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Alterations in Cervical
4
Muscle Function in Neck Pain
Introduction
The combination of the number of muscles acting on the
cervical spine together with its capacity for multiple degrees
of freedom1 makes the cervical muscle system highly
redundant (Chapter 3). That is, specific forces may be
produced by several combinations of muscle actions.2 Given
the complexity of the cervical spine, it is not surprising that
neck pain induces a major reorganization of motor control
strategies.
Many techniques, such as electromyography (EMG),
magnetic resonance imaging, ultrasonography, muscle
biopsy, laser Doppler flowmetry, and cervical dynamometry,
have been used to expose a diverse range of neuromuscular
adaptations in people with neck pain.3–9 Studies utilizing
experimental neck pain models have also shed light on the
mechanisms underlying these changes.10 Knowledge gained
from cervical spine muscle research has underpinned our
specific approach to the assessment and rehabilitation of
cervical muscle function. This research has extended to the
development of therapeutic exercise regimes (Chapter 14)
that have shown positive therapeutic benefits when tested in
clinical trials.11–15
This chapter reviews evidence which describes alterations
cervical and axioscapular muscle function associated with
neck pain, explores the physiological mechanisms underlying
these observations, and provides the foundation for the
therapeutic exercise approach described in Chapter 14.
42 Whiplash, Headache, and Neck Pain
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Figure 4.1 Reorganization of cervical flexor muscle activity during craniocervical flexion: representative raw electromyogram (EMG) data
are shown for a control subject and person with neck pain during a task of staged craniocervical flexion. Data are shown for the deep
cervical flexors (DCF) and left (L) and right (R) anterior scalene (AS) and sternocleidomastoid (SM) muscles. Note the incremental increase
in EMG activity for all muscles with increasing craniocervical flexion (recorded as an increase in pressure in a pressure sensor under the
cervical spine) but with lesser activity in the deep cervical flexors and greater activity in the superficial muscles for the neck pain patient.
EMG calibration, 0.5 mV. (Reprinted from Falla et al.7 with permission.)
with neck pain during a typing task38 which muscle activity was observed during a
may also increase compressive loading on prolonged computer task.40 Moreover,
the spine. This may indicate a measurable significantly higher amplitude ratios of
compensation for poor passive or active upper trapezius/cervical extensor activity
segmental support.39 was identified for the patients complaining
A reorganization of cervical extensor and of the most discomfort throughout the task.
axioscapular muscle activity has also been Altered axioscapular muscle function is a
observed in persons with neck pain. common clinical observation in people with
Increased activity was found in the cervical cervical spine pain; however, its prevalence
extensors of office workers with neck pain in and role in the etiology of cervical spine
a 5-minute typing task.38 However, reduced disorders are not yet clearly understood.
activation of the cervical extensor muscles Alterations in scapular kinematics and
concomitant with increased upper trapezius axioscapular muscle activity have certainly
44 Whiplash, Headache, and Neck Pain
AD EMG
DCF EMG
(L) AS EMG
(R) AS EMG
(L) SM EMG
(R) SM EMG
100 ms
Figure 4.2 Delayed activation of the cervical flexor muscles during a perturbation: representative raw electromyogram (EMG) data are
shown for the anterior deltoid (AD), deep cervical flexors (DCF), left (L) and right (R) sternocleidomastoid (SM) and the anterior scalene
(AS) muscles for a control subject and person with neck pain during rapid upper-limb flexion. Line indicates onset of the anterior deltoid;
filled triangle denotes onset of neck muscle activation. Note the delayed activation of the neck muscles for the neck pain patient.
(Reprinted from Falla et al.6 with permission.)
observation of increased type IIC transitional chronic whiplash showed larger CSAs of
fibers is consistent with a transformation of multifidus and variable reductions in the
slow-twitch oxidative type I fibers to fast- CSAs in semispinalis cervicis and capitis.
twitch glycolytic type IIB fibers. This would The CSAs mirrored the degree of fatty
suggest a diminution of the tonic contractile infiltrate, indicating that both measures
capacity of the cervical muscles and is need to be considered in defining muscle
consistent with reduced endurance of the changes in neck pain.66
cervical muscles in patients with neck Muscle biopsies and laser Doppler
pain,18, 20, 61 particularly the reduced endurance flowmetry have also shown specific
determined for low force contractions, as morphological and histological changes in
demonstrated in the craniocervical flexors.9 the upper trapezius muscle in people with
Atrophy and connective tissue infiltration trapezius myalgia, including morphological
of the deep suboccipital muscles have also signs of disturbed mitochondrial function
been documented in people with chronic (ragged red and cytochrome-c oxidase
neck pain.8, 62–64 In a recent study, fatty negative fibers),67, 68 reduced adenosine
infiltrate of both deep and superficial cervi- triphosphate content,3, 69 and increased CSA
cal extensor muscles was identified in of type I muscle fibers despite a lower
people with whiplash-associated disorders.8 capillary-to-fiber-area ratio.3, 67, 68 Such
Although fatty infiltrate was generally changes may be associated with overload of
higher in all muscles investigated for the low-threshold motor units70 that may explain
patient group, it was highest in the deeper pain development in individuals performing
muscles – the rectus capitis minor/major repetitive tasks at low forces.71, 72
and multifidi and in particular at the level of The observed greater proportion of type
the third cervical vertebrae (Figure 4.3). IIC fibers and lower capillary-to-fiber area
Consistent with this observation, reduced in the muscles of people with neck pain is
cross-sectional area (CSA) has also been also indirectly in agreement with the finding
demonstrated in the deep multifidus in of greater myoelectric manifestations of
chronic whiplash65 and in the intermediate cervical muscle fatigue during sustained
semispinalis capitis measured at the C2 contraction.73, 74 People with chronic neck
level in people with chronic cervicogenic pain were shown to have a greater decrease
headache.32 However, a recent magnetic of the mean frequency of EMG signal
resonance imaging study of persons with detected from the sternocleidomastoid and
A B
Figure 4.3 Fatty tissue infiltration of the cervical multifidus: bilateral axial magnetic resonance images of the segmental cervical
multifidus muscle at the level of the third cervical vertebra in (A) a healthy control and (B) a person with whiplash-associated disorder.
(Reprinted from Elliott et al.8 with permission.)
CHAPTER
Alterations in Cervical Muscle Function in Neck Pain 47
anterior scalene muscles during sustained limited and to some degree speculative.
isometric contractions.74 Moreover people That is, it is often difficult to differentiate
with chronic neck pain demonstrate a the potential physiological mechanisms
greater decrease of upper trapezius muscle which may contribute to a specific change
fiber conduction velocity during repetitive in cervical neuromuscular function.
shoulder elevation75 (Figure 4.4). Furthermore, given the spectrum of neck
In view of the observation that pain may pain disorders it would be naive to consider
result in motor control and peripheral that stimulation of peripheral nociceptors is
modifications of the cervical muscles, it is solely responsible for all the neuromuscular
necessary to consider the possible changes that have been observed in patients.
mechanisms for this effect. Rather, it is necessary to consider the inter-
action between biological, psychological, and
social elements of the pain experience and
Mechanisms underlying the effect that each factor may have on
neuromuscular adaptations neuromuscular function of the cervical spine.
in neck pain It is beyond the scope of this chapter to
address all aspects and therefore readers are
Despite our expanding knowledge of referred to Chapter 7 for a discussion of the
changes in muscle function in people with psychosocial aspects of neck pain disorders.
neck pain, interpretations of the mechanisms Rather, this section will consider the direct
underlying these observations have been effects that pain has on muscle function.
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Figure 4.4 Subjective and objective measures of muscle fatigue during repetitive upper-limb elevation. (A) Area of fatigue reported
by control subjects (left) and neck pain patients (right) following performance of a repetitive upper-limb task performed for up to
5 minutes. Note the more widespread area of fatigue for the neck pain patient group. (B) Mean and standard error of the upper
trapezius muscle fiber conduction velocity (CV) calculated across the duration of the repetitive upper-limb task. Note the higher initial
values and greater decrease of CV estimates across the duration of the task for the patient group. (Reprinted from Falla and
Farina75 with permission.)
48 Whiplash, Headache, and Neck Pain
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Figure 4.5 Pain-induced reorganization of cervical muscle activity during isometric contraction: representative force and
electromyogram (EMG) data are presented from one subject performing a linearly increasing cervical flexion force contraction from
0 to 60% of the maximum voluntary contraction. Data are presented before (baseline) and during (pain) hypertonic saline-induced
sternocleidomastoid muscle pain. A, force; B, sternocleidomastoid EMG ipsilateral to the injection; C, sternocleidomastoid EMG
contralateral to the injection; D, splenius capitis EMG ipsilateral to the injection; E, splenius capitis contralateral to the injection. Note the
reduction in both sternocleidomastoid and splenius capitis EMG amplitude following sternocleidomastoid muscle pain. (Reprinted from
Falla et al.78 with permission.)
strategies78 rather than simply a change in in muscle activity are not just simply a
motor neuron excitability. Moreover, it has change in excitability or delayed
been observed that experimental excitation transmission of the motor command. As
of cervical nociceptors results in bilateral described previously, when people move
inhibition of the sternocleidomastoid muscle an arm rapidly, the onset of activation of
during cervical flexion, whereas during the deep cervical flexor muscles is
cervical extension, the agonist (splenius independent of the direction of the arm
capitis) demonstrated a unilateral inhibition.78 movement.6 If the delayed response
This finding further supports inhibitory observed during neck pain was a result of a
effects at the cortical level in response to change in excitability, it may be predicted
nociceptive input.86 that the response would remain consistent
In clinical neck pain conditions, there are between movement directions, although
also findings which suggest that alterations delayed when people have pain. However,
50 Whiplash, Headache, and Neck Pain
this is not the case and rather the direction- example, larger changes in upper trapezius
specific response observed in neck pain muscle fiber conduction velocity observed
suggests that there is a change in motor in neck pain patients during repetitive
planning. Consistent with this hypothesis, shoulder elevation75 cannot be reproduced
studies have reported that experimental in healthy subjects by experimental
pain changes the activity of regions of the stimulation of the nociceptors.83 Similarly,
brain involved in movement planning and larger myoelectric manifestations of fatigue
performance.87 observed in neck pain patients during
Modified cervical afferent input may also sustained cervical contractions74 cannot be
affect control of movement. Several studies reproduced in healthy subjects by
have reported decreased proprioceptive experimental neck pain.98 Thus, greater fatigue
acuity,88–90 disturbances of eye movement of the cervical muscles, which has been
control91, 92 and balance93–95 in people with observed in people with neck pain,74 is more
neck pain disorders which may reflect likely to reflect a chronic adaptation to pain,
abnormal input from cervical afferents i.e., changes in muscle composition.60, 67, 68 It
(Chapter 5). It has also been proposed that has also been proposed that vasoconstriction
neck muscle fatigue may affect mechanisms due to increased sympathetic outflow may
of postural control by producing abnormal explain the observed changes in muscle
sensory input to the central nervous system microcirculation in people with trapezius
and a lasting sense of instability.96 More- myalgia.97 In turn, an altered metabolite
over, psychological stress and anxiety with concentration in the intercellular muscle
consequent enhancement in sympathetic interstitium may activate chemosensitive
drive have the potential to affect the group III and IV muscle afferents that are
contractility of muscle fibers and to modulate known to exert complex reflex actions on
the proprioceptive information arising from spinal neurons, thus leading to altered motor
the muscle spindle receptors, thus affecting control strategies.97
motor control of the cervical muscles.97 Although fatty infiltration of the neck
This leads us to explore the mechanisms muscles may be the consequence of either
underlying changes in the peripheral a minor nerve injury or irritated and
properties of the cervical muscles and the subsequently demyelinated nerve tissue
link between muscular and neural changes resulting from an acute inflammatory
in people with neck pain. process,99 it may also be perpetuated by a
change in motor strategy. The observation
that connective tissue infiltration of the
Possible mechanisms underlying cervical extensor muscles is widespread and
not isolated suggests that the degeneration
changes in the peripheral
may be a consequence of generalized disuse.8
properties of cervical muscles It has been argued that atrophic changes in
In addition to the controversial cause– muscle are not uniform and are more likely
effect relationship between pain and to affect slow-twitch muscle fibers.100, 101 For
neuromuscular changes, the association example, rapid atrophy of type I fibers has
between motor control changes and been observed following injury to the knee100
modification of the peripheral properties of and painful stimulation of the sural nerve
the cervical muscles is also not fully results in selective inhibition of type I muscle
understood. Some data suggest that pain by fibers.102 Consistent with this hypothesis,
itself does not explain all electrophysiological greatest changes in people with neck pain
observations in patients with neck pain. For were identified for the deeper multifidus
CHAPTER
Alterations in Cervical Muscle Function in Neck Pain 51
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Figure 4.6 Interrelationships between pain, altered control strategies, and peripheral changes of the cervical muscles. (Reprinted from
Falla and Farina103 with permission.)
52 Whiplash, Headache, and Neck Pain
Control Patient
160
140
Normalized values
120 ARV
Force
100
CV
80 MNF
60
40
0 2 4 6 8 10 12 14 16 18 20 0 2 4 6 8 10 12 14 16 18 20
Time (s) Time (s)
B
50% 25% 10%
1.2
1.0 * * * * * * * * * * * *
change (Hz/s)
0.8
MNF rate of
0.6
0.4
0.2
0
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(L) SM (R) SM (L) AS (R) AS (L) SM (R) SM (L) AS (R) AS (L) SM (R) SM (L) AS (R) AS
Figure 4.7 Greater cervical muscle fatigability is reduced following specific exercise intervention. (A) Example of fatigue plots obtained
from the sternocleidomastoid muscle of a control subject and a neck pain patient contracting at 50% of maximum force. The data
represent the electromyogram (EMG) average rectified value (ARV), conduction velocity (CV), and mean frequency (MNF) normalized
with respect to the intercept of the regression line. Greater fatigue of the sternocleidomastoid muscle is evident for the neck pain patient,
as characterized by the faster rate of change of the MNF over time. (Reprinted from Falla et al.13 with permission) (B) Change in muscle
fatigue following exercise intervention: data (mean and sd) are shown for the change (pre- to postintervention) in MNF rate of change for
the left (L) and right (R) sternocleidomastoid (SM) and anterior scalene (AS) muscles contracting at 50%, 25%, and 10% of the maximum
voluntary contraction. Patients with chronic neck pain were randomized into two groups: endurance and strength training of the cervical
flexors or low-load craniocervical flexion retraining. Following 6 weeks of exercise intervention, a reduction in cervical muscle fatigue was
identified only for the patients who participated in the strength and endurance training program. *P < 0.05 between groups. (Reprinted
from Falla et al.74 with permission.)
towards the patient to ensure that this currently in remission of symptoms at the
criterion can be met. Other therapeutics time of testing.74 Furthermore, changes in
which assist in resolving pain will also play cervical muscle activation have been shown
an important role in the management of to persist in people who have had a whiplash
motor control dysfunction. injury, even if full recovery of symptoms is
reported.109, 110 Similar findings of continuous
muscle inhibition have been reported for
Rehabilitation for prevention
the multifidus muscle in low-back pain
of recurrence patients111 and the quadriceps muscle
The observed changes in motor control of following knee surgery112 despite recovery
the cervical spine in people with neck pain of symptoms and return to normal activity.
have often been detected in patients who are Although not confirmed, ongoing changes
54 Whiplash, Headache, and Neck Pain
in muscle function may explain the high has been documented in people with
recurrence rate of neck pain symptoms.113 neck pain. These include both modification
Moreover, actual pain may not necessarily of cervical motor control as well as
have to be present for motor control changes peripheral modifications, including atrophy
to be existent. Factors such as fear of of specific muscle fibers and changes in
pain may have similar effects and may muscle microcirculation. Our progressive
explain motor control changes in patients understanding of changes in cervical muscle
with musculoskeletal pain when they are function in the presence of neck pain has
in remission.50 Taken together, these directed rehabilitation programs to include
observations further emphasize the need more specific therapeutic exercise regimes as
for early and effective rehabilitation of a component of a multimodal intervention.
altered cervical muscle function. Moreover, clinical trials have demonstrated
that exercise programs should be tailored
Conclusion towards the impairments and thus based on a
detailed and specific assessment to detect
Pain induces an immediate change in cervical these changes. An evidence-based detailed
muscle function. Accordingly, a complex clinical assessment and rehabilitation approach
array of cervical neuromuscular adaptations are provided in Chapters 12 and 14.
References
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