Split School of Medicine, Split, Croatia
D. Gugić Bokun
Clinical Department of Pathology, Forensic Medicine and
Cytology, University Hospital of Split, Split, Croatia
J. Aljinović · A. Poljičanin
Department of Health Studies, University of Split, Split,
Croatia
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right 57.47 ± 13.82 kPa vs. 87.84 ± 23.23 kPa; left 54.4 ±
12.68 kPa vs. 87.21 ± 26.47 kPa). Muscle stiffness in
splenius capitis and sternocleidomastoid muscles
was not suitable for analysis because of asymmetrical
data distribution. Patients with less than 76 kPa of
muscle stiffness in trapezius muscle are unlikely to
belong in whiplash injury group (sensitivity 90% for
right and 97% for left trapezius muscle, specificity
72% and 73%, respectively).
Conclusion Patients measuring below 76 kPa of muscle stiffness in the trapezius muscle might have no
whiplash injury. Further follow-up of the patients
measuring higher than cut-off value might be beneficial for detecting patients with prolonged neck muscle spasm that can lead to chronic cervical pain syndrome.
Keywords Elastography · Ultrasound · Trapezius ·
Shear wave · Neck pain
Introduction
Whiplash injury and whiplash-associated disorder are
the most common injuries resulting from a car accident [1]. Recovery usually occurs within 3 months of
the accident [2, 3]. Although most of the people recover completely, in about 25% of the cases medium
to severe chronic neck pain develops [3]. Negative
predictive factors for complete recovery reported in
the literature are high initial neck pain intensity [4],
high neck disability index score, development of posttraumatic stress syndrome and pain catastrophizing
[5]. Some preaccident factors, such as high psychological distress, female gender, low educational level, and
being unemployed, sick-listed or receiving social assistance were also reported as possible predictive factors for developing chronic neck pain after whiplash
Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?
original article
injury [6]. Poor coping strategies were one of the proposed mechanisms in those patients.
In the study by Ritchie et al. regarding whiplash injury it was proposed that a tool named clinical prediction rule (CPR) could be used in predicting outcomes,
such as developing either disability after whiplash injury or full recovery [2]. It consists of eight domains:
initial neck disability index (NDI), initial neck pain on
visual analogue scale (VAS), cold pain threshold, range
of neck movement, age, gender, presence of headache
and posttraumatic stress disorder (PTSD). This tool is
still not in use in clinical practice and all of the eight
domains are undergoing a validation procedure.
The mechanism of pain after whiplash injury is still
unexplained, but the strain of muscles and ligaments
followed by reactive spasm is believed to be the main
cause. Usually only plain radiographs of the cervical
spine are performed in patients involved in car accidents. A radiograph can detect cervical spine straightening and prior intervertebral osteochondrosis and
radiograph can exclude fractures of the cervical vertebra. So far little is known about the status of muscle
injury or reactive spasm, both of which are not detectable on plain radiographs and their involvement
in the chronic pain development is not defined.
Ultrasound examination with shear wave elastography (SWE) is a relatively new radiological method
that can access structural changes in different tissues
including muscles [7]. This method can measure the
level of muscle stiffness (elasticity) and permits both
qualitative and quantitative evaluation of the elasticity
properties of soft tissues and their alteration in traumatic lesions and degenerative pathology. The SWE
method uses a combination of the radiation force induced in a tissue by an ultrasonic beam and the ultrafast imaging sequence capable of catching the propagation of the resulting shear waves in real time. It is
worth mentioning that the ultrasound SWE is harmless for both the patient and the medical practitioner.
Within a given region of interest (ROI), defined by an
electronic cursor positioned by the radiologist, values
for the maximum tissue stiffness, mean stiffness and
standard deviation (SD) are produced. Areas of stiffness within a muscle can thus be clearly mapped. This
reproducible, quantitative information is not available
with standard elastography and yet it can aid both the
diagnosis and rehabilitation evaluation of acute musculoskeletal injuries or chronic myofascial pain [8].
The problem of this radiological method is the lack
of standardization of applied pressure onto the tissue
during the examination. Also, there are no standardized values available in the literature for normal stiffness of the examined muscles with only one paper has
been published, which addressed passive muscle stiffness in young children [9]. Two papers were published
in adults: one addressing quantitative estimation of
muscle shear elastic modulus of the upper trapezius
muscle with supersonic shear imaging during arm po-
sitioning [10] and the other quantifying cervical and
axioscapular muscle stiffness using SWE [11].
In the CPR tool, the level of muscle stiffness is not
included as one of the domains for outcome prediction. The literature research produced no papers that
would refer on muscle stiffness as a possible predictive factor for prolonged pain. The circulus vitiosus
that bonds muscle stiffness and pain appears to be
an important factor for development of chronic pain
sensation.
It was hypothesized that some people who did not
sustain a true whiplash injury after a car accident are
going to physical therapy in order to attempt false
insurance claims. We believe those patients would
have normal muscle stiffness measurements and no
clinical signs, such as radiculopathy or limitation of
neck movement. In order to test this presumption,
we needed to obtain basic data of muscle stiffness in
healthy people and whiplash injury patients.
Until now the only verification of injury status was
the patient’s own pain perception measured by VAS.
That measure is highly subjective and sometimes exaggerated. By measurement of passive neck muscle
stiffness in a whiplash injury using SWE we would
have a quantifiable measure that can objectively inform us of the true postinjury muscle tone.
This study aimed to investigate the difference in
muscle stiffness between two groups: subjects who
suffered whiplash injury examined by a specialist of
physical medicine and rehabilitation (PMR) and a
control group of healthy people. We also sought to
compare the possible differences in pain perception
as reported by the patients themselves versus pain estimation by an experienced physician during clinical
examination. Additionally, we compared muscle stiffness values in subjects who took analgesics or/and
myorelaxant drugs after the whiplash injury with the
muscle stiffness values measured in subjects who
did not take the aforementioned drugs. Ultimately,
we aimed to establish which muscles were most affected by prolonged spasm in the first 3 months after
whiplash injury. The three biggest muscles of the
neck region that usually suffer strains and sprains
after uncontrolled movement of the neck were analyzed: posteriorly located trapezius muscle, anteriorly
located sternocleidomastoid muscle and laterally located splenius capitis muscle.
Materials and methods
This prospective study was conducted at the Institute
of Physical and Rehabilitation Medicine and Clinical
Department of Diagnostic and Interventional Radiology in University Hospital Split, Croatia. It was approved by the Ethical Committee of the University
Hospital Split. Patients and healthy control subjects
were informed about the study design and goals and
informed consent was obtained in written form.
Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?
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original article
Fig. 1
Position of ultrasound probe for analyzing
neck muscles. a Trapezius
muscle; b Splenius capitis muscle; c Sternocleidomastoid muscle
The study was designed to evaluate ultrasound SWE
as a diagnostic method in the quantification of the
neck muscle stiffness in patients who were involved
in a car accident and suffered a whiplash injury. Only
patients that were examined by PMR specialist within
90 days from the car accident and diagnosed as having a whiplash injury were included in the study (Quebec Task Force classification grade 1: pain in the neck
alone, grade 2: pain and decrease of movement in the
neck or point tenderness, grade 3: additional neurological signs such as decreased or absent deep tendon
reflex and/or muscle weakness and/or sensory defect)
[12]. Exclusion criteria for this study were: Quebec
Task Force classification grade 4 with sustained fracture of cervical vertebrae [12], bone fractures of any
other location sustained in accident and whiplash injury in any other type of vehicle other than the automobile.
This study was conducted during 8 months from
August 2017 through April 2018, and 93 patients were
examined with the diagnosis of whiplash injury. From
this number only 75 patients were included in the
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study as 8 patients had exclusion criteria while 10 patients refused to participate. The control group was
formed from 75 randomly selected healthy volunteers,
with no prior muscular injuries reported. Participants
were age and gender matched between control and
whiplash groups. Whiplash injury group had 75 patients of which 32 were men and 43 women (43% vs.
57%). Mean age of the patients was 43.1 ± 13.5 years
(mean ± SD). There were 75 people in the control
group, 34 men and 41 women (45% vs. 55%), with the
mean age of 46.5 ± 16.3 years.
Data collected from the medical documentation
and from the interviews with patients included age
and sex, date of the car accident, driver or passenger status, seat belt usage, concomitant analgesics
and myorelaxant usage, and evaluation of the cervical spine radiographs. For the use of analgesics the
answers available to the patients were: yes, no and
sometimes, while for the myorelaxant use at any time
from the accident, they had only yes or no choices.
Radiographs of the cervical spine were analyzed and
either a normal X-ray, a straightening of the cervical
Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?
original article
lordosis or a prior intervertebral osteochondrosis were
noted. This was followed by a clinical examination
and evaluation of the level of pain in the neck region
by VAS (values from 0–10) completed by the physician
and the patient.
Before any physical therapy procedures all of the
patients and control subjects were examined by the
same experienced musculoskeletal radiologist on
the same ultrasound machine. The radiologist involved in this study subspecializes in ultrasound and
has 20 years of experience in musculoskeletal radiology. In his everyday practice he uses SWE for
breast tissue and for supraspinatus and Achilles tendon examinations. The radiologist was blinded to
whether the analyzed individual was in the whiplash
or the control group. A multi-frequency linear probe
(2–10 MHz; Aixplorer Supersonic Ultrasound system,
Aix en Provence, France) was used for the ultrasound examination with SWE and measurement of
difference in muscle stiffness. This machine was previously validated for SWE ultrasound in liver fibrosis
staging [13]. Tissue stiffness was measured by a physical quantity called Young’s modulus and expressed
in pressure units (kilopascals [kPa]). We have used
absolute elasticity values ranging from 0–300 kPa.
Examination was done on the preselected muscles:
trapezius, splenius capitis and sternocleidomastoid
muscles, on both sides of the neck. Two ROI were
picked in each muscle at the thickest part of the
muscle (without the fascia) and three measurements
were made in each muscle for every ROI. The mean
value from those six values was used for statistical
analysis. Furthermore, these measurements where
used to calculate intrarater reliability. Standardization
of the SWE examination was done by using minimal
pressure of the ultrasound probe against the skin to
prevent tissue from deforming and thus inadvertently
increasing the stiffness. All patient body postures for
different muscles were also standardized as follows:
trapezius muscle was examined in the seated position with the relaxed shoulder girdle and the arms
in supination resting on the thighs. The head was
slightly flexed forward. The ultrasound probe was
positioned in the upper part of trapezius muscle at
the thickest part of the muscle in midpoint from the
shoulder and head (Figs. 1a and 2). The splenius capitis muscle was examined in the same seated position
with the probe located in the upper lateral part of the
neck with 45° inclination (Fig. 1b). In this position the
splenius capitis muscle is located nearest to the skin
with the trapezius muscle below and sternocleidomastoid muscle above. Only the sternocleidomastoid
muscle was examined with the subject lying in the
supine position with the chin-up and the probe located in the middle of lateral side of the neck on the
thickest portion of the muscle (Fig. 1c).
Data distribution of elastography measures in each
of the muscles analyzed was tested by Shapiro–Wilk
test. The difference between VAS pain scale reported
Fig. 2 Optimal positioning of the ultrasound probe over
trapezius muscle during SWE. (drawing)
by the patient and by the physician was tested with
t-test for independent samples. The difference of
elastography values of the left and right trapezius
muscle in the same person and between control and
whiplash group was tested with 2-way ANOVA test.
Results of the 2-way ANOVA test were later analyzed
by post hoc Tuckey HSD test. Correlation between
X-ray, VAS reported by patient and physician, use of
analgesics or myorelaxant drugs and muscle tension
was tested with Spearman’s r test. For sensitivity
and specificity of SWE the receiver operating characteristic curve (ROC) analysis was performed. All
statistical analyses except correlation were done in
GraphPad Prism 8.0 software (GraphPad Software, La
Jolla, CA, USA). Correlation analysis was done in Past3
Software (Øyvind Hammer, Natural History Museum,
University of Oslo, Norway).
Results
In the control group the values for stiffness of analyzed muscles obtained by elastography were for
the trapezius muscles 57.5 ± 13.8 kPa for the right and
54.4 ± 12.7 kPa for the left one; the splenius muscles
26.7 ± 8.7 kPa for the right and 25.9 ± 7.4 kPa for the
left one and for the sternocleidomastoid muscles
Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?
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original article
Fig. 3
Elastography values of trapezius muscles in healthy people
and whiplash injury patients. Ctr control group,
Whp whiplash group, r right,
l left, ****p < 0.0001
21.4 ± 4.9 kPa for the right and 21.2 ± 4.1 kPa for the left
one.
In whiplash injury group elastography values for
trapezius muscles were 87.8 ± 23.3 kPa for the right
and 87.2 ± 26.7 kPa for the left one. Splenius muscles
showed mean values of 39.6 ± 23.5 kPa for the right
and 43.9 ± 22.3 kPa for the left one; sternocleidomastoid muscles had mean values of 34.7 ± 21.8 kPa for the
right muscle and 31.2 ± 15.9 kPa for the left muscle.
On further statistical analysis only trapezius muscles had normal distribution of data both in whiplash
and control group. Splenius capitis muscles and sternocleidomastoid muscles had asymmetrical data distribution and therefore were not included in further
statistical analysis.
We have found that both trapezius muscles had
more stiffness in the whiplash group when compared with control group and the difference was
significant (2-way ANOVA, f = 185.82, p < 0.001; right
57.47 ± 13.82 kPa vs. 87.84 ± 23.23 kPa, p < 0.001; left
54.4 ± 12.68 kPa vs. 87.21 ± 26.47 kPa, p < 0.001, Fig. 3).
The results show that there is no difference in the
level of tension between trapezius muscles of left and
right side within the whiplash injury group and within
the control group (f = 0.64, p = 0.425, left vs. right
whiplash group 87.21 ± 26.47 vs. 87.84 ± 23.23 kPa;
control group 54.4 ± 12.68 vs. 57.47 ± 13.82 kPa).
Mean time elapsed from the car accident was
36.4 ± 17.9 days with the minimum of 10 days and the
maximum of 85 days.
Patients reported higher intensity of pain in the cervical region on VAS then estimated by the experienced
physician after clinical examination and palpation of
tested muscles (doctor vs. patient 5.7 ± 1.5 vs. 4.3 ± 1.7,
t = –5.4, p < 0.001).
Radiographs of the cervical spine were normal in
28 patients, 29 had straightening of the cervical spine,
while 14 had previous intervertebral osteochondrosis
together with straightening of the spine. Four patients
were not X-rayed. There was no difference in muscle tension in patients with normal X-rays (group 1),
cervical spine lordosis straightening (group 2) or intervertebral osteochondrosis (group 3) both between
left and right side and within the group or between
groups (right side: group 1: 91.1 ± 26.3 kPa; group 2:
83.13 ± 21.6 kPa; group 3: 87.6 ± 21.5 kPa; left side:
group 1: 87.91 ± 25.1 kPa; group 2: 80.54 ± 25.5 kPa;
group 3: 91.35 ± 27.8 kPa).
Of the patients 57 (76%) were driving at the time of
the accident while 18 (24%) were passengers in the car.
Fig. 4
Elastography values of trapezius muscles 1,
2 and 3 months after the
whiplash injury. R right,
L left. Horizontal bar time
from injury in days, vertical bar trapezius stiffness in
kPa. * p < 0.05
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Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?
original article
Table 1
Specificity and sensitivity of shear wave elastography in whiplash injury of the neck vs. control healthy population
Test
Cut-off (kPa)
AUC (fraction)
(95% CI)
Sensitivity (%), (95%CI)
Specificity (%) (95%CI)
LR+, (95%CI)
LR–
(95%CI)
Tension in right trapezius
76
0.8745
(0.82–0.93)
90.67
(81.97–95.41)
73.33
(62.37–82.02)
3.39
(2.17–5.3)
0.12
(0.05–0.28)
Tension in left trapezius
75.6
0.8589
(0.79–0.92)
97.33
(90.73–99.53)
72
(60.96–80.90)
3.47
(2.32–5.21)
0.03
(0.005–0.15)
AUC area under ROC curve, LR+ positive likelihood ratio, LR– negative likelihood ratio, kPa kilopascal, CI Confidence interval
Table 2 Intrarater variability of elastography measurements in analyzed muscles
Elastography of muscle
ICC coefficient
95% CI
Trapezius R
0.975
[0.9291, 0.9932]
Trapezius L
0.9337
[0.8211, 0.9815]
Splenius capitis R
0.9759
[0.9315, 0.9934]
Splenius capitis L
0.9331
[0.8195, 0.9813]
Sternocleidomastoid R
0.8685
[0.6706, 0.9621]
Sternocleidomastoid L
0.886
[0.7089, 0.9674]
R right, L left, ICC inter-class correlation, CI Confidence interval
Only three patients stated they had not fastened the
seat belt (4% of whiplash injury group), while others
stated they had fastened it.
Most of the patients took analgesics on demand
(48 patients, 64%), 17 patients took analgesics regularly (23%) and 10 patients did not take any analgesics at all (13%). There was no statistically significant difference in trapezius muscle stiffness between
patients who took analgesics and the ones who did
not (right side: no analgesics vs. analgesics group,
96.2 ± 26.46 kPa vs. 86.56 ± 22.8 kPa, t = 1.1, p = 0.295;
left side 85.36 ± 26.7 kPa vs. 87.5 ± 26.66 kPa, t = –0.22,
p = 0.828).
Although almost always prescribed by the physicians at emergency departments, less than half of
the patients took a myorelaxant agent like diazepam
(33 patients, 44%). There was no significant difference in muscle stiffness between patients who
took a myorelaxant agent and the ones that did not
(right side: no myorelaxant vs. myorelaxant group
88.92 ± 22.4 kPa vs. 86.46 ± 24.57 kPa, t = 0.45, p = 0.654;
left side 82.62 ± 28.19 kPa vs. 93.06 ± 23.93 kPa, t = –1.73,
p = 0.087).
The correlation between level of muscle tension
and VAS reported by patients was tested and no
statistical significance was noted. Patient’s age and
trapezius tension did not show any correlation (right
r = –0.01, p = 0.91, left r = 0.02, p = 0.06).
Upon dividing whiplash injury patients into three
groups regarding time elapsed from the accident
(group 1: <30 days, group 2: 30–60 days and group 3:
60–90 days) we have found statistically significant increase of right trapezius stiffness in group 3 vs. both
groups 1 and 2 (Fig. 3; group 1 vs. group 3: MD;
–24.14, CI –46.6 to –1.7, p = 0.02, group 2 vs. group 3:
MD; –23.66, CI –47.8 to 0.46, p = 0.03). Left trapezius
tension showed no significant differences between
groups (Fig. 4).
We calculated the sensitivity and specificity of
SWE measurements of trapezius muscle stiffness in
determining into which group the analyzed person
belongs to. Our data showed that people who had
less than 76 kPa of muscle stiffness in the trapezius
muscle were unlikely to belong to the whiplash injury
group with calculated sensitivity of 90.6% (95% CI;
81.97–95.41) for right and 97.3% (95% CI; 90.73–99.53)
for left trapezius muscle (Table 1). The specificity
of SWE in detecting if the analyzed person in fact
belongs to the whiplash injury group is lower: 73.3%
for right trapezius (95% CI; 62.37–82.02) and 72%
for left trapezius muscle (95% CI; 60.96–80.90) (Table 1). Intrarater variability was assessed by interclass
correlation coefficient (ICC) using the model 3.1 of
Shrout and Fleiss [14]. For all muscles ICC was above
0.85 which indicates good and excellent reliability
(Table 2).
Discussion
The current presumption is that sudden and extreme acceleration-deceleration movement of the
neck causes a painful response of the neck muscles
through nociceptors which subsides within 3 weeks
following the injury by neck rest and medication [15].
In some patients who present with no new injuries
(either of bones, facet joints, spinal cord, intervertebral discs, or nerve roots) functional disorders like
spasms and cramps can persist longer than 3 weeks.
These patients were our targeted population. In this
study patients with whiplash injury had more stiffness
in all of the analyzed muscles than control group as
detected by SWE. Trapezius muscle proved to be the
ideal muscle for detection of muscle stiffness because
it displayed normal data distribution and statistically significant difference in whiplash versus control
group. Splenius and sternocleidomastoid muscles dis-
Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?
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original article
played highly asymmetric data distribution and thus
were neither suitable for relevant statistical analyses
nor referencing in the routine clinical practice.
There was no significant difference in the level
of muscle stiffness between right and left trapezius
muscle in whiplash group, therefore we conclude that
the force suffered in a car accident symmetrically
affects both sides of the neck. All but three patients
in whiplash group fastened the seat belt so the group
was homogeneous. For this study the ethics committee of the local institution allowed only inquiries
about the driver vs. passenger status, usage of the
seat belt and type of vehicle involved in the accident.
Additional questions, such as the responsibility of the
patient for the car crash, or the mechanics of it (i.e.
velocity, site of impact) were not allowed due to legislative issues and open court cases. This fact limited
our ability to explain extremely high values of trapezius muscle stiffness in few patients who presumably
suffered a high velocity or side impact.
After analyzing the data, we determined that most
of the patients were referred to physical therapy because of the pain and stiffness in cervical muscles.
Mean stiffness of trapezius muscles in whiplash injury patients was more than 30 kPa higher than in
control group. Some patients with lesser pain levels might not have been referred to a PMR specialist
and have self-treated their pain at home which we
perceive as a study flaw. We presume that the difference between stiffness in trapezius muscle between
whiplash and control group would be smaller if these
milder cases were included. On the other hand, some
patients might have aggravated their symptoms because of possible insurance issues in the aftermath
of the car accident. Whilst gathering patients who
were referred to a PMR specialist with the diagnosis
of neck whiplash injury ten people refused to participate in this study. We hypothesize that if there indeed were some simulants they would have been in
this excluded set therefore we can presume that the
studied whiplash injury group consisted of correctly
diagnosed patients with an objectively and clinically
relevant condition.
Whiplash injury patients reported stronger pain on
VAS scale then was estimated by experienced PMR
specialist after an examination. In both groups mean
VAS of pain was above 4 which suggests a need for
pain treatment either with analgesics or physical
therapy or both (VAS patient vs. VAS medical doctor
5.7 ± 1.5 vs. 4.3 ± 1.7). A meta-analysis in 2013 showed
that initial pain reporting by patients of more than
5.5 on VAS scale is a risk factor for poor recovery [16],
therefore most of our patients can be regarded as
high-risk patients for chronic pain development.
The shortcoming of this study is that there exists no
validated questionnaire with which a physician would
estimate and grade the pain of the patient. We have
therefore used an experienced PMR specialist’s estimation of pain severity elicited during an examina-
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tion of the patient through indirect signs such as facial
grinning, occurrence of palpable myogelosis, tenderness during palpation, and painful limitation of movement. All PMR specialists who were involved in this
estimation had examined and diagnosed more than
100 whiplash patients prior to this study.
Patients with whiplash injury usually wear soft neck
collars and use medicament treatment (analgesics or
myorelaxant agents). We did not find any significant
difference in trapezius muscle stiffness in subjects
who took analgesics or myorelaxant agent and the
ones who did not. Also, the level of muscle stiffness
did not differ between patients who took analgesics
regularly compared to patients who took analgesics
on an as-needed basis. The same result was obtained
for myorelaxant drugs. These results suggest that
effects of drugs are temporary and that the dosage
of these medications should be on an as-needed
scheme. This is in agreement with Curatolo’s findings from 2016, who concluded, upon searching the
available literature that there was a lack of evidence
for long-term benefits of nonsteroidal anti-inflammatory drugs (NSAID) in chronic whiplash injury [17].
Curatolo also stressed possible gastrointestinal and
renal side effects and advised their use in the acute
posttraumatic phase. As for diazepam, which was
used both as myorelaxant and antidepressive in half
of the patients in this study, we have found no longterm effect on level of stiffness. The literature shows
that diazepam may be helpful in conditions such as
hyperalgesia, sleep disorder associated with pain, or
depression connected to whiplash injury [17]. A paper
from Australia showed that 1 out of 10 people with
whiplash injury have had opioids in the treatment of
whiplash-associated pain [18]. Recently opioid use
became controversial in many conditions due to lack
of evidence of long-term benefits and possible development of drug dependence. Since the aspect of
different drugs and their separate influence on muscle stiffness was not of special interest in this study,
NSAIDs, paracetamol and/or opioid drugs were jointly
taken into account, that is as one group of analgesics.
As for radiological procedures and their role in
quantifying muscle spasm, radiographs were first to
be analyzed since all but 4 patients had them. It is
a common belief in the wider medical community
that cervical lordosis straightening as portrayed on
radiographs is connected to prolonged muscle spasm
of the cervical region; however, this hypothesis was
disproved in studies by Helliwell et al. and Beltsios
et al. where the authors concluded that the alterations
in normal cervical lordosis in patients with neck injury must be considered coincidental since cervical
lordosis straightening appears in healthy individuals
likewise [19, 20]. This is in agreement with our results
since we have found no difference in the trapezius
muscle stiffness between groups with normal X-ray
findings, cervical lordosis straightening and previous
intervertebral osteochondrosis. This suggests that
Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?
original article
radiographs of the cervical spine alone are not an adequate tool to either hypothesize or objectify which
patients have more tension in their cervical region
post-injury. In 2007 Grob et al. measured global curvature of the spine from C2 to C7 and each segmental
angle in more than 50 patients with degenerative neck
pain and healthy individuals and concluded that no
significant difference between the two groups could
be found in relation to the global curvature, the segmental angles, or the incidence of straight spine or
kyphotic deformity [21]. Incidence of cervical kyphosis in neck whiplash injury in comparison to normal
population is not known and neither did we examine
the segmental cervical kyphosis in our study, which
leaves an interesting niche of questions and opportunities that should encourage future investigations.
No correlation was found between age and level of
muscle stiffness in a patient. In the group of patients
for whom the time elapsed from the accident was between 60 and 90 days only the right trapezius showed
increased tension compared to other groups with less
time elapsed from the accident. We can only hypothesize about the possible reason(s). Maybe those
patients suffered a more complex mechanics and
stronger forces during the accident or they might be
the group from which individuals developing chronicity of the cervical neck pain will be derived. Another
question arises: why only the right trapezius muscle
had increased tension within the 60–90 days group?
Could it be because of the seat belt design which
restraints movements of left shoulder more efficiently
during an accident therefore acceleration-deceleration forces are lesser on the left side in car drivers?
Could it be that the left hand is usually holding on
to the steering wheel therefore having a protective
role during impact while the right one is more mobile
due to the manual gearbox? We must also take into
account that sometimes position of radiologist during
assessment of muscle stiffness could differ from side
to side but we tried to minimize this by using revolving chairs and by positioning patients as described in
the “Material and methods section”.
Further research in patients with uncomplicated
whiplash injury is required to standardize muscle stiffness values in different age and population groups;
however, it is clear that patients with whiplash injury have higher values of muscle stiffness in trapezius
muscle and some of them could probably be in need
of PMR specialist for treatment of prolonged muscle
stiffness.
Upon statistical analysis of trapezius muscle stiffness measurements by SWE in whiplash and control
groups, we have demonstrated a high sensitivity of
this method. Therefore, we are able to claim, with
more than 90% probability that the patient with muscle stiffness below 76 kPa is not in the whiplash injury
group. Specificity of this method is somewhat lower
(around 70%) meaning we correctly position a person
in the whiplash injury group in 7 out of 10 cases, if
they measure above 76 kPa of trapezius muscle stiffness as determined by SWE.
Ultrasound SWE is the only method that can objectively quantify muscle stiffness, while all other
methods are subjective. We believe that elastography
should be a part of the standardized examination in
whiplash injury patients in order to quantify the level
of neck muscle stiffness. This measurement would be
useful for patient follow-up and unbiased evaluation
of response to physical therapy procedures.
Among numerous advantages of elastography the
most prominent ones are that it is not time consuming and it is not harmful for the patient or the
examiner. Furthermore, elastography can easily detect patients who have prolonged muscle spasm and
therefore should be selected and subjected to early
physical therapy in order to prevent development of
chronic neck pain. The clinical prediction tool is reported in scientific papers that addresses prognosis
of whiplash injury and it consists of eight different
predictor variables. Some of them, like older age
and initially higher levels of neck disability index,
have shown positive predictive value for developing
moderate disability; however, stiffness of the muscles
in the neck region, especially the trapezius, has not
been included as a clinical prediction tool variable
and we as authors believe it should be considered as
a strong candidate as this is a quantitative variable
and it is easily obtainable by SWE when performed by
an experienced radiologist.
Although there have been reports of positive effect of low-frequency electric stimulation on erector
spinae muscle and far-infrared irradiation of cervical
muscles, quantitative measures on decrease of spasm
are not currently known [22]. Further research is
needed on the effect of other physical therapy modalities such as exercise [23], ultrasound, paraffin and
transcutaneous electric nerve stimulation (TENS) on
whiplash-associated disorders as already suggested
by other authors [24] and we likewise propose that
quantifying muscle stiffness of trapezius muscle by
SWE before and after these procedures could show
us which treatment is the best for decreasing muscle
stiffness.
The major limitation of this study is that interrater
reliability of the SWE could not be calculated because
there was only one experienced musculoskeletal radiologist for the SWE employed in our institution. The
examination was standardized in a way that two ROIs
were picked in each muscle at the thickest part of the
muscle (without the fascia) and three measurements
were made in each muscle for every ROI and that the
mean value from those six values was used for statistical analysis. Furthermore, these measurements where
used to calculate intrarater reliability. Standardization
of the pressure during SWE examination was done
by using minimal pressure of the ultrasound probe
against the skin to prevent tissue from deforming and
thus inadvertently increasing muscle stiffness.
Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?
K
original article
Conclusion
Increased muscle stiffness was noticed in trapezius
muscle bilaterally in the whiplash group when compared to the control group (p < 0.001; right 57.47 ±
13.82 vs. 87.84 ± 23.23; left 54.4 ± 12.68 vs. 87.21 ±
26.47 kPa). Muscle stiffness in splenius capitis and
sternocleidomastoid muscles was not suitable for
analysis because of asymmetrical data distribution.
Patients with less than 76 kPa of muscle stiffness in
trapezius muscle are unlikely to belong in whiplash
injury group (sensitivity 90% for right and 97% for
left trapezius muscle, specificity 72% and 73%, respectively). Further research on this subject could
conclude whether stratification of patients after uncomplicated whiplash injury can be made with ultrasound SWE of trapezius muscle stiffness. Further
follow-up of the patients measuring higher than cutoff value might be beneficial for detecting patients
with prolonged neck muscle spasm that can lead to
chronic cervical pain syndrome.
Acknowledgements The authors would like to acknowledge
Professor Goran Kardum, PhD, for statistical analysis, Ana
Krnić, MD and Benjamin Benzon, MD, PhD for their help
with the study design, and Renato Igrec MD for drawing the
ultrasound probe positioning.
Conflict of interest J. Aljinović, I. Barišić, A. Poljičanin,
S. Kuzmičić, K. Vukojević, D. Gugić Bokun, and T. Vlak
declare that they have no competing interests.
References
1. Connelly LB, Supangan R. Theeconomiccostsof roadtraffic
crashes: Australia, states and territories. Accid Anal Prev.
2006;38(6):1087–93.
2. Ritchie C, Sterling M. Recovery pathways and prognosis after whiplash injury. J Orthop Sports Phys Ther.
2016;46(10):851–61.
3. Sterling M. Whiplash-associated disorder: musculoskeletal
pain and related clinical findings. J Man Manip Ther.
2011;19(4):194–200.
4. Koren L, PeledE, Trogan R, Norman D, BerkovichY, IsraelitS.
Gender, age and ethnicity influence on pain levels and
analgesic use in the acute whiplash injury. Eur J Trauma
Emerg Surg. 2015;41(3):287–91.
5. Carriere JS, Thibault P, Milioto M, Sullivan MJL. Expectancies mediate the relations among pain catastrophizing, fear
of movement, and return to work outcomes after whiplash
injury. J Pain. 2015;16(12):1280–7.
6. Carstensen TB. The influence of psychosocial factors on
recovery following acute whiplash trauma. Dan Med J.
2012;59(12):B4560.
7. Paluch L, Nawrocka-Laskus E, Wieczorek J, Mruk B, Frel M,
Walecki J. Use of ultrasound elastography in the assessment
of the musculoskeletal system. Pol J Radiol. 2016;81:240–6.
8. Brandenburg JE, Eby SF, Song P, Zhao H, Brault JS, Chen S,
et al. Ultrasound elastography: the new frontier in direct
measurement of muscle stiffness. Arch Phys Med Rehabil.
2014;95(11):2207–19.
K
9. Brandenburg JE, Eby SF, Song P, Zhao H, Landry BW, Kingsley-Berg S, et al. Feasibility and reliability of quantifying passive muscle stiffness in young children by using
shear wave ultrasound elastography. J Ultrasound Med.
2015;34(4):663–70.
10. Leong HT, Ng GY, Leung VY, Fu SN. Quantitative estimation
of muscle shear elastic modulus of the upper trapezius with
supersonic shear imaging during arm positioning. Plos
One. 2013;8(6):e67199.
11. Xie Y, Thomas L, Hug F, Johnston V, Coombes BK. Quantifying cervical and axioscapular muscle stiffness using shear wave elastography. J Electromyogr Kinesiol.
2019;48:94–102.
12. Spitzer WO, Skovron ML, Salmi LR, Cassidy JD, Duranceau J,
SuissaS,etal. ScientificmonographoftheQuebectaskforce
on whiplash-associated disorders: redefining “whiplash”
and its management. Spine. 1995;20(8 Suppl):1S–73S.
13. Dhyani M, Grajo JR, Bhan AK, Corey K, Chung R, Samir AE.
Validation of shear wave elastography cutoff values on
the supersonic Aixplorer for practical clinical use in liver
fibrosis staging. Ultrasound Med Biol. 2017;43(6):1125–33.
14. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86(2):420–8.
15. McClune T, Burton AK, Waddell G. Whiplash associated
disorders: a review of the literature to guide patient information and advice. Emerg Med J. 2002;19(6):499–506.
16. WaltonDM,MacdermidJC,GiorgianniAA,MascarenhasJC,
West SC, Zammit CA. Risk factors for persistent problems
following acute whiplash injury: update of a systematic
review and meta-analysis. J Orthop Sports Phys Ther.
2013;43(2):31–43.
17. Curatolo M. Pharmacological and interventional management of pain after whiplash injury. J Orthop Sports Phys
Ther. 2016;46(10):845–50.
18. Nikles J, Yelland M, Bayram C, Miller G, Sterling M. Management of whiplash associated disorders in Australian general
practice. BMC Musculoskelet Disord. 2017;18(1):551.
19. Helliwell PS, Evans PF, Wright V. The straight cervical spine:
does it indicate muscle spasm? J Bone Joint Surg Br.
1994;76(1):103–6.
20. Beltsios M, Savvidou O, Mitsiokapa EA, Mavrogenis AF,
Kaspiris A, Efstathopoulos N, et al. Sagittal alignment of
the cervical spine after neck injury. Eur J Orthop Surg
Traumatol. 2013;23(Suppl 1):47–51.
21. Grob D, Frauenfelder H, Mannion AF. The association
between cervical spine curvature and neck pain. Eur
Spine J. 2007;16(5):669–78.
22. Matsui T, Iwata M, Endo Y, Shitara N, Hojo S, Fukuoka H,
et al.
Effect of intensive inpatient physical therapy
on whole-body indefinite symptoms in patients with
whiplash-associated disorders. BMC Musculoskelet Disord. 2019;20(1):251.
23. MichaleffZA,MaherCG,LinCW,RebbeckT,JullG,LatimerJ,
et al. Comprehensive physiotherapy exercise programme
or advicefor chronicwhiplash(PROMISE): apragmaticrandomised controlled trial. Lancet. 2014;384(9938):133–41.
24. Sterling M. Physiotherapy management of whiplash-associated disorders (WAD). J Physiother. 2014;60(1):5–12.
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Can measuring passive neck muscle stiffness in whiplash injury patients help detect false whiplash claims?