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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 />

80<br />

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 />

flexion<br />

0<br />

22 24 26 28 30<br />

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 />

120<br />

100<br />

80<br />

60<br />

40<br />

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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