Unravelling the complexity of muscle impairment ... - Neck Pain Relief
Unravelling the complexity of muscle impairment ... - Neck Pain Relief
Unravelling the complexity of muscle impairment ... - Neck Pain Relief
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Abstract<br />
Manual Therapy 9 (2004) 125–133<br />
Masterclass<br />
<strong>Unravelling</strong> <strong>the</strong> <strong>complexity</strong> <strong>of</strong><strong>muscle</strong> <strong>impairment</strong> in<br />
chronic neck pain<br />
D. Falla*<br />
Division <strong>of</strong> Physio<strong>the</strong>rapy, The University <strong>of</strong> Queensland, Brisbane QLD 4072, Australia<br />
Received 4 May 2004; accepted 8 May 2004<br />
www.elsevier.com/locate/math<br />
Exercise interventions are deemed essential for <strong>the</strong> effective management <strong>of</strong> patients with neck pain. However, <strong>the</strong>re has been a<br />
lack <strong>of</strong>consensus on optimal exercise prescription, which has resulted from a paucity <strong>of</strong>studies to quantify <strong>the</strong> precise nature <strong>of</strong><br />
<strong>muscle</strong> <strong>impairment</strong>, in people with neck pain. This masterclass will present recent research from our laboratory, which has utilized<br />
surface electromyography to investigate cervical flexor <strong>muscle</strong> <strong>impairment</strong> in patients with chronic neck pain. This research has<br />
identified deficits in <strong>the</strong> motor control <strong>of</strong><strong>the</strong> deep and superficial cervical flexor <strong>muscle</strong>s in people with chronic neck pain,<br />
characterized by a delay in onset <strong>of</strong>neck <strong>muscle</strong> contraction associated with movement <strong>of</strong><strong>the</strong> upper limb. In addition, people with<br />
neck pain demonstrate an altered pattern <strong>of</strong><strong>muscle</strong> activation, which is characterized by reduced deep cervical flexor <strong>muscle</strong> activity<br />
during a low load cognitive task and increased activity <strong>of</strong><strong>the</strong> superficial cervical flexor <strong>muscle</strong>s during both cognitive tasks and<br />
functional activities. The results have demonstrated <strong>the</strong> complex, multifaceted nature <strong>of</strong> cervical <strong>muscle</strong> <strong>impairment</strong>, which exists in<br />
people with a history <strong>of</strong>neck pain. In turn, this has considerable implications for <strong>the</strong> rehabilitation <strong>of</strong><strong>muscle</strong> function in people with<br />
neck pain disorders.<br />
r 2004 Elsevier Ltd. All rights reserved.<br />
1. Introduction<br />
Chronic neck pain is becoming increasingly prevalent<br />
in society. Estimations indicate that 67% <strong>of</strong>individuals<br />
will suffer neck pain at some stage throughout life (Cote<br />
et al., 1998). With an increasing sedentary population,<br />
especially with reliance on computer technology in <strong>the</strong><br />
workplace, it is predicted that <strong>the</strong> prevalence rate will<br />
continue to rise. Effective management <strong>of</strong> this condition<br />
is vital, not only for <strong>the</strong> relief <strong>of</strong> symptoms but perhaps<br />
more importantly, for <strong>the</strong> prevention <strong>of</strong> recurrent<br />
episodes <strong>of</strong>cervical pain, personal su fering and lost<br />
work productivity.<br />
It is estimated that <strong>the</strong> osseoligamentous system<br />
contributes 20% to <strong>the</strong> mechanical stability <strong>of</strong><strong>the</strong><br />
cervical spine while 80% is provided by <strong>the</strong> surrounding<br />
neck musculature (Panjabi et al., 1998). The ligaments’<br />
role in stabilization occurs mainly at end <strong>of</strong>range<br />
postures (Harms-Ringdahl et al., 1986) while <strong>muscle</strong>s<br />
*Corresponding author. Tel.: +61-7-3365-4529; fax: +61-7-3365-<br />
2775.<br />
E-mail address: d.falla@shrs.uq.edu.au (D. Falla).<br />
1356-689X/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.<br />
doi:10.1016/j.math.2004.05.003<br />
ARTICLE IN PRESS<br />
supply dynamic support in activities around <strong>the</strong> neutral<br />
and mid-range postures, which are commonly adopted<br />
during functional daily tasks. In <strong>the</strong> presence <strong>of</strong> injury<br />
or pathology, <strong>the</strong> role <strong>of</strong><strong>the</strong> muscular system becomes<br />
even greater which highlights <strong>the</strong> need to address <strong>the</strong><br />
<strong>muscle</strong> system during both <strong>the</strong> assessment and rehabilitation<br />
<strong>of</strong>patients with neck pain.<br />
Exercise interventions are deemed essential for <strong>the</strong><br />
effective management <strong>of</strong> patients with neck pain. In <strong>the</strong><br />
past however, <strong>the</strong>re has been a lack <strong>of</strong>consensus on<br />
optimal exercise prescription. This results from a<br />
paucity <strong>of</strong>studies to quantify <strong>the</strong> precise nature <strong>of</strong><br />
<strong>impairment</strong> in both <strong>the</strong> deep and superficial cervical<br />
<strong>muscle</strong>s in neck pain patients.<br />
Anecdotal evidence (Janda, 1994) suggests <strong>the</strong> cervical<br />
flexor <strong>muscle</strong>s become dysfunctional in <strong>the</strong> presence <strong>of</strong><br />
neck pain. Fur<strong>the</strong>rmore, simple clinical mechanical<br />
measures have demonstrated a reduction in <strong>the</strong> strength<br />
and endurance capabilities <strong>of</strong><strong>the</strong> cervical flexor <strong>muscle</strong>s<br />
in neck pain patients (Silverman et al., 1991; Vernon<br />
et al., 1992; Watson and Trott, 1993; Barton and Hayes,<br />
1996; Placzek et al., 1999). However, such basic<br />
mechanical measures may oversimplify <strong>the</strong> deficits
126<br />
within <strong>the</strong> <strong>muscle</strong> system in people with neck pain<br />
disorders.<br />
Detection, recording and analysis <strong>of</strong>myoelectric<br />
signals with surface electromyography (EMG) provides<br />
a more sophisticated means <strong>of</strong>determining aberrant<br />
<strong>muscle</strong> function. Although EMG has been used to<br />
analyse superficial cervical <strong>muscle</strong> function in <strong>the</strong> past,<br />
such investigations are infrequent and regular inconsistencies<br />
in <strong>the</strong> applied methodology limits <strong>the</strong> interpretation<br />
<strong>of</strong>results. Moreover, <strong>the</strong> inaccessibility <strong>of</strong><strong>the</strong><br />
deep cervical flexor (DCF) <strong>muscle</strong>s has rendered <strong>the</strong> use<br />
<strong>of</strong>conventional surface EMG measures inappropriate.<br />
Recent research has refined <strong>the</strong> application <strong>of</strong>surface<br />
EMG for <strong>the</strong> assessment <strong>of</strong> <strong>the</strong> cervical flexor <strong>muscle</strong>s.<br />
This has involved optimizing <strong>the</strong> application <strong>of</strong>surface<br />
EMG for <strong>the</strong> assessment <strong>of</strong> <strong>the</strong> superficial cervical<br />
flexors (sternocleidomastoid and <strong>the</strong> scalenes) (Falla<br />
et al., 2002a, b) and secondly establishing a new EMG<br />
electrode and technique for obtaining a direct measure<br />
<strong>of</strong><strong>the</strong> DCF <strong>muscle</strong>s (Falla et al., 2003a).<br />
Upon developing <strong>the</strong> methodology we investigated<br />
cervical flexor <strong>muscle</strong> function in patients with neck pain<br />
in three main areas <strong>of</strong>EMG assessment (1) myoelectric<br />
manifestations <strong>of</strong> cervical <strong>muscle</strong> fatigue (2) analysis <strong>of</strong><br />
<strong>the</strong> cervical flexor <strong>muscle</strong> activation patterns and (3)<br />
analysis <strong>of</strong>cervical neuromotor control. This paper will<br />
(A)<br />
Normalized values w.r.t. initial values<br />
(B)<br />
160<br />
140<br />
120<br />
100<br />
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60<br />
ARTICLE IN PRESS<br />
D. Falla / Manual Therapy 9 (2004) 125–133<br />
Direction <strong>of</strong><br />
neck effort<br />
Control<br />
2 load cells,FS=250 N each<br />
Normalized values w.r.t. initial values<br />
present this recent evidence from our laboratory <strong>of</strong> <strong>the</strong><br />
<strong>complexity</strong> <strong>of</strong>cervical <strong>muscle</strong> <strong>impairment</strong> in neck pain<br />
patients and in turn will highlight <strong>the</strong> implications for<br />
rehabilitation.<br />
2. Muscle fatigability<br />
40<br />
0 2 4 6 8<br />
Time (s)<br />
10 12 14<br />
40<br />
0 2 4<br />
Numerous studies have demonstrated a reduction in<br />
<strong>the</strong> strength and endurance capacity <strong>of</strong><strong>the</strong> cervical<br />
flexor and extensor <strong>muscle</strong>s in patients with neck pain<br />
(Watson and Trott, 1993; Treleaven et al., 1994; Barton<br />
and Hayes, 1996; Placzek et al., 1999). With advances in<br />
EMG technology, more sophisticated measures have<br />
been used to quantify cervical <strong>muscle</strong> fatigability in<br />
patients with neck pain (Falla et al., 2003b, 2004e, f;<br />
Gogia and Sabbahi, 1994). In a recent study (Falla et al.,<br />
2003b) we examined fatigability <strong>of</strong> <strong>the</strong> sternocleidomastoid<br />
(SCM) and anterior scalene (AS) <strong>muscle</strong>s during<br />
sustained cervical flexion contractions at 25% and 50%<br />
<strong>of</strong><strong>the</strong> maximum voluntary contraction (MVC) in<br />
patients with chronic neck pain compared to controls.<br />
Greater myoelectric manifestations <strong>of</strong> SCM and AS<br />
<strong>muscle</strong> fatigue were identified for <strong>the</strong> neck pain patient<br />
group as indicated by a significantly greater slope <strong>of</strong><strong>the</strong><br />
mean frequency (Fig. 1). Whilst <strong>the</strong> results <strong>of</strong>our study<br />
Visual feedback display<br />
160<br />
140<br />
120<br />
100<br />
80<br />
60<br />
nMNF nARV nC V nFORCE<br />
<strong>Neck</strong> <strong>Pain</strong> Patient<br />
6 8 10 12 14<br />
Time (s)<br />
Fig. 1. (A) The subject’s head rests on a padded head support <strong>of</strong>a custom designed cervical flexion force-measuring device. An adjustable Velcro<br />
strap is fastened across <strong>the</strong> forehead acting to stabilize <strong>the</strong> head and provide resistance during cervical flexion isometric contractions. (B) Example <strong>of</strong><br />
fatigue plots obtained from <strong>the</strong> SCM <strong>muscle</strong> <strong>of</strong> a neck pain patient and control subject contracting at 50% <strong>of</strong> <strong>the</strong> MVC for <strong>the</strong> EMG variables<br />
average rectified value (ARV), conduction velocity (CV), and mean frequency (MNF). The values <strong>of</strong> each variable are normalized with respect to <strong>the</strong><br />
intercept <strong>of</strong> <strong>the</strong> regression line. Greater fatigue <strong>of</strong> <strong>the</strong> SCM <strong>muscle</strong> is evident for <strong>the</strong> neck pain patient as characterized by <strong>the</strong> faster rate <strong>of</strong> change <strong>of</strong><br />
<strong>the</strong> MNF over time. (Adapted from Fig. 2 in Falla et al., 2003b).
confirmed greater fatigability <strong>of</strong> <strong>the</strong> cervical flexors at<br />
moderate loads (50% MVC) which was identified by<br />
Gogia and Sabbahi (1994), our results also established<br />
greater cervical flexor <strong>muscle</strong> fatigability during low<br />
load sustained contractions (25% MVC) in <strong>the</strong> patient<br />
group which reflects <strong>the</strong> clinical observation <strong>of</strong>reduced<br />
endurance in <strong>the</strong> cervical flexors in neck pain patients<br />
(Treleaven et al., 1994; Watson and Trott, 1993; Barton<br />
and Hayes, 1996; Placzek et al., 1999). Fur<strong>the</strong>rmore, an<br />
increase <strong>of</strong><strong>the</strong> mean frequency at <strong>the</strong> beginning <strong>of</strong><strong>the</strong><br />
contraction was observed for both <strong>muscle</strong>s in <strong>the</strong> neck<br />
pain group. This could be attributed to modification <strong>of</strong><br />
<strong>the</strong> recruited motor unit pool in which <strong>the</strong> number <strong>of</strong><br />
type II fibres is increased with respect to <strong>the</strong> type I fibres.<br />
These findings were in accordance with results <strong>of</strong><strong>muscle</strong><br />
biopsy studies <strong>of</strong>subjects with neck pain undergoing<br />
spinal surgery, which established an increase in <strong>the</strong><br />
number <strong>of</strong>type-IIC transitional fibres in <strong>the</strong> neck flexor<br />
<strong>muscle</strong>s resulting from transformations <strong>of</strong> slow-twitch<br />
oxidative type-I fibres to fast-twitch glycolytic type-IIB<br />
fibres (Uhlig et al., 1995).<br />
Subsequent to <strong>the</strong>se results, <strong>the</strong> specificity <strong>of</strong>this<br />
aberrant <strong>muscle</strong> function was analysed (Falla et al.,<br />
2004e). In examining for differences in <strong>the</strong> fatigability <strong>of</strong><br />
SCM and AS <strong>muscle</strong>s between <strong>the</strong> painful and nonpainful<br />
sides in patients with chronic unilateral neck<br />
pain, results revealed greater estimates <strong>of</strong><strong>the</strong> initial<br />
value and slope <strong>of</strong> <strong>the</strong> mean frequency for both <strong>the</strong> SCM<br />
and AS <strong>muscle</strong>s ipsilateral to <strong>the</strong> side <strong>of</strong>pain at 25%<br />
and 50% <strong>of</strong>MVC. These results indicate <strong>the</strong> need to<br />
address fatigability <strong>of</strong> <strong>the</strong> cervical flexor <strong>muscle</strong>s when<br />
prescribing <strong>the</strong>rapeutic exercise for neck pain patients.<br />
The outcomes advocate <strong>the</strong> need for specificity and<br />
perhaps a unilateral bias to <strong>the</strong>rapeutic exercise in <strong>the</strong><br />
management <strong>of</strong>patients with unilateral neck pain to<br />
attain optimal <strong>muscle</strong> rehabilitation. Ofinterest, <strong>the</strong><br />
duration <strong>of</strong>neck pain does not appear to correlate with<br />
<strong>the</strong> extent <strong>of</strong>SCM and AS <strong>muscle</strong> fatigability in patients<br />
with chronic neck pain. This finding would suggest that<br />
<strong>the</strong> greater fatigability <strong>of</strong> <strong>the</strong> cervical flexor <strong>muscle</strong>s,<br />
which has been identified in patients with neck pain,<br />
occurs early with <strong>the</strong> onset <strong>of</strong>neck pain and does not<br />
worsen with time (Falla et al., 2004f).<br />
3. Muscle activation patterns during cognitive tasks<br />
Whilst direct evidence <strong>of</strong>deep cervical extensor<br />
<strong>muscle</strong> dysfunction has been identified in neck pain<br />
patients (Hallgren et al., 1994; McPartland et al., 1997),<br />
until recently, <strong>the</strong>re was no succinct evidence that<br />
described <strong>impairment</strong> in <strong>the</strong> DCF <strong>muscle</strong>s. The DCF<br />
<strong>muscle</strong>s, including <strong>the</strong> longus colli, longus capitis, rectus<br />
capitis anterior and rectus capitis lateralis, are histologically<br />
and morphologically designed to provide support<br />
to <strong>the</strong> cervical lordosis and <strong>the</strong> cervical joints (Winters<br />
ARTICLE IN PRESS<br />
D. Falla / Manual Therapy 9 (2004) 125–133 127<br />
and Peles, 1990; Mayoux-Benhamou et al., 1994; Conley<br />
et al., 1995; Vasavada et al., 1998; Boyd Clark et al.,<br />
2001, 2002). Accordingly, our research has been<br />
orientated towards <strong>the</strong> identification and quantification<br />
<strong>of</strong>deficits in <strong>the</strong> DCF <strong>muscle</strong>s in patients with neck pain<br />
disorders.<br />
Our interest commenced with <strong>the</strong> development <strong>of</strong><strong>the</strong><br />
cranio-cervical flexion (C-CF) test (Jull et al., 1999; Jull,<br />
2000), which is a low load task, based on <strong>the</strong> anatomical<br />
action <strong>of</strong><strong>the</strong> deep longus capitis and colli <strong>muscle</strong>s. The<br />
C-CF test was considered to provide an indirect measure<br />
<strong>of</strong>DCF <strong>muscle</strong> activation and endurance capacity,<br />
which could be utilized in a clinical environment. The<br />
test is performed in crook lying, and requires <strong>the</strong> person<br />
to perform a head nod action (cranio-cervical flexion) in<br />
five incremental stages <strong>of</strong>increasing range and hold each<br />
position for 5–10 s. Performance is guided by feedback<br />
from a pressure sensor, which is positioned suboccipitally<br />
to monitor <strong>the</strong> flattening <strong>of</strong><strong>the</strong> cervical<br />
lordosis, which occurs with <strong>the</strong> contraction <strong>of</strong>longus<br />
colli (Mayoux-Benhamou et al., 1994, 1997).<br />
Earlier clinical research demonstrated significantly<br />
inferior performance on <strong>the</strong> C-CF test in patients with<br />
idiopathic neck pain and with neck pain after a whiplash<br />
injury (Jull et al., 1999; Jull, 2000). In general, patients<br />
demonstrated a reduced ability to reach and maintain<br />
<strong>the</strong> targets <strong>of</strong>pressure in <strong>the</strong> cu funder <strong>the</strong> cervical<br />
spine. Fur<strong>the</strong>rmore, surface EMG recordings <strong>of</strong> <strong>the</strong><br />
superficial cervical flexor (sternocleidomastoid) indicated<br />
that performance on <strong>the</strong> test was associated with<br />
significantly higher EMG amplitude <strong>of</strong>this <strong>muscle</strong><br />
compared with controls (Jull, 2000; Jull et al., 2004b).<br />
Based on this research it was hypo<strong>the</strong>sized that impaired<br />
performance on <strong>the</strong> C-CF test (1) reflected a deficit in<br />
motor control <strong>of</strong>C-CF in patients with neck pain (2)<br />
reflected poor activation <strong>of</strong>DCF <strong>muscle</strong>s and (3)<br />
reflected poor <strong>muscle</strong> support <strong>of</strong>cervical joints (Jull,<br />
2000). The difficulty in substantiating <strong>the</strong>se hypo<strong>the</strong>ses<br />
was related to <strong>the</strong> difficulty in obtaining a direct<br />
recording <strong>of</strong><strong>the</strong> DCF <strong>muscle</strong>s due to <strong>the</strong>ir depth and<br />
close proximity to nearby structures such as <strong>the</strong><br />
lymphatic system, <strong>the</strong> sympa<strong>the</strong>tic chain, vagus nerve<br />
and <strong>the</strong> carotid artery. However, our recent research<br />
(Falla et al., 2003a) led to <strong>the</strong> development <strong>of</strong>an<br />
electrode capable <strong>of</strong>recording DCF <strong>muscle</strong> activity<br />
(Fig. 2) without <strong>the</strong> need for fine wire EMG and thus<br />
provided <strong>the</strong> opportunity to corroborate or refute <strong>the</strong>se<br />
hypo<strong>the</strong>ses.<br />
Utilizing this new EMG technique, we investigated<br />
activation <strong>of</strong><strong>the</strong> DCF <strong>muscle</strong>s in patients with and<br />
without chronic neck pain during performance <strong>of</strong> <strong>the</strong> C-<br />
CF test (Falla et al., 2004c). The results demonstrated<br />
reduced activation <strong>of</strong><strong>the</strong> DCF <strong>muscle</strong>s for <strong>the</strong> neck pain<br />
patient group across all stages <strong>of</strong><strong>the</strong> C-CF test with <strong>the</strong><br />
difference becoming statistically significant at <strong>the</strong> higher<br />
levels <strong>of</strong><strong>the</strong> test (representing increasingly inner range
128<br />
positions <strong>of</strong>C-CF (Fig. 3). Fur<strong>the</strong>rmore, <strong>the</strong> neck pain<br />
patient group demonstrated reduced C-CF range <strong>of</strong><br />
motion across all stages <strong>of</strong><strong>the</strong> C-CF test (Fig. 3). This<br />
finding suggests that <strong>the</strong> pressure increase in <strong>the</strong> cuff<br />
Connection to<br />
suction tubing<br />
(A)<br />
Nasopharynx<br />
(B)<br />
Dens<br />
Oropharynx<br />
1c m<br />
Electrode<br />
contacts<br />
Suction<br />
portal<br />
Nasal septum<br />
ARTICLE IN PRESS<br />
Nasopharyngeal Electrode<br />
Uvula<br />
Deep Cervical Flexors<br />
Tongue<br />
Fig. 2. (A) Electrode for <strong>the</strong> detection <strong>of</strong> DCF <strong>muscle</strong> activity. (B) A<br />
nasopharyngeal application is used to suction surface electrodes over<br />
<strong>the</strong> posterior oropharyngeal wall. The DCF <strong>muscle</strong>s lie directly<br />
posterior to <strong>the</strong> oropharyngeal wall, allowing myoelectric signals to be<br />
detected from <strong>the</strong>se <strong>muscle</strong>s (adapted from Figs. 1 and 2 in Falla et al.,<br />
2003a).<br />
(A)<br />
DCF normalised RMS values<br />
(B)<br />
140<br />
120<br />
100<br />
80<br />
60<br />
40<br />
20<br />
Cranio-cervical<br />
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Stage <strong>of</strong> C-CFT (mmHg)<br />
D. Falla / Manual Therapy 9 (2004) 125–133<br />
*<br />
Visual feedback display<br />
Pressure Bi<strong>of</strong>eedback Unit<br />
*<br />
% Full C-CF ROM<br />
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20<br />
0<br />
under <strong>the</strong> cervical spine <strong>of</strong>neck pain patients was<br />
induced by a different movement strategy such as head/<br />
neck retraction, which is commonly observed clinically.<br />
Based on <strong>the</strong> results <strong>of</strong>this study it was concluded that<br />
neck pain patients have a disturbance in <strong>the</strong> neck flexor<br />
synergy, where <strong>impairment</strong> in <strong>the</strong> deep <strong>muscle</strong>s,<br />
important for segmental control and support, appears<br />
to be compensated for by increased activity in <strong>the</strong><br />
superficial <strong>muscle</strong>s (SCM and AS).<br />
4. Neuromuscular efficiency<br />
Increased EMG activity <strong>of</strong><strong>the</strong> superficial cervical<br />
musculature which has been identified in people with<br />
neck pain during performance <strong>of</strong> <strong>the</strong> C-CF test (Jull,<br />
2000; Jull et al., 2004b), could be considered an<br />
inefficient neuromuscular activation pattern. This<br />
concept was explored recently by investigating <strong>the</strong><br />
neuromuscular efficiency (NME) <strong>of</strong> <strong>the</strong> SCM and AS<br />
<strong>muscle</strong>s, defined as <strong>the</strong> quotient <strong>of</strong>force and <strong>the</strong><br />
integrated EMG (van der Hoeven et al., 1993), during<br />
cervical flexion contractions at 25% and 50% <strong>of</strong>MVC<br />
in patients with and without chronic neck pain (Falla<br />
et al., 2004b). The results <strong>of</strong>our study confirmed<br />
less NME for <strong>the</strong> SCM and AS <strong>muscle</strong>s contracting<br />
at 25% MVC in <strong>the</strong> neck pain patient group. Reduced<br />
NME indicates that <strong>the</strong> neck pain patients required<br />
*<br />
*<br />
22 24 26 28 30<br />
Stage <strong>of</strong> C-CFT (mmHg)<br />
*<br />
*<br />
*<br />
Control subjects<br />
<strong>Neck</strong> pain patients<br />
Fig. 3. (A) Subjects were positioned supine with <strong>the</strong> Pressure Bi<strong>of</strong>eedback Unit placed sub-occipitally behind <strong>the</strong> neck to detect increases in pressure<br />
with <strong>the</strong> gentle nodding action <strong>of</strong>C-CF. Subjects received visual feedback <strong>of</strong>pressure level. (B) Normalized root mean square (RMS) values (mean<br />
and standard deviation) for <strong>the</strong> DCF <strong>muscle</strong>s and percentage <strong>of</strong> full C-CF range <strong>of</strong> motion (ROM) for each stage <strong>of</strong> <strong>the</strong> C-CF test (C-CFT).<br />
Indicates significant difference between control subjects and neck pain patients (Po0:05) (adapted from Figs. 1 and 2 in Falla et al., 2004c).
greater muscular electrical activity to produce an<br />
equivalent amount <strong>of</strong>force as compared to <strong>the</strong> control<br />
subjects, or conversely, with a comparable amount <strong>of</strong><br />
electrical activity, neck pain patients would produce a<br />
lower force output (Falla et al., 2004b). The greater<br />
SCM and AS EMG activity recorded for <strong>the</strong> neck pain<br />
group could <strong>the</strong>oretically be attributed to (1) greater<br />
excitability <strong>of</strong><strong>the</strong> motoneuronal pool, (2) modification<br />
<strong>of</strong>neural activation patterns accommodating for weakness<br />
or inhibition <strong>of</strong>ano<strong>the</strong>r <strong>muscle</strong>, or (3) a combination<br />
<strong>of</strong><strong>the</strong>se mechanisms.<br />
5. Muscle activation during functional tasks<br />
Until now, <strong>the</strong> evidence <strong>of</strong>cervical <strong>muscle</strong> <strong>impairment</strong><br />
presented within this manuscript corresponds to altered<br />
<strong>muscle</strong> function identified during prescribed motor<br />
tasks. In particular, research has demonstrated <strong>the</strong><br />
presence <strong>of</strong>overactivity or neuromuscular inefficiency<br />
<strong>of</strong><strong>the</strong> superficial cervical <strong>muscle</strong>s under conditions <strong>of</strong><br />
low biomechanical load (Jull, 2000; Falla et al., 2004b,<br />
c). However, this altered pattern <strong>of</strong>neuromuscular<br />
activation has been detected during non-functional<br />
tasks. Therefore, extrapolation <strong>of</strong> <strong>the</strong>se findings to<br />
function must be done so with caution.<br />
1.0<br />
0.8<br />
0.6<br />
0.4<br />
0.2<br />
1.0<br />
0.8<br />
0.6<br />
0.4<br />
0.2<br />
*<br />
* *<br />
10s<br />
*<br />
* *<br />
Left SCM<br />
Left AS<br />
60s 120s<br />
Condition<br />
ARTICLE IN PRESS<br />
D. Falla / Manual Therapy 9 (2004) 125–133 129<br />
*<br />
* *<br />
*<br />
* *<br />
* * *<br />
* * * * *<br />
post<br />
Control Idiopathic WAD<br />
In order to assess whe<strong>the</strong>r <strong>the</strong> presence <strong>of</strong>increased<br />
EMG activity <strong>of</strong><strong>the</strong> superficial cervical flexor <strong>muscle</strong>s<br />
was present during functional activities in people with<br />
neck pain, we investigated activity <strong>of</strong><strong>the</strong> SCM and AS<br />
<strong>muscle</strong>s during a low load, functional upper limb task<br />
(Falla et al., 2004a). Subjects were asked to perform a<br />
repetitive unilateral task, which involved marking three<br />
targets, positioned on a desk in front <strong>of</strong> <strong>the</strong>m, using<br />
<strong>the</strong>ir right hand. Their left forearm rested motionless on<br />
<strong>the</strong> desk in front <strong>of</strong> <strong>the</strong>m. Previous research using this<br />
task has demonstrated higher co-activation <strong>of</strong><strong>the</strong> upper<br />
trapezius <strong>muscle</strong> in neck pain patients compared to<br />
controls during performance <strong>of</strong> <strong>the</strong> task and a decreased<br />
ability to relax <strong>the</strong> upper trapezius <strong>muscle</strong> on completion<br />
<strong>of</strong><strong>the</strong> task (Nederhand et al., 2000).<br />
As demonstrated in Fig. 4, <strong>the</strong> altered pattern <strong>of</strong><br />
<strong>muscle</strong> activation identified for both idiopathic neck<br />
pain and whiplash patients was characterized by<br />
increased EMG amplitude for <strong>the</strong> AS and SCM <strong>muscle</strong>s<br />
bilaterally throughout performance <strong>of</strong> <strong>the</strong> functional<br />
activity. Fur<strong>the</strong>rmore, neck pain patients demonstrated<br />
a decreased ability to relax <strong>the</strong> SCM and AS <strong>muscle</strong>s on<br />
completion <strong>of</strong><strong>the</strong> task. It was suggested that <strong>the</strong> altered<br />
pattern <strong>of</strong><strong>muscle</strong> activation identified for <strong>the</strong> neck<br />
pain groups represents an altered motor strategy to<br />
minimize activation <strong>of</strong>painful <strong>muscle</strong>s or compensate<br />
1.0<br />
0.8<br />
0.6<br />
0.4<br />
0.2<br />
1.0<br />
0.8<br />
0.6<br />
0.4<br />
0.2<br />
*<br />
* *<br />
*<br />
*<br />
10s<br />
*<br />
* *<br />
60s<br />
Right SCM<br />
*<br />
*<br />
Right AS<br />
Condition<br />
Fig. 4. Boxplots representing (25th quartile, mean, 75th quartile and 95% confidence intervals) normalized root mean square (RMS) values for <strong>the</strong><br />
left (L) and right (R) SCM and AS <strong>muscle</strong>s in patients with whiplash associated disorder (WAD), idiopathic neck pain and control subjects. Values<br />
are given for conditions 10, 60 and 120 s into <strong>the</strong> performance <strong>of</strong> a repetitive upper limb task and 10 s after completion <strong>of</strong> <strong>the</strong> repetitive upper limb<br />
task (post). Indicate significant differences between groups calculated from <strong>the</strong> logarithm values <strong>of</strong> <strong>the</strong> data set. Statistical significance was defined<br />
as <strong>the</strong> mean value for one group falling outside <strong>the</strong> 95% confidence interval <strong>of</strong> <strong>the</strong> comparison group. (Adapted from Fig. 1 in Falla et al., 2004a).<br />
*<br />
* *<br />
*<br />
*<br />
120s<br />
*<br />
*<br />
*<br />
*<br />
post
130<br />
Relative latencies (ms)<br />
Deltoid<br />
onset<br />
Relative latencies (ms)<br />
Deltoid<br />
onset<br />
for inhibited <strong>muscle</strong>s and might represent a functional<br />
correlate <strong>of</strong>performance on <strong>the</strong> C-CF test (Falla et al.,<br />
2004a).<br />
6. Muscle activation during postural perturbations<br />
250<br />
200<br />
150<br />
100<br />
50<br />
0<br />
250<br />
200<br />
150<br />
100<br />
50<br />
0<br />
Flexion<br />
DCF (R) SCM (L) SCM (R) AS (L) AS<br />
Evidence was starting to reveal specific deficits within<br />
<strong>the</strong> cervical flexor <strong>muscle</strong>s in patients with neck pain.<br />
This was identified during performance <strong>of</strong> prescribed<br />
motor tasks and during functional activities. The next<br />
stage <strong>of</strong>our research was to identify whe<strong>the</strong>r <strong>the</strong><br />
automatic function <strong>of</strong> <strong>the</strong> cervical <strong>muscle</strong>s was impaired<br />
in people with neck pain.<br />
We know from research in healthy individuals that<br />
during performance <strong>of</strong> rapid arm movements which<br />
induce a postural perturbation, <strong>the</strong> cervical <strong>muscle</strong>s are<br />
co-activated within 50 ms <strong>of</strong><strong>the</strong> onset <strong>of</strong>deltoid activity.<br />
This indicates that this response is too fast to be<br />
mediated by even <strong>the</strong> fastest reflexes. Instead <strong>the</strong>se<br />
responses are considered to be preplanned by <strong>the</strong><br />
nervous system and are termed ‘‘feed-forward’’ adjustments<br />
(Gurfinkel et al., 1988; van der Fits et al., 1998;<br />
Falla et al., 2004g).<br />
In reference to <strong>the</strong> lumbar spine model, a significant<br />
delay has been identified for <strong>the</strong> transversus abdominis<br />
<strong>muscle</strong> in patients with low back pain during rapid arm<br />
movements (Hodges and Richardson, 1996). Utilizing<br />
<strong>the</strong> same experimental model we aimed to determine<br />
whe<strong>the</strong>r a deficit in <strong>the</strong> timing <strong>of</strong><strong>the</strong> cervical <strong>muscle</strong>s<br />
would be present in people with chronic neck pain. The<br />
results <strong>of</strong>our study confirmed <strong>the</strong> hypo<strong>the</strong>sis <strong>of</strong>delayed<br />
onset <strong>of</strong><strong>the</strong> DCF and <strong>the</strong> SCM and AS <strong>muscle</strong>s in<br />
*<br />
DCF<br />
Extension<br />
(R) SCM (L) SCM (R) AS (L) AS<br />
ARTICLE IN PRESS<br />
D. Falla / Manual Therapy 9 (2004) 125–133<br />
* *<br />
* *<br />
(A) (B)<br />
AD EMG<br />
DCF EMG<br />
(L) AS EMG<br />
(R) AS EMG<br />
(L) SCM EMG<br />
(R) SCM EMG<br />
Control <strong>Neck</strong> <strong>Pain</strong><br />
Fig. 5. (A) Group data for neck flexor <strong>muscle</strong> EMG onsets during unilateral arm movements. Data are shown for <strong>the</strong> control (white bars) and neck<br />
pain subjects (black bars). Mean and standard error <strong>of</strong> <strong>the</strong> relative latencies (ms) for <strong>the</strong> left (L) and right (R) SCM, AS and DCF <strong>muscle</strong>s during<br />
unilateral upper limb flexion and extension. Indicates significant difference Po0:05: (B) Representative electromyographic activity with rapid arm<br />
movements. Raw EMG data are shown for <strong>the</strong> anterior deltoid (AD), DCF, SCM and <strong>the</strong> AS <strong>muscle</strong>s for a control and chronic neck pain subject<br />
during rapid upper limb flexion. Note <strong>the</strong> delayed activation <strong>of</strong> <strong>the</strong> neck <strong>muscle</strong>s for <strong>the</strong> neck pain patient. (Adapted from Figs. 1 and 2 in Falla et al.,<br />
2004d).<br />
people with a history <strong>of</strong>neck pain compared to control<br />
subjects (Fig. 5) (Falla et al., 2004d).<br />
Although each <strong>of</strong><strong>the</strong> neck <strong>muscle</strong>s demonstrated<br />
some difference in onset time between groups, <strong>the</strong> DCF<br />
demonstrated <strong>the</strong> most significant deviation during<br />
rapid shoulder flexion. The relative latency <strong>of</strong><strong>the</strong><br />
DCF contraction exceeded <strong>the</strong> criteria for feed-forward<br />
contraction during movements in both directions in <strong>the</strong><br />
neck pain group, which indicates a significant deficit in<br />
<strong>the</strong> automatic feed-forward control <strong>of</strong> <strong>the</strong> cervical spine.<br />
Considering <strong>the</strong> deep cervical <strong>muscle</strong>s, longus colli and<br />
longus capitis, are fundamentally important for <strong>the</strong><br />
provision <strong>of</strong>support for <strong>the</strong> cervical lordosis and <strong>the</strong><br />
cervical joints (Mayoux-Benhamou et al., 1994; Conley<br />
et al., 1995; Vasavada et al., 1998), it was concluded that<br />
a change in <strong>the</strong> feed-forward response might leave <strong>the</strong><br />
cervical spine vulnerable to strain (Falla et al., 2004d).<br />
7. Implications for rehabilitation<br />
100 ms<br />
In summary, contemporary research has demonstrated<br />
<strong>impairment</strong> in <strong>the</strong> deep cervical <strong>muscle</strong>s, which<br />
are considered to be functionally important for joint<br />
support and control (Jull, 2000; Falla et al., 2004c, d),<br />
deficits in <strong>muscle</strong> co-ordination which could result in<br />
poor support and potential overload on cervical<br />
structures (Jull, 2000; Falla et al., 2004a), insufficiency<br />
in <strong>the</strong> pre-programmed activation <strong>of</strong>cervical <strong>muscle</strong>s<br />
(Falla et al., 2004d), inefficient neuromuscular activation<br />
(Falla et al., 2004b), and greater fatigability <strong>of</strong><br />
superficial cervical <strong>muscle</strong>s in people with chronic neck<br />
pain (Gogia and Sabbahi, 1994; Falla et al., 2003b,
2004e). In consideration <strong>of</strong><strong>the</strong> evidence, it would seem<br />
apparent that <strong>the</strong>re is a need for specificity when<br />
prescribing <strong>the</strong>rapeutic exercise in <strong>the</strong> management <strong>of</strong><br />
people with neck pain.<br />
There is some evidence to indicate that deficits in <strong>the</strong><br />
motor system occur early in <strong>the</strong> history <strong>of</strong>onset <strong>of</strong>neck<br />
pain (Sterling et al., 2003) and does not resolve<br />
automatically with lessening or resolution <strong>of</strong>symptoms<br />
(Jull et al., 2002; Sterling et al., 2003). This would<br />
suggest that <strong>the</strong>rapeutic exercise forms an essential<br />
component <strong>of</strong><strong>the</strong> rehabilitation <strong>of</strong>patients with neck<br />
pain, as a reduction <strong>of</strong>pain alone would seem<br />
insufficient to fully restore <strong>muscle</strong> function. Moreover,<br />
it emphasizes <strong>the</strong> importance <strong>of</strong>early rehabilitation <strong>of</strong><br />
<strong>muscle</strong> function in people with neck pain disorders.<br />
When developing exercises for treatment, it is<br />
necessary to have an understanding <strong>of</strong>abnormalities in<br />
<strong>the</strong> muscular system associated with painful dysfunctional<br />
joints. The results <strong>of</strong>recent research have<br />
significantly advanced our understanding <strong>of</strong><strong>the</strong> <strong>impairment</strong><br />
in <strong>the</strong> deep and superficial cervical flexor <strong>muscle</strong>s<br />
in patients with neck pain syndromes. This knowledge<br />
provides <strong>the</strong> foundation to fur<strong>the</strong>r develop and evaluate<br />
specific exercises for <strong>the</strong> management <strong>of</strong> this condition.<br />
Based on <strong>the</strong> <strong>muscle</strong> deficits considered to occur in<br />
neck pain, two types <strong>of</strong>exercise programs have been<br />
proposed in <strong>the</strong> literature to address cervical flexor<br />
<strong>muscle</strong> <strong>impairment</strong>. These two types <strong>of</strong>exercise programs<br />
are focused on two different functional requirements.<br />
The first exercise regime consists <strong>of</strong>general<br />
streng<strong>the</strong>ning and endurance exercises for <strong>the</strong> neck<br />
flexor <strong>muscle</strong>s (Berg et al., 1994; Highland et al., 1992;<br />
Jordan et al., 1998; Bronfort et al., 2001). These<br />
exercises involve high load training and thus recruit all<br />
<strong>the</strong> <strong>muscle</strong> synergists that is, both <strong>the</strong> deep and<br />
superficial <strong>muscle</strong>s. For example, streng<strong>the</strong>ning <strong>the</strong> neck<br />
flexor <strong>muscle</strong>s is achieved by performing a head lift<br />
manoeuvre which would recruit all <strong>muscle</strong>s capable <strong>of</strong><br />
contributing to this action including, SCM, AS, longus<br />
colli and longus capitis. A typical exercise program<br />
would train <strong>the</strong> cervical flexors with <strong>the</strong> controlled head<br />
lift exercise and focus on training endurance and<br />
increasing <strong>the</strong> number <strong>of</strong>repetitions. Although several<br />
studies have reported a reduction in pain and improvement<br />
in function with this style <strong>of</strong> exercise (Highland<br />
et al., 1992; Berg et al., 1994; Bronfort et al., 2001),<br />
critical reviews and meta-analyses have generally concluded<br />
that fur<strong>the</strong>r well-designed randomized controlled<br />
trials are warranted (Aker et al., 1996; Kjellman et al.,<br />
1999; Panel, 2001).<br />
The second exercise regime has been designed to focus<br />
on <strong>the</strong> <strong>muscle</strong> control aspects and aims at improving<br />
control <strong>of</strong><strong>the</strong> <strong>muscle</strong>s within <strong>the</strong> neck flexor synergy<br />
(Jull et al., 2004a). In contrast to more traditional high<br />
load strength and endurance exercises, low load exercise<br />
is used to train <strong>the</strong> coordination between <strong>the</strong> layers <strong>of</strong><br />
ARTICLE IN PRESS<br />
D. Falla / Manual Therapy 9 (2004) 125–133 131<br />
neck flexor <strong>muscle</strong>s. With this protocol, patients perform<br />
and hold progressively inner ranges <strong>of</strong> C-CF while<br />
trying to minimize activation <strong>of</strong><strong>the</strong> superficial flexors.<br />
This exercise approach is based on biomechanical<br />
evidence <strong>of</strong><strong>the</strong> functional interplay <strong>of</strong><strong>the</strong> deep and<br />
superficial neck <strong>muscle</strong>s and on physiological and<br />
clinical evidence <strong>of</strong><strong>impairment</strong>s in <strong>the</strong>se <strong>muscle</strong>s in<br />
neck pain patients. The efficacy <strong>of</strong> this emphasis on retraining<br />
<strong>the</strong> C-CF action in association with similar<br />
exercises for <strong>the</strong> shoulder girdle was tested recently in a<br />
randomized controlled clinical trial <strong>of</strong>physio<strong>the</strong>rapy<br />
management for cervicogenic headache (Jull et al.,<br />
2002). The results indicated that <strong>the</strong> specific exercise<br />
program significantly reduced <strong>the</strong> frequency <strong>of</strong> headache<br />
and neck pain and results were maintained in <strong>the</strong> long<br />
term at <strong>the</strong> 12-month follow-up. General streng<strong>the</strong>ning<br />
exercises are not recommended in <strong>the</strong> early stages in this<br />
exercise approach as it is considered that general<br />
exercise will not necessarily address <strong>the</strong> dysfunction<br />
between <strong>the</strong> deep and superficial <strong>muscle</strong>s (Jull, 2000).<br />
Thus specific emphasis is first placed on reeducating <strong>the</strong><br />
deep and postural <strong>muscle</strong>s and general streng<strong>the</strong>ning<br />
exercises are only introduced once <strong>the</strong> imbalance<br />
between <strong>the</strong> deep and superficial neck synergists has<br />
been addressed.<br />
However, <strong>the</strong> results <strong>of</strong>recent research have created<br />
an interesting situation. There is evidence <strong>of</strong>reduced<br />
activation capacity <strong>of</strong><strong>the</strong> DCF <strong>muscle</strong>s with concurrent<br />
increased activity in <strong>the</strong> superficial <strong>muscle</strong>s. Conversely,<br />
<strong>the</strong> superficial <strong>muscle</strong>s have demonstrated greater<br />
fatigability and <strong>the</strong>re is evidence <strong>of</strong> less strength.<br />
Therefore, <strong>the</strong>re is some indication that both exercise<br />
regimes may be beneficial in <strong>the</strong> management <strong>of</strong>cervical<br />
<strong>muscle</strong> dysfunction in neck pain patients.<br />
Although clinical trials <strong>of</strong>both exercise regimes have<br />
produced results to suggest a decrease in neck pain, <strong>the</strong><br />
physiological mechanisms <strong>of</strong>efficacy <strong>of</strong>cervical flexor<br />
<strong>muscle</strong> retraining regimes remain uncertain. For example,<br />
an improvement in DCF <strong>muscle</strong> activation would be<br />
expected following an exercise program based on<br />
retraining <strong>the</strong> activation capacity <strong>of</strong><strong>the</strong> deep <strong>muscle</strong>s.<br />
However, would this program influence <strong>the</strong> fatigability<br />
or neuromuscular efficiency <strong>of</strong> <strong>the</strong> superficial cervical<br />
flexor <strong>muscle</strong>s? Similarly, we would expect a training<br />
regime focused on high load resistance training to<br />
enhance superficial cervical flexor <strong>muscle</strong> strength and<br />
reduce fatigability, but would it alter <strong>the</strong> neuromotor<br />
control <strong>of</strong><strong>the</strong> DCF <strong>muscle</strong>s? There is a paucity <strong>of</strong>good<br />
clinical studies regarding <strong>the</strong> efficacy <strong>of</strong> <strong>the</strong>rapeutic<br />
exercise in neck pain patients, precluding any consensus<br />
on <strong>the</strong> most effective exercise prescribed. Although both<br />
exercise regimes are based on sound <strong>the</strong>oretical rationale,<br />
<strong>the</strong> mechanism <strong>of</strong> efficacy for ei<strong>the</strong>r program is<br />
unclear. Fur<strong>the</strong>r research is warranted to evaluate <strong>the</strong><br />
physiological factors that change with each exercise<br />
intervention and to compare <strong>the</strong> different exercise
132<br />
modalities in order to identify <strong>the</strong> most effective means<br />
to induce <strong>the</strong>se changes. This work is currently underway.<br />
8. Conclusion<br />
In recent years, research has started to unravel <strong>the</strong><br />
<strong>complexity</strong> <strong>of</strong><strong>muscle</strong> <strong>impairment</strong>, which occurs in<br />
people with neck pain disorders. These findings have<br />
considerable implications for <strong>the</strong> prescription <strong>of</strong> <strong>the</strong>rapeutic<br />
exercise. Whilst knowledge <strong>of</strong><strong>the</strong> pathophysiology<br />
underlying cervical <strong>muscle</strong> dysfunction remains<br />
somewhat imprecise, <strong>the</strong> results <strong>of</strong>recent research have<br />
contributed greatly to our understanding <strong>of</strong><strong>the</strong> <strong>impairment</strong><br />
in <strong>the</strong> cervical <strong>muscle</strong>s in people with neck pain,<br />
which has lead to an improved understanding and<br />
direction for <strong>the</strong> management <strong>of</strong> this condition. Fur<strong>the</strong>r<br />
research is now necessary to clarify <strong>the</strong> physiological<br />
mechanisms <strong>of</strong>efficacy <strong>of</strong>cervical <strong>muscle</strong> retraining to<br />
ensure evidence based, optimal practice is embraced in<br />
modern practice.<br />
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