Original article

The relationship between supercial muscle activity during the cranio-cervical

exion test and clinical features in patients with chronic neck pain
Shaun OLeary
a, b,
*
, Deborah Falla
c, d
, Gwendolen Jull
a
a
NHMRC Centre for Clinical Research Excellence in Spinal Pain, Injury and Health, The University of Queensland, Brisbane, Australia
b
Physiotherapy Department, Royal Brisbane and Womens Hospital, Brisbane, Australia
c
Pain Clinic, Center for Anesthesiology, Emergency and Intensive Care Medicine, University Hospital Gttingen, Gttingen, Germany
d
Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Gttingen, Georg-August University, Gttingen,
Germany
a r t i c l e i n f o
Article history:
Received 6 October 2010
Received in revised form
9 December 2010
Accepted 11 February 2011
Keywords:
Neck pain
Electromyography
Cervical exors
a b s t r a c t
Changes in motor behavior are a known feature of chronic mechanical neck pain disorders. This study
examined the strength of the association between reported levels of pain and disability from 84 indi-
viduals (63 women, 21 men) with chronic mechanical neck pain and levels of electromyographic activity
recorded from supercial cervical exor (sternocleidomastoid; SCM and anterior scalene; AS) muscles
during progressive stages of the cranio-cervical exion muscle test. A signicant positive association was
observed between supercial muscle activity and pain intensity (P < 0.003), but not pain duration
(P > 0.5) or perceived disability (P > 0.21). The strongest relationship between pain intensity and
supercial muscle activity occurred at the nal increment of the cranio-cervical exion test (inner-range
test position) for both the SCM and AS muscles (R
2
0.16). Although a positive and signicant rela-
tionship between pain intensity and supercial muscle activity was shown, the relationship was only
modest (16% explained variance), indicating that multiple factors contribute to the altered motor func-
tion observed in individuals with chronic mechanical neck pain.
2011 Elsevier Ltd. All rights reserved.
1. Introduction
Chronic mechanical neck pain (CMNP) is a nonspecic disorder
that is characteristically aggravated by neck movement and activity
(Bogduk, 1984) with a course marked by periods of remission and
exacerbation (Cote et al., 2004). During any 6-month period 54% of
adults suffer from CMNP (Cote et al., 1998) and only 6.3% of indi-
viduals who suffered fromneck pain in the previous year are free of
recurrence (Picavet andSchouten, 2003). It has beenspeculatedthat
aberrant cervical motor behavior may contribute to the persistence
of CMNPdue tofactors suchas the perpetual mechanical irritationof
cervical structures and muscle fatigue (Panjabi, 1992; Jull et al.,
2008b; Madeleine, 2010). Certainly within the literature there is
mounting evidence of an association between CMNP and altered
neuromuscular control (OLeary et al., 2009; Madeleine, 2010).
One aspect of altered neuromuscular control that has been
shown to be characteristic of CMNP is heightened activity of the
supercial cervical exor muscles, namely the sternocleidomastoid
and anterior scalene muscles. Elevated activity of these muscles has
been observed in participants with neck pain during repetitive
upper limbs tasks, (Falla et al., 2004a) as well as during specic
muscle tests of cervical motor performance. In particular, height-
ened activity of these muscles in individuals with neck pain
compared to healthy controls have been reported in multiple
studies that have utilized the Cranio-Cervical Flexion Test (CCFT)
(Falla et al., 2004b; Jull et al., 2004b, 2007), which is a lowintensity
graded test of cervical exor muscle performance (Jull et al., 2008a).
Several reasoned hypotheses have been offered as to the underlying
cause of the heightened activity of these supercial muscles. These
hypotheses include factors such as compensatory mechanisms for
coinciding decits in deep cervical exor function (Falla et al.,
2004b), changes in muscle spindle sensitivity through sympa-
thetic activation (Passatore and Roatta, 2006), reex-mediated
adaptation of motor neuron discharges to pain (Sohn et al., 2000;
Farina et al., 2004), alterations in cortical excitability and changes
in the descending drive to muscles (Le Pera et al., 2001) as well as
psychological distress (Bansevicius and Sjaastad, 1996; Nilsen et al.,
2006). At this stage the exact mechanismunderlying the changes in
* Corresponding author. NHMRC Centre for Clinical Research Excellence in
Spinal Pain, Injury and Health, The University of Queensland, Brisbane, Australia.
Tel.: 61 7 3636 2290; fax: 61 7 3365 2775.
E-mail address: shaun_oleary@health.qld.gov.au (S. OLeary).
Contents lists available at ScienceDirect
Manual Therapy
j ournal homepage: www. el sevi er. com/ mat h
1356-689X/$ e see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2011.02.008
Manual Therapy 16 (2011) 452e455
neuromuscular control in relation to CMNP are unclear and are
most likely multifaceted.
What is also unclear is the relationship between changes in
neuromuscular control and the severity of patient-reported sym-
ptoms. While some studies infer a relationship between altered
levels of muscle activation and discomfort in cervical spine disor-
ders (Szeto et al., 2005; stensvik et al., 2009), there is generally
a lack of studies examining the strength of the relationship
between clinical symptoms and altered muscle activity. The
purpose of this study was to examine the magnitude of the rela-
tionship between reported levels of neck pain and disability and
activation of the supercial cervical exor muscles during the CCFT
inpatients with CMNP. It is anticipated that the ndings will further
clarify the relationship between clinical symptoms and physical
ndings in the assessment of CMNP that will further inform deci-
sion making in the clinical management of this condition.
2. Methods
2.1. Design
This was a cohort study utilizing individual participant data
fromtwo previous trials conducted in our laboratory (OLeary et al.,
2008; Jull et al., 2009).
2.2. Subjects
Eighty-four volunteers (63women) withCMNP(age; meanSD;
37.5 12.1 yrs) participated in the study. Participants were included
if theywereagedbetween18and60years, reporteda historyof neck
pain of greater than six months duration, scored 5 points or greater
out of a possible 50 points on the Neck Disability Index (NDI)
(Vernon, 1996), and demonstrated positive ndings on a physical
examination of the cervical spine (altered joint motion and painful
reactivity to palpation) (Jull, 1994). Participants were excluded if
theyhadundergone anexercise programtoconditionthe muscles of
their neck or shoulder girdle in the preceding six months, if they
experienced neck pain or headache from non-musculoskeletal
causes or demonstrated neurological signs.
Participants were recruited from the University and general
community. Ethical clearance for the study was granted by the
Universitys Medical Research Ethics Committee and the study was
conducted in accordance with the declaration of Helsinki. Informed
consent was obtained from each subject.
2.3. Measurements and procedures
Following inclusion into the study, participants completed self-
reported measurements of neck pain and disability followed by the
measurements of supercial cervical exor muscle activity during
an isometric cranio-cervical exion task.
2.3.1. Self-reported measurements of neck pain and disability
Visual Analogue Scale (VAS): Participants were asked to indicate
their average neck pain intensity over the previous week by placing
a mark on a 100 mm line bordered at one end by the words no
pain and the other end by the words worst pain ever (Kelly,
2001).
Neck Disability Index (NDI): The NDI is a 10-item questionnaire
relating to daily activities and cervical spine related pain. Each item
is scored from 0 to 5, and the total score out of 50 points is
summated (MacDermid et al., 2009).
Duration of Neck Pain (DUR): The duration of the patients
painful symptoms was recorded in months.
2.3.2. Cranio-cervical exion test (CCFT)
Bipolar surface EMGsignals were detected fromthe sternal head
of the sternocleidomastoid (SCM) and anterior scalene (AS)
muscles bilaterally during the CCFT in accordance with an estab-
lished protocol (Jull et al., 2008a). Pairs of electrodes (Grass Tech-
nologies) were positioned 20 mm apart over the SCM and AS
following skin preparation and using guidelines for electrode
placement (Falla et al., 2002). EMG data were bandpass ltered
between 20 and 450 Hz and sampled at 2048 Hz (ASE16 amplier,
LISiN Centro di Bioingegneria, Italy) and converted to digital form
by a 12-bit analog-to-digital converter. A reference electrode was
placed around the right wrist.
The CCFT was conducted using the standard clinical protocol
(Jull et al., 2008a). Subjects were comfortably positioned in supine,
crook lying with the head and neck in a mid-position and were
instructed to perform a cranio-cervical exion action (anatomical
action of the deep cervical exors). The task consisted of ve
incremental movements of increasing cranio-cervical exion range
of motion. Performance was guided by visual feedback from an air-
lled pressure sensor (Stabilizer, Chattanooga Group Inc. USA)
which was placed sub-occipitally behind the subjects neck and
inated to a baseline pressure of 20 mmHg. The pressure sensor
monitors the slight attening of the neck which occurs with the
contraction of the longus capitis and longus colli muscles (Mayoux
Benhamou et al., 1994). During the test, subjects were required to
perform the gentle nodding motions of cranio-cervical exion that
progressed in range to increase the pressure by ve incremental
levels, with each increment representing 2 mmHg (22e30 mmHg).
Subjects practiced targeting the ve test levels between 22 and
30 mmHg in two practice trials before the electrodes were applied.
Following the application of electrodes participants performed
a standardized manoeuvre for EMG normalization (reference
voluntary contraction). This reference voluntary contraction inv-
olved a head lift (cervical and cranio-cervical exion) just clear of
the bed which was maintained for 10 s during which EMG data was
recorded. One minute rest period was given before participants
then performed the experimental CCFT condition during which
EMG data was recorded. The experimental CCFT condition included
all ve stages of the test (22e30 mmHg) with participants ins-
tructed to maintain the pressure steady on each stage target for
10 s, and resting for 30 s between stages. For each of the incre-
mental pressure levels tested, recording of EMG data commenced
when it was observed by the investigator that the participant had
reached the pressure target. A consistent starting point for each
level tested was attained by ensuring the participant had returned
to the neutral head/neck position which corresponded to the pre-
ssure level reading of 20 mmHg.
2.4. Data management and statistical analysis
To obtain a measure of EMG signal amplitude, the root mean
square (RMS) of the EMGwas calculated fromintervals of 1 s during
the 10 s contractions. The values of RMS were expressed as a per-
centage of the maximumRMS value during the reference voluntary
contraction (head lift). Because the RMS values for the left and right
SCM or AS muscles did not differ statistically, the data were aver-
aged across sides.
Associations between changes in EMG RMS recorded from
the SCM and AS muscles during the cranio-cervical exion test
(5 factors: 22, 24, 26, 28, 30 mmHg increments) and pain and
disability characteristics (VAS, DUR, NDI) were investigated using
a repeated-measures ANOVA. Signicant associations between pain
and disability characteristics and EMG RMS were the further eval-
uated using multiple regression analyses which were performed
S. OLeary et al. / Manual Therapy 16 (2011) 452e455 453
separately for the SCM and AS muscles. Signicance was set at
P < 0.05.
3. Results
Pain and disability characteristics (average standard devia-
tion, range) of participants included a VAS score of 3.7 1.8, 0.9e9)/
10 mm, an NDI score of 10.6 2.4, 5e16)/50 points, and a duration
of symptoms of 7.6 6.9, 0.5e40) years.
A signicant association was observed between the changes in
SCM RMS recorded during the 5 stages of the test and the VAS
measure (P < 0.001) but not the DUR (P 0.52) or NDI (P 0.67)
measures. Similarly, changes in the AS RMS during the test showed
a signicant association with the VAS measure (P 0.002) but not
the DUR (P 0.82) or NDI (P 0.23) measures. As shown in Table 1,
the regression analysis indicated that although the VAS measure
was signicantly related to the RMS values of both muscles (SCM,
AS) for all 5 stages of the test (P < 0.04), the R
2
values were largest
for the nal increment of the test (30 mmHg) for both the SCM and
AS muscles (R
2
0.16) as depicted in Fig. 1.
4. Discussion
Heightened activity of muscles is commonly reported in studies
involving participants with CMNP (Szeto et al., 2005; stensvik
et al., 2009). Multiple studies have shown CMNP to be associated
with heightened activity of the supercial cervical exor muscles
(sternocleidomastoid and anterior scalene) during the CCFT (Falla
et al., 2004b; Jull et al., 2004b, 2007). This study has shown, that
in participants with CMNP, the level of supercial cervical exor
muscle activity during the CCFT bears a positive relationship with
the level of reported pain intensity.
As depicted in Fig. 1, higher magnitudes of supercial cervical
exor activity during the CCFT were observed in those participants
with higher levels of reported pain intensity. This relationship was
signicant for both the sternocleidomastoid and anterior scalene
muscles. Experimental studies suggest that the reorganization of
neuromuscular control in CMNP such as those observed in this
study, may reect compensatory neural strategies, redistributing
loads between muscles to sustain motor and force output to ach-
ieve a task such as the CCFT (Ge et al., 2005; Falla et al., 2007). Its
considered that in the long term, these neuromuscular adaptations
may contribute to the persistence of painful cervical disorders due
to factors such as muscle fatigability and prolonged mechanical
irritation of cervical structures (Panjabi, 1992; Falla and Farina,
2005; Jull et al., 2008b; Madeleine, 2010).
Caution needs to be taken in interpreting the ndings of this
study. Although the relationship between pain intensity and
supercial muscle activity was signicant, pain intensity only
accounted for up to 16% of supercial muscle activity during the
CCFT (Table 1). It is apparent that pain intensity is not the only factor
impacting on alterations of neuromuscular control of the neck in
patients with CMNP, the underlying mechanisms of which are likely
to be multifaceted. Furthermore these ndings are only relevant for
supercial muscle activity during the CCFT. Additional studies will
need to be performed before inferences can be made of the rela-
tionship between supercial muscle activity and pain during other
activities of the cervical spine andupper limb. Notwithstanding this,
these ndings support the notion that heightened activity of
supercial cervical exor muscles is associatedwithneckpainwhich
has underpinned recommendations for cervical neuromuscular
evaluation in the clinical management of neck pain (Jull et al.,
2004a). Furthermore the ndings lend support to clinical recom-
mendations for minimizing supercial muscle activity when
training cranio-cervical exion in the management of individuals
with CMNP (Jull et al., 2008b).
In contrast to the ndings for pain intensity, there was no
relationship between supercial cervical exor activity during the
CCFT and the duration of neck pain or the level of neck disability as
measured using the NDI. The lack of correlation between muscle
activity and duration of symptoms is not surprising. Previous
studies have shown that heightened activity of the supercial
cervical exor muscles occurs quickly (within 1 month) in patients
with a whiplash injury following a motor vehicle accident (Sterling
et al., 2003). Furthermore, increased activity of the sternocleido-
mastoid has been observed immediately in healthy volunteers
following physiological sympathetic activation elicited by the cold
pressor test (Boudreau et al., 2010). Similarly, studies investigating
experimentally induced muscle pain in healthy volunteers have
shown immediate changes in neuromuscular control of the cervical
spine, although the direction of response (increase or decrease in
muscle activity) is variable and task-dependent (Falla et al., 2007).
Table 1
Regression analysis results (B, P, and R
2
values) indicating the relationship between
measures of pain intensity (Visual Analogue Scale) and normalized root mean square
values for both the sternocleidomastoid and anterior scalene muscles.
Sternocleidomastoid Anterior Scalene
B P R
2
B P R
2
22 mmHg 0.05 0.02 0.07 0.04 0.03 0.06
24 mmHg 0.03 0.01 0.08 0.04 <0.001 0.14
26 mmHg 0.03 0.001 0.12 0.03 0.001 0.13
28 mmHg 0.02 0.002 0.11 0.02 0.002 0.11
30 mmHg 0.02 <0.001 0.16 0.02 <0.001 0.16
Fig. 1. Scatter plot of pain visual analogue scale (VAS) values and normalized root
mean square values for the anterior scalene (A) and sternocleidomastoid (B) muscles
recorded during the nal stage of the cranio-cervical exion test (30 mmHg).
S. OLeary et al. / Manual Therapy 16 (2011) 452e455 454
It should be noted that the ndings of this study only relate to
sternocleidomastoid and anterior scalene muscle activity. For
a comprehensive evaluation of the relationship between painful
symptoms and neuromuscular dysfunction, further studies need to
evaluate other cervical muscles inpatients with neck pain. Similarly
only one measure of pain intensity (average pain intensity over the
previous week) was utilized in this study, future studies may wish
to consider other pain intensity ratings (current, best, worst over
the past 24 h) (Cleland et al., 2008) by which to examine the rel-
ationship with physical ndings such as muscle activity. Further-
more results can only be inferred for chronic neck pain of an
insidious onset and not for neck pain of a traumatic onset such as
that experienced by individuals with a whiplash injury.
5. Conclusion
The ndings of this study support a relationship between neck
pain and altered neuromuscular function. This study has shown
that the magnitude of supercial muscle activity during the CCFT is
related to the level of patient-reported pain intensity, not the
duration of painful symptoms or the level of patient-reported neck
disability. Although the relationship between supercial muscle
activity and pain intensity was statistically signicant, it should be
noted that the relationship was only modest and probably reects
that there are multifaceted contributors to altered neuromuscular
function associated with chronic mechanical neck pain. For clini-
cians managing painful cervical spine disorders, the ndings
support the inclusion of neuromuscular assessment and the pre-
scription of therapeutic exercise to address neuromuscular dys-
function as a management strategy.
Acknowledgments
SupportedbytheDanishMedical ResearchCouncil (271-08-0795).
Shaun OLeary is supported by a Queensland Health, Health
Practitioner Research Fellowship, and an NHMRC of Australia
Research Training Fellowship.
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