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Original article

Association between neck muscle coactivation, pain, and strength


in women with neck pain
Rene Lindstrm
a
, Jochen Schomacher
a
, Dario Farina
a
, Lotte Rechter
b, c
, Deborah Falla
a,
*
a
Center for SensoryeMotor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Fredrik Bajers Vej 7 D-3, DK-9220 Aalborg, Denmark
b
Multidisciplinary Pain Center, Aalborg, Denmark
c
Department of Occupational Therapy and Physiotherapy, Aalborg Hospital, Aarhus University Hospital, Aalborg, Denmark
a r t i c l e i n f o
Article history:
Received 14 April 2010
Received in revised form
7 July 2010
Accepted 12 July 2010
Keywords:
Neck pain
Coactivation
Preferred direction
Neck muscles
a b s t r a c t
This study investigates the relationship between neck muscle coactivation, neck strength and perceived
pain and disability in women with neck pain. Surface electromyography (EMG) was acquired from the
sternocleidomastoid (SCM) and splenius capitis (SC) muscles of 13 women with chronic neck pain and 10
controls as they performed 1) maximal voluntary contractions (MVC) in exion, extension and left and
right lateral exion, 2) ramped contractions from 0% to 50% MVC in exion and extension and 3) circular
contractions in the horizontal plane at 15 N and 30 N force. Higher values of EMG amplitude were
observed for the SC (antagonist) during ramped neck exion and for the SCM during ramped extension in
the patient group (P <0.05). The patients displayed reduced values of directional specicity in the
surface EMG of the SCM and SC for the circular contractions (P <0.05). The EMG amplitude of SC during
cervical exion was positively correlated with the patients pain (R
2
0.35, P <0.05) and perceived
disability (R
2
0.53, P <0.01). An inverse correlation was evident between the amount of activation of SC
during cervical exion and strength (R
2
0.54, P <0.01). These observations indicate a relationship
between alterations in neuromuscular control in patients with neck pain and functional consequences,
including impaired motor performance and increased levels of perceived disability.
2010 Elsevier Ltd. All rights reserved.
1. Introduction
Chronic neck pain is a common musculoskeletal disorder
(Picavet and Schouten, 2003; Webb et al., 2003). Epidemiological
studies show a lifetime prevalence of neck pain between 43% and
66.7% (Bovim et al., 1994; Ct et al., 1998, 2004; Guez et al., 2002),
a one-year prevalence rate which ranges between 17.9% (Croft et al.,
2001) and 64% (Niemelinen et al., 2006), and a point prevalence
around 20% (Ct et al., 1998; Picavet and Schouten, 2003). Neck
pain is also associated with a high recurrence rate (Ghaffari et al.,
2006; Holmberg and Thelin, 2006) and, subsequently, high
economic costs (Korthals-de Bos et al., 2003).
Altered activation of the neck muscles is a well-known feature of
neck pain. Patients with neck pain show increased antagonistic
activity of their supercial neck muscles (Falla et al., 2004a;
Fernndez-de-las-Peas et al., 2008). Reduced specicity of ster-
nocleidomastoid muscle activation was observed in patients with
neck painwhenperforming isometric contractions with continuous
change in force direction in the range 0e360

, resulting in
increased activation of the muscle when acting as an antagonist
(Falla et al., 2010). This result supports the consistent nding of
augmented activity of the supercial neck muscles in patients with
neck pain (Falla et al., 2004b; Szeto et al., 2005; OLeary et al., 2007;
Johnston et al., 2008). These observations are also in agreement
with experimental pain studies which show a pain-induced reor-
ganization of the motor strategy characterized by reduced activity
of the agonist muscle and increased activity of the antagonist
muscle (Graven-Nielsen et al., 1997). Possible explanations for
these ndings include the direct effects of nociception on motor
neuron output, effects of pain on sympathetic activity, and changes
in motor planning.
Although increased coactivation of the neck muscles may be
benecial inthepresenceof acutepaintoenhancecervical stabilityby
reducing velocity and range of movement, it may reduce neck
strength and contribute to recurrent pain by altering the load distri-
bution on the spine and irritating pain sensitive structures. However,
therelationshipbetweenneck muscle coactivation, strengthandpain
intensity is unknown. Therefore, the purpose of this study is to
investigate the relationship between the extent of neck muscle
coactivation, the maximum amount of neck strength and perceived
pain and disability in women with persistent neck pain.
* Author for correspondence. Tel.: 45 99 40 74 59; fax: 45 98 15 40 08.
E-mail address: deborahf@hst.aau.dk (D. Falla).
Contents lists available at ScienceDirect
Manual Therapy
j ournal homepage: www. el sevi er. com/ mat h
1356-689X/$ e see front matter 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2010.07.006
Manual Therapy 16 (2011) 80e86
2. Methods
2.1. Subjects
Thirteen women with chronic neck pain greater than 1 year
(mean SD: 7.1 6.1 yrs) participated in the study. Subjects were
excludedif theypreviouslyhadcervical spine surgery, previous neck
trauma, presented with neurological signs in the upper limb or had
participated in a neck exercise program in the past 12 months.
Ten women were recruited as controls. Control subjects were
free of shoulder and neck pain, had no past history of orthopedic
disorders affecting the shoulder or neck region and no history of
neurological disorders. Ethical approval for the study was granted
by the Ethics Committee (nr 20070045) and the procedures were
conducted according to the Declaration of Helsinki.
2.2. Procedure
Participants were seated with their head rigidly xed in a device
for the measurement of multidirectional neck force (Aalborg
University, Denmark) with their back supported, knees and hips in
90

of exion and their torso rmly strapped to the seat back. The
device is equipped with eight adjustable contacts which are
fastened around the head to stabilize the head and provide resis-
tance during isometric contractions of the neck. The force device is
equipped with force transducers (strain gauges) to measure force in
the sagittal and coronal planes. The electrical signals fromthe strain
gauges were amplied (LISiN e OT Bioelettronica, Torino, Italy) and
their output was displayed on an oscilloscope as visual feedback to
the subject.
Following a period of familiarization with the measuring device
and practice of the contractions, subjects performed two maximum
voluntary contractions (MVC) for cervical exion, extension, left
lateral exion, and right lateral exion, with 1-min rest between
contractions. Verbal encouragement was provided to the subject to
promote higher forces in each trial. The highest value of force
recorded over the 2 maximum contractions for each direction was
selected as the reference MVC, and used to calculate the sub-
maximal force targets. The order of the MVC contractions was
randomized between movement directions.
A rest of 30 min followed the MVCs. Subsequently, the subjects
performed a linearly increasing force contraction from 0% to 50%
MVC in 3 s (ramp contraction) in cervical exion and extension.
Visual feedback on force was provided to the subject during these
contractions. A rest of 2-min was provided between contractions
which were randomized for force direction.
Following a further 10 min of rest, the subjects performed an
isometric contraction at 15 and 30 N force in the horizontal plane
against the head restraint with change in force direction in the
range 0e360

(circular isometric contractions). Circular templates


were superimposed on the oscilloscope to provide force feedback
to the subjects during these contractions. Following a period of
w10 min to practice for the task, the subjects performed the 15 and
30 N contractions in both clockwise and counter-clockwise direc-
tions with 2-min of rest between contractions. Each circular
contraction had a duration of w12 s and was performed at constant
velocity by the subjects under guidance of a counter for time and
visual feedback on force direction and magnitude. The direction of
the contractions was randomized and each contraction was fol-
lowed by rest periods of 2-min.
2.3. Electromyography recordings
Bipolar surface electromyography (EMG) signals were detected
from the sternal head of the sternocleidomastoid and splenius
capitis muscles bilaterally with pairs of electrodes (Neuroline
72001-k; Medicotest, Denmark) positioned 20 mm apart following
skin preparation. For the splenius capitis, electrodes were posi-
tioned over the muscle belly at the C2eC3 level between the
uppermost parts of trapezius and sternocleidomastoid. For the
sternocleidomastoid muscle, electrodes were placed over the distal
portion of the muscle belly (Falla et al., 2002). The bipolar EMG
signals were amplied (128-channel surface EMG amplier, LISiN-
OT Bioelettronica, Torino, Italy; 3 dB bandwidth 10e500 Hz) by
a factor of 2000, sampled at 2048 Hz, and converted to digital form
by a 12-bit A/D converter. A ground electrode was placed around
the right wrist.
2.4. Signal analysis
For the ramped contractions, the force signal was low-pass
ltered (anti-causal Butterworth lter of order 4, cut-off frequency
10 Hz) and normalized with respect to the MVC force. The average
rectied value (ARV) was estimated from the EMG signals over 5
intervals of 250-ms duration, during which the average force level
was 10e50% MVC (10% MVC increments).
During the circular contractions, the surface EMG ARV was esti-
mated in intervals of 250 ms and analyzed as a function of the angle
of force direction (directional activation curve). The directional
activation curves represent the modulation in intensity of muscle
activity with the direction of force exertion and represent a closed
area when expressed in polar coordinates. The line connecting the
originwith the central point of this area dened a directional vector,
whoselengthwas expressedas a percent of themeanARVduringthe
entire task. This normalized vector length represents the specicity
of muscle activation: it is equal to zero when the EMG amplitude is
the same in all directions and corresponds to 100% when the EMG
amplitude is exclusivelyinone direction(the muscle is active inonly
one direction). In addition, the EMG amplitude was averaged across
the entire circular contraction to provide an indicator of the overall
muscle activity. Since no signicant differences were observed for
the data extracted from the circular contractions in the clockwise
and counter-clockwise directions, the data were combined to obtain
an average.
2.5. Statistical analysis
A two-way analysis of variance (ANOVA) was used to evaluate
differences between patients and controls for maximum neck
strength with group (patient, control) as the between subjects
variable and direction (exion, extension, right lateral exion, left
lateral exion) as the within subject variable.
The ARV of the sternocleidomastoid and splenius capitis
muscles during the ramped contractions was assessed with muscle
(left and right sternocleidomastoid and splenius capitis) and force
(10e50% MVC in 10% increments) as the within subject variables
and group (patient, control) as the between subjects variable.
A three-way ANOVA was conduced to assess differences in the
directional specicityof sternocleidomastoidmuscleactivity(vector
length) with force (15 N, 30 N) and muscle (left and right sterno-
cleidomastoid and splenius capitis) as the within subject variables
and group (patient, control) as the between subjects variable.
Signicant differences revealed by ANOVA were followed by post-
hoc StudenteNewmaneKeuls (SNK) pair-wise comparisons.
Linear correlation analysis was used to determine the associa-
tion between the patients average neck pain intensity, Neck
Disability Index (NDI) and the ARV of the sternocleidomastoid and
splenius capitis during the ramped contractions. Results are
reported as mean and SD in the text and SE in the gures. Statistical
signicance was set at P <0.05.
R. Lindstrm et al. / Manual Therapy 16 (2011) 80e86 81
3. Results
3.1. Participants
Patients did not differ (P >0.05) in age (37.7 7.8 yrs), weight
(77.2 18.5 kg) or height (168.8 4.0 cm) from controls (33.1 9.3
yrs, 66.8 13.0 kg, 165.9 8.2 cm respectively). The patients
average score for the Neck Disability Index (0e50) (Vernon and
Mior, 1991) was 21.6 8.4 and their average pain intensity rated
on a visual analogue scale (0e10) was 5.1 1.8.
3.2. Motor output
The maximumvoluntary neck strength was dependent on force
direction (F 46.7, P <0.00001); extension and bilateral lateral
exion showed higher values of force compared to exion (SNK: all
P <0.001). Furthermore, extension force was greater than left and
right lateral exion force (SNK: both P <0.05). However, the patient
group exerted lower force across all directions compared to the
control subjects (F 6.8, P <0.05; Table 1).
3.3. Ramp contractions
Both sternocleidomastoid and splenius capitis ARV increased
with increasing cervical exion force (F 110.7, P <0.0001, Fig. 1).
The ARV of sternocleidomastoid (agonist) did not differ between
patients and controls during cervical exion, however higher
values of ARV were observed for the right splenius capitis (antag-
onist) at all force levels in the patient group (SNK: all P <0.05,
Fig. 1). Higher values of left splenius capitis ARV were also observed
for the patient group during cervical exion at force levels 20e50%
(all SNK: P <0.05, Fig. 1).
Both splenius capitis (agonist) and sternocleidomastoid
(antagonist) ARV increased with increasing cervical extension force
(F 23.1, P <0.0001, Fig. 2). However, splenius capitis and sterno-
cleidomastoid ARV were greater for the patients across all force
levels compared to the control subjects (F 4.4, P <0.05, Fig. 2).
3.4. Directional activation curves
Representative directional activation curves during a circular
contraction performed at 15 N are illustrated in Fig. 3 for a control
subject and a patient. In this example, the control subject presents
with dened activation of the sternocleidomastoid and splenius
capitis muscles with the highest amplitude of activity towards
ipsilateral anterolateral exion and ipsilateral posterolateral
extension respectively. Note that both the sternocleidomastoid and
splenius capitis are minimally active during the antagonist phase.
Conversely, the directional activation curves for the representative
patient show activation of the sternocleidomastoid during exten-
sion and splenius capitis during exion supporting the results from
the isometric ramped contraction of increased antagonist muscle
activity.
Accordingly, overall the patient group displayed reduced values
of directional specicity in the surface EMG for both the sterno-
cleidomastoid and splenius capitis muscles bilaterally for both the
15 N and 30 N circular contractions (main effect for group: F 6.0;
P <0.05, Fig. 4).
3.5. Association between pain, strength and antagonist muscle
activity
The ARV of splenius capitis (averaged across sides) during
cervical exion was positively correlated with the patients repor-
ted pain (R
2
0.35, P <0.05) and perceived disability (R
2
0.53,
P <0.01) (Fig. 5). The ARV of splenius capitis (averaged across sides)
during cervical exion showed a tendency to be inversely corre-
lated with the patients maximum cervical exion force (R
2
0.26,
P 0.07, Fig. 6). When considering the total neck strength (sum
across all directions of force), the inverse correlation between the
amount of activation of splenius capitis during cervical exion and
neck strength was evident (R
2
0.54, P <0.01, Fig. 6). No correla-
tions were observed between the amount of activation of the
sternocleidomastoid muscle during cervical extension and the
patients strength (extension strength: R
2
0.00; P 0.97; total
Table 1
Mean SD of maximumvoluntary force (N) produced for cervical exion, extension,
right lateral exion and left lateral exion in patients with neck pain and control
subjects.
Force Direction Neck pain Controls Comparison between
patients and controls
Flexion 97.7 40.4 N 143.0 41.4 N P <0.05
Extension 182.5 77.7 N 235.7 54.6 N P <0.05
Right lateral exion 114.0 47.6 N 170.7 55.5 N P <0.05
Left lateral exion 119.8 49.2 N 176.7 46.0 N P <0.05
0
10
20
30
40
50
60
70
Control Right Side
Patient Right Side
Control Left Side
Patient Left Side
A
v
e
r
a
g
e

R
e
c
t
i
f
i
e
d

V
a
l
u
e

(

V
)
Agonist
10 20 30 40 50
Submaximal Force (% MVC)
A
Antagonist
0
10
20
30
40
50
60
A
v
e
r
a
g
e

R
e
c
t
i
f
i
e
d

V
a
l
u
e

(

V
)
10 20 30 40 50
Submaximal Force (% MVC)
B
Fig. 1. Mean SE of the left and right sternocleidomastoid (A) and splenius capitis (B) average rectied value during ramped cervical exion from 0% to 50% of the maximal
voluntary contraction (MVC) for the patient and control groups.
R. Lindstrm et al. / Manual Therapy 16 (2011) 80e86 82
neck strength: R
2
0.01; P 0.73) or perceived pain and disability
(pain: R
2
0.08; P 0.24; NDI: R
2
0.12; P 0.34).
4. Discussion
This study showed that patients with neck pain have higher
levels of coactivation of the sternocleidomastoid and splenius
capitis muscles compared to control subjects. Furthermore,
increased coactivation of the splenius capitis muscle was associated
with lower neck strength and higher levels of pain and associated
disability.
Patients with neck pain showed an overall reduction of neck
strength. Maximum strength was 31.7%, 22.6%, 33.2%, and 32.2%
less for the patients than controls for exion, extension, right lateral
0
10
20
30
40
50
60
10 20 30 40 50
Submaximal Force (% MVC)
A
v
e
r
a
g
e

R
e
c
t
i
f
i
e
d

V
a
l
u
e

(

V
)
Agonist
A
Antagonist
0
5
10
15
20
25
10 20 30 40 50
Submaximal Force (% MVC)
A
v
e
r
a
g
e

R
e
c
t
i
f
i
e
d

V
a
l
u
e

(

V
)
B
Control Right Side
Patient Right Side
Control Left Side
Patient Left Side
Fig. 2. Mean SE of the left and right splenius capitis (A) and sternocleidomastoid (B) average rectied value during ramped cervical extension from 0% to 50% of the maximal
voluntary contraction (MVC) for the patient and control groups.
60
240
30
210
0
180
330
150
300
120
270 90
60
240
30
210
180
330
150
300
120
270 90
0
60
240
30
210
0
180
330
150
300
120
270 90
60
240
30
210
180
330
150
300
120
270 90
0
Control Neck Pain
B
A
Fig. 3. Representative directional activation curves for the sternocleidomastoid (A) and splenius capitis (B) of a control subject and a patient performing a circular contraction in the
horizontal plane at 15 N with change in force direction in the range 0e360

.
R. Lindstrm et al. / Manual Therapy 16 (2011) 80e86 83
exion and left lateral exion, respectively, resulting in a total neck
strength which was 29.2% lower for the patient group. The strength
loss found in this study is similar to the results of several previous
studies. For example, Ylinen et al. (2004) reported a 29% force loss
in patients with neck pain for both exion and extension and Chiu
and Lo (2002) found reductions in force of 17.8%, 25.9%, 13.3%, and
16.3% for exion, extension, right lateral exion and left lateral
exion. However, there is a large variability in the results reported
in the literature and other studies showed greater reductions.
Pearson et al. (2009) found a 52% reduction in force in patients with
neck pain for exion, 60% for left lateral exion, 62% for right lateral
exion, and 66% for extension and Prushansky et al. (2005) repor-
ted a 90% reduction of neck force in all directions. Variability of neck
strength in patients is presumably due to differences in patient
populations (pain intensity, duration, cause of neck pain), but may
also reect varying degrees of neck muscle coactivation, which was
investigated in this study. Furthermore the general physical activity
level of the patients may inuence strength measurements and
may partially account for the reduced force output compared to
control subjects.
The sternocleidomastoid (Blouin et al., 2007; Falla et al., 2010)
and most extensor muscles (Blouin et al., 2007) have well-dened
preferred directions of activation in healthy subjects, which was
conrmed in this study. It has been shown that the directional
specicity of sternocleidomastoid muscle activity is reduced in
patients with neck pain and is associated with reduced modula-
tion of sternocleidomastoid motor unit discharge rate with
multidirectional force contractions (Falla et al., 2010). The results
of the current study show that reduced specicity of activity is not
unique to the sternocleidomastoid, since similar observations
were made for the splenius capitis muscle. Reduced specicity of
muscle activity results mainly in increased activation of the
muscle when acting as an antagonist (Fig. 3) and is consistent with
the increased antagonist activation of the extensors during the
ramped contraction. This suggests that increased antagonist
activity is a common feature associated with neck pain. Further-
more, the results of this study show that increased levels of neck
extensor antagonistic activity are associated with impaired neck
strength.
Increased neck muscle coactivation likely reects reorganiza-
tion of the motor control strategy potentially to enhance cervical
spine stability (Fernndez-de-las-Peas et al., 2008). Coactivation
of the neck exor and extensor muscles is considered a normal
strategy to increase stiffness of the spine (Cheng et al., 2008), for
example when a postural perturbation is applied to the trunk
(Danna-Dos-Santos et al., 2007). Up to 80% of cervical spine stability
is provided by the surrounding muscles (Panjabi, 1992), especially
the deeper muscles with their smaller moment arms and attach-
ments to adjacent vertebrae (Blouin et al., 2007). Weakness of the
deep cervical exor muscles is known to be present in patients with
neck pain and is associated with increased activity of supercial
synergists (Falla et al., 2003). Increased coactivation of neck
muscles may therefore indicate an attempt to enhance the stability
of the neck. Fear of pain during maximal contractions (kinesi-
ophobia) may also induce a strategy of increased neck muscle
coactivation. Fear of pain during neck extension is thought to limit
extensor force in patients with whiplash-induced neck pain who
often have injured posterior cervical spine structures (Prushansky
et al., 2005). However, a non-signicant correlation between
kinesiophobia and neck strength, and between pain catastrophiz-
ing and neck strength was shown in patients with chronic whiplash
(Pearson et al., 2009). Increased sternocleidomastoid and splenius
muscle activity for the patient group may also be due to an
0
5
10
15
20
25
30
35
40
Right SCM Left SCM Right SC Left SC
Neck Pain
Controls
0
5
10
15
20
25
30
35
40
A
B
R
e
l
a
t
i
v
e

m
u
s
c
l
e

s
p
e
c
i
f
i
c
i
t
y

t
o

d
i
r
e
c
t
i
o
n

(
%
)
R
e
l
a
t
i
v
e

m
u
s
c
l
e

s
p
e
c
i
f
i
c
i
t
y

t
o

d
i
r
e
c
t
i
o
n

(
%
)
Fig. 4. Mean SE of the directional specicity in the surface EMG of the right and left
sternocleidomastoid (SCM) and splenius capitis (SC) obtained during the circular
contractions at both 15 (A) and 30 N (B) of force for the patients with neck pain and
control subjects.
0 10 20 30 40
0
20
40
60
80
100
Neck Disability Index (0-50)
S
p
l
e
n
i
u
s

C
a
p
i
t
i
s

A
v
e
r
a
g
e

R
e
c
t
i
f
i
e
d

V
a
l
u
e

(

V
)
S
p
l
e
n
i
u
s

C
a
p
i
t
i
s

A
v
e
r
a
g
e

R
e
c
t
i
f
i
e
d

V
a
l
u
e

(

V
)
Average Neck Pain Intensity (0-10)
2 4 6 8
0
20
40
60
80
100
B
A
Fig. 5. Scatter plot of the splenius capitis average rectied value obtained during the ramped cervical exion contraction and the patients perceived disability rated on the Neck
Disability Index (A) and average neck pain intensity rated on a visual analogue scale (B).
R. Lindstrm et al. / Manual Therapy 16 (2011) 80e86 84
increased sympatho-adrenal outow as a consequence of pain.
Increased activity of the sternocleidomastoid and splenius muscle
has been observed in healthy volunteers following physiological
sympathetic activation elicited by the cold pressor test (Boudreau
et al., 2010).
Although increased coactivation of the neck muscles may be
benecial in the presence of pain to increase cervical stability, as
observed in this study, it is associated with functional conse-
quences, i.e. reduced neck strength. Furthermore, increased neck
muscle coactivation may contribute to recurrent pain by altering
the load distribution on the spine and subsequently aggravating
the patients condition. Coactivation of agonist/antagonist
muscles signicantly increases spinal stiffness (Lee et al., 2006)
and spinal compression which is considered sufcient to induce
lumbar spine injuries and consequently low-back pain (van Dien
and Kingma, 2005) and may also be relevant in persistent neck
pain disorders (Choi, 2003). Unique to this study, we showed that
the degree of coactivation of the splenius capitis muscle is
positively correlated with the patients reported pain and
perceived disability which supports this premise. Surprisingly,
a similar relation was not observed for the sternocleidomastoid
muscle despite reduced specicity of sternocleidomastoid
activity and increased activation of the sternocleidomastoid
muscle during the ramped cervical extension contraction in the
patient group. This nding may be attributed to the greater
reduction in neck exion strength for the patient group (31.7%
less than controls) compared to extension (22.6% less than
controls). That is, increased muscle coactivation may particularly
occur in the directions of least strength.
5. Conclusion
Patients with neck pain have higher levels of coactivation of the
sternocleidomastoid and splenius capitis muscles. Furthermore,
increased coactivation is associated with reduced neck strength
and higher levels of pain and associated disability. These observa-
tions indicate a relation between alterations in neuromuscular
control of the cervical spine in patients with neck pain and func-
tional consequences including impaired motor performance and
increased levels of perceived disability.
Acknowledgements
Supported by the Danish Medical Research Council, Kiropra-
ktorfonden, Denmark and stifterne, Denmark.
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Neck Flexion Strength (N) Total Neck Strength (N)
Fig. 6. Scatter plot of the splenius capitis average rectied value obtained during the ramped cervical exion contraction and the patients neck exion strength (A) and total neck
strength (B).
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