lable at ScienceDirect

Manual Therapy 16 (2011) 80e86

Contents lists avai

Manual Therapy

journal homepage: www.elsevier .com/math

Original article

Association between neck muscle coactivation, pain, and strengthin women with neck pain

Rene Lindstrøm a, Jochen Schomacher a, Dario Farina a, Lotte Rechter b,c, Deborah Falla a,*

aCenter for SensoryeMotor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Fredrik Bajers Vej 7 D-3, DK-9220 Aalborg, DenmarkbMultidisciplinary Pain Center, Aalborg, DenmarkcDepartment of Occupational Therapy and Physiotherapy, Aalborg Hospital, Aarhus University Hospital, Aalborg, Denmark

a r t i c l e i n f o

Article history:Received 14 April 2010Received in revised form7 July 2010Accepted 12 July 2010

Keywords:Neck painCoactivationPreferred directionNeck muscles

* Author for correspondence. Tel.: þ45 99 40 74 59E-mail address: deborahf@hst.aau.dk (D. Falla).

1356-689X/$ e see front matter � 2010 Elsevier Ltd.doi:10.1016/j.math.2010.07.006

a b s t r a c t

This study investigates the relationship between neck muscle coactivation, neck strength and perceivedpain and disability in women with neck pain. Surface electromyography (EMG) was acquired from thesternocleidomastoid (SCM) and splenius capitis (SC) muscles of 13 womenwith chronic neck pain and 10controls as they performed 1) maximal voluntary contractions (MVC) in flexion, extension and left andright lateral flexion, 2) ramped contractions from 0% to 50% MVC in flexion and extension and 3) circularcontractions in the horizontal plane at 15 N and 30 N force. Higher values of EMG amplitude wereobserved for the SC (antagonist) during ramped neck flexion and for the SCM during ramped extension inthe patient group (P< 0.05). The patients displayed reduced values of directional specificity in thesurface EMG of the SCM and SC for the circular contractions (P< 0.05). The EMG amplitude of SC duringcervical flexion was positively correlated with the patients’ pain (R2¼ 0.35, P< 0.05) and perceiveddisability (R2¼ 0.53, P< 0.01). An inverse correlation was evident between the amount of activation of SCduring cervical flexion and strength (R2¼ 0.54, P< 0.01). These observations indicate a relationshipbetween alterations in neuromuscular control in patients with neck pain and functional consequences,including impaired motor performance and increased levels of perceived disability.

� 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Chronic neck pain is a common musculoskeletal disorder(Picavet and Schouten, 2003; Webb et al., 2003). Epidemiologicalstudies show a lifetime prevalence of neck pain between 43% and66.7% (Bovim et al., 1994; Côté et al., 1998, 2004; Guez et al., 2002),a one-year prevalence rate which ranges between 17.9% (Croft et al.,2001) and 64% (Niemeläinen et al., 2006), and a point prevalencearound 20% (Côté et al., 1998; Picavet and Schouten, 2003). Neckpain is also associated with a high recurrence rate (Ghaffari et al.,2006; Holmberg and Thelin, 2006) and, subsequently, higheconomic costs (Korthals-de Bos et al., 2003).

Altered activation of the neckmuscles is awell-known feature ofneck pain. Patients with neck pain show increased antagonisticactivity of their superficial neck muscles (Falla et al., 2004a;Fernández-de-las-Peñas et al., 2008). Reduced specificity of ster-nocleidomastoid muscle activation was observed in patients withneck painwhenperforming isometric contractions with continuouschange in force direction in the range 0e360�, resulting in

; fax: þ45 98 15 40 08.

All rights reserved.

increased activation of the muscle when acting as an antagonist(Falla et al., 2010). This result supports the consistent finding ofaugmented activity of the superficial neck muscles in patients withneck pain (Falla et al., 2004b; Szeto et al., 2005; O’Leary et al., 2007;Johnston et al., 2008). These observations are also in agreementwith experimental pain studies which show a pain-induced reor-ganization of the motor strategy characterized by reduced activityof the agonist muscle and increased activity of the antagonistmuscle (Graven-Nielsen et al., 1997). Possible explanations forthese findings include the direct effects of nociception on motorneuron output, effects of pain on sympathetic activity, and changesin motor planning.

Although increased coactivation of the neck muscles may bebeneficial in thepresenceof acutepain toenhancecervical stabilitybyreducing velocity and range of movement, it may reduce neckstrength and contribute to recurrent pain by altering the load distri-bution on the spine and irritating pain sensitive structures. However,the relationship betweenneckmuscle coactivation, strengthandpainintensity is unknown. Therefore, the purpose of this study is toinvestigate the relationship between the extent of neck musclecoactivation, the maximum amount of neck strength and perceivedpain and disability inwomenwith persistent neck pain.

R. Lindstrøm et al. / Manual Therapy 16 (2011) 80e86 81

2. Methods

2.1. Subjects

Thirteen women with chronic neck pain greater than 1 year(mean� SD: 7.1�6.1 yrs) participated in the study. Subjects wereexcluded if theypreviouslyhad cervical spine surgery, previous necktrauma, presented with neurological signs in the upper limb or hadparticipated in a neck exercise program in the past 12 months.

Ten women were recruited as controls. Control subjects werefree of shoulder and neck pain, had no past history of orthopedicdisorders affecting the shoulder or neck region and no history ofneurological disorders. Ethical approval for the study was grantedby the Ethics Committee (nr 20070045) and the procedures wereconducted according to the Declaration of Helsinki.

2.2. Procedure

Participants were seated with their head rigidly fixed in a devicefor the measurement of multidirectional neck force (AalborgUniversity, Denmark) with their back supported, knees and hips in90� of flexion and their torso firmly strapped to the seat back. Thedevice is equipped with eight adjustable contacts which arefastened around the head to stabilize the head and provide resis-tance during isometric contractions of the neck. The force device isequippedwith force transducers (strain gauges) tomeasure force inthe sagittal and coronal planes. The electrical signals from the straingauges were amplified (LISiN e OT Bioelettronica, Torino, Italy) andtheir output was displayed on an oscilloscope as visual feedback tothe subject.

Following a period of familiarization with the measuring deviceand practice of the contractions, subjects performed twomaximumvoluntary contractions (MVC) for cervical flexion, extension, leftlateral flexion, and right lateral flexion, with 1-min rest betweencontractions. Verbal encouragement was provided to the subject topromote higher forces in each trial. The highest value of forcerecorded over the 2 maximum contractions for each direction wasselected as the reference MVC, and used to calculate the sub-maximal force targets. The order of the MVC contractions wasrandomized between movement directions.

A rest of 30 min followed the MVCs. Subsequently, the subjectsperformed a linearly increasing force contraction from 0% to 50%MVC in 3 s (ramp contraction) in cervical flexion and extension.Visual feedback on force was provided to the subject during thesecontractions. A rest of 2-min was provided between contractionswhich were randomized for force direction.

Following a further 10 min of rest, the subjects performed anisometric contraction at 15 and 30 N force in the horizontal planeagainst the head restraint with change in force direction in therange 0e360� (circular isometric contractions). Circular templateswere superimposed on the oscilloscope to provide force feedbackto the subjects during these contractions. Following a period ofw10 min to practice for the task, the subjects performed the 15 and30 N contractions in both clockwise and counter-clockwise direc-tions with 2-min of rest between contractions. Each circularcontraction had a duration ofw12 s and was performed at constantvelocity by the subjects under guidance of a counter for time andvisual feedback on force direction and magnitude. The direction ofthe contractions was randomized and each contraction was fol-lowed by rest periods of 2-min.

2.3. Electromyography recordings

Bipolar surface electromyography (EMG) signals were detectedfrom the sternal head of the sternocleidomastoid and splenius

capitis muscles bilaterally with pairs of electrodes (Neuroline72001-k; Medicotest, Denmark) positioned 20 mm apart followingskin preparation. For the splenius capitis, electrodes were posi-tioned over the muscle belly at the C2eC3 level between theuppermost parts of trapezius and sternocleidomastoid. For thesternocleidomastoid muscle, electrodes were placed over the distalportion of the muscle belly (Falla et al., 2002). The bipolar EMGsignals were amplified (128-channel surface EMG amplifier, LISiN-OT Bioelettronica, Torino, Italy; �3 dB bandwidth 10e500 Hz) bya factor of 2000, sampled at 2048 Hz, and converted to digital formby a 12-bit A/D converter. A ground electrode was placed aroundthe right wrist.

2.4. Signal analysis

For the ramped contractions, the force signal was low-passfiltered (anti-causal Butterworth filter of order 4, cut-off frequency10 Hz) and normalized with respect to the MVC force. The averagerectified value (ARV) was estimated from the EMG signals over 5intervals of 250-ms duration, during which the average force levelwas 10e50% MVC (10% MVC increments).

During the circular contractions, the surface EMG ARV was esti-mated in intervals of 250 ms and analyzed as a function of the angleof force direction (directional activation curve). The directionalactivation curves represent the modulation in intensity of muscleactivity with the direction of force exertion and represent a closedarea when expressed in polar coordinates. The line connecting theoriginwith the central point of this area defined a directional vector,whose lengthwasexpressedasapercentof themeanARVduring theentire task. This normalized vector length represents the specificityof muscle activation: it is equal to zero when the EMG amplitude isthe same in all directions and corresponds to 100% when the EMGamplitude is exclusively in one direction (themuscle is active in onlyone direction). In addition, the EMG amplitude was averaged acrossthe entire circular contraction to provide an indicator of the overallmuscle activity. Since no significant differences were observed forthe data extracted from the circular contractions in the clockwiseand counter-clockwise directions, the datawere combined to obtainan average.

2.5. Statistical analysis

A two-way analysis of variance (ANOVA) was used to evaluatedifferences between patients and controls for maximum neckstrength with group (patient, control) as the between subjectsvariable and direction (flexion, extension, right lateral flexion, leftlateral flexion) as the within subject variable.

The ARV of the sternocleidomastoid and splenius capitismuscles during the ramped contractions was assessed with muscle(left and right sternocleidomastoid and splenius capitis) and force(10e50% MVC in 10% increments) as the within subject variablesand group (patient, control) as the between subjects variable.

A three-way ANOVA was conduced to assess differences in thedirectional specificityof sternocleidomastoidmuscle activity (vectorlength) with force (15 N, 30 N) and muscle (left and right sterno-cleidomastoid and splenius capitis) as the within subject variablesand group (patient, control) as the between subjects variable.Significant differences revealed by ANOVA were followed by post-hoc StudenteNewmaneKeuls (SNK) pair-wise comparisons.

Linear correlation analysis was used to determine the associa-tion between the patient’s average neck pain intensity, NeckDisability Index (NDI) and the ARV of the sternocleidomastoid andsplenius capitis during the ramped contractions. Results arereported as mean and SD in the text and SE in the figures. Statisticalsignificance was set at P< 0.05.

Table 1Mean� SD of maximumvoluntary force (N) produced for cervical flexion, extension,right lateral flexion and left lateral flexion in patients with neck pain and controlsubjects.

Force Direction Neck pain Controls Comparison betweenpatients and controls

Flexion 97.7� 40.4 N 143.0� 41.4 N P< 0.05Extension 182.5� 77.7 N 235.7� 54.6 N P< 0.05Right lateral flexion 114.0� 47.6 N 170.7� 55.5 N P< 0.05Left lateral flexion 119.8� 49.2 N 176.7� 46.0 N P< 0.05

R. Lindstrøm et al. / Manual Therapy 16 (2011) 80e8682

3. Results

3.1. Participants

Patients did not differ (P> 0.05) in age (37.7� 7.8 yrs), weight(77.2�18.5 kg) or height (168.8� 4.0 cm) from controls (33.1�9.3yrs, 66.8� 13.0 kg, 165.9� 8.2 cm respectively). The patients’average score for the Neck Disability Index (0e50) (Vernon andMior, 1991) was 21.6� 8.4 and their average pain intensity ratedon a visual analogue scale (0e10) was 5.1�1.8.

3.2. Motor output

The maximum voluntary neck strength was dependent on forcedirection (F¼ 46.7, P< 0.00001); extension and bilateral lateralflexion showed higher values of force compared to flexion (SNK: allP< 0.001). Furthermore, extension force was greater than left andright lateral flexion force (SNK: both P< 0.05). However, the patientgroup exerted lower force across all directions compared to thecontrol subjects (F¼ 6.8, P< 0.05; Table 1).

3.3. Ramp contractions

Both sternocleidomastoid and splenius capitis ARV increasedwith increasing cervical flexion force (F¼ 110.7, P< 0.0001, Fig. 1).The ARV of sternocleidomastoid (agonist) did not differ betweenpatients and controls during cervical flexion, however highervalues of ARV were observed for the right splenius capitis (antag-onist) at all force levels in the patient group (SNK: all P< 0.05,Fig. 1). Higher values of left splenius capitis ARVwere also observedfor the patient group during cervical flexion at force levels 20e50%(all SNK: P< 0.05, Fig. 1).

0

10

20

30

40

50

60

70

Cont

PatieCont

Patie

Aver

age

Rec

tifie

d Va

lue

(µV)

Agonist

10 20 30 40 50Submaximal Force (% MVC)

A B

Fig. 1. Mean� SE of the left and right sternocleidomastoid (A) and splenius capitis (B) avvoluntary contraction (MVC) for the patient and control groups.

Both splenius capitis (agonist) and sternocleidomastoid(antagonist) ARV increased with increasing cervical extension force(F¼ 23.1, P< 0.0001, Fig. 2). However, splenius capitis and sterno-cleidomastoid ARV were greater for the patients across all forcelevels compared to the control subjects (F¼ 4.4, P< 0.05, Fig. 2).

3.4. Directional activation curves

Representative directional activation curves during a circularcontraction performed at 15 N are illustrated in Fig. 3 for a controlsubject and a patient. In this example, the control subject presentswith defined activation of the sternocleidomastoid and spleniuscapitis muscles with the highest amplitude of activity towardsipsilateral anterolateral flexion and ipsilateral posterolateralextension respectively. Note that both the sternocleidomastoid andsplenius capitis are minimally active during the antagonist phase.Conversely, the directional activation curves for the representativepatient show activation of the sternocleidomastoid during exten-sion and splenius capitis during flexion supporting the results fromthe isometric ramped contraction of increased antagonist muscleactivity.

Accordingly, overall the patient group displayed reduced valuesof directional specificity in the surface EMG for both the sterno-cleidomastoid and splenius capitis muscles bilaterally for both the15 N and 30 N circular contractions (main effect for group: F¼ 6.0;P< 0.05, Fig. 4).

3.5. Association between pain, strength and antagonist muscleactivity

The ARV of splenius capitis (averaged across sides) duringcervical flexion was positively correlated with the patients’ repor-ted pain (R2¼ 0.35, P< 0.05) and perceived disability (R2¼ 0.53,P< 0.01) (Fig. 5). The ARV of splenius capitis (averaged across sides)during cervical flexion showed a tendency to be inversely corre-lated with the patients’ maximum cervical flexion force (R2¼ 0.26,P¼ 0.07, Fig. 6). When considering the total neck strength (sumacross all directions of force), the inverse correlation between theamount of activation of splenius capitis during cervical flexion andneck strength was evident (R2¼ 0.54, P< 0.01, Fig. 6). No correla-tions were observed between the amount of activation of thesternocleidomastoid muscle during cervical extension and thepatient’s strength (extension strength: R2¼ 0.00; P¼ 0.97; total

rol Right Side

nt Right Siderol Left Side

nt Left Side

Antagonist

0

10

20

30

40

50

60

Aver

age

Rec

tifie

d Va

lue

(µV)

10 20 30 40 50Submaximal Force (% MVC)

erage rectified value during ramped cervical flexion from 0% to 50% of the maximal

0

10

20

30

40

50

60

10 20 30 40 50Submaximal Force (% MVC)

Aver

age

Rec

tifie

d Va

lue

(µV)

AgonistA Antagonist

0

5

10

15

20

25

10 20 30 40 50Submaximal Force (% MVC)

Aver

age

Rec

tifie

d Va

lue

(µV)

B

Control Right Side

Patient Right SideControl Left Side

Patient Left Side

Fig. 2. Mean� SE of the left and right splenius capitis (A) and sternocleidomastoid (B) average rectified value during ramped cervical extension from 0% to 50% of the maximalvoluntary contraction (MVC) for the patient and control groups.

R. Lindstrøm et al. / Manual Therapy 16 (2011) 80e86 83

neck strength: R2¼ 0.01; P¼ 0.73) or perceived pain and disability(pain: R2¼ 0.08; P¼ 0.24; NDI: R2¼ 0.12; P¼ 0.34).

4. Discussion

This study showed that patients with neck pain have higherlevels of coactivation of the sternocleidomastoid and splenius

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

Control

B

A

Fig. 3. Representative directional activation curves for the sternocleidomastoid (A) and splenhorizontal plane at 15 N with change in force direction in the range 0e360� .

capitis muscles compared to control subjects. Furthermore,increased coactivation of the splenius capitis musclewas associatedwith lower neck strength and higher levels of pain and associateddisability.

Patients with neck pain showed an overall reduction of neckstrength. Maximum strength was 31.7%, 22.6%, 33.2%, and 32.2%less for the patients than controls for flexion, extension, right lateral

60

240

30

210180

330

150

300

120

270 90

0°

60

240

30

210180

330

150

300

120

270 90

0°

Neck Pain

ius capitis (B) of a control subject and a patient performing a circular contraction in the

0

5

10

15

20

25

30

35

40

Right SCM Left SCM Right SC Left SC

Neck Pain

Controls

0

5

10

15

20

25

30

35

40

A

B

Rel

ativ

e m

uscl

e sp

ecifi

city

to

dire

ctio

n (%

)R

elat

ive

mus

cle

spec

ifici

ty

to d

irect

ion

(%)

Fig. 4. Mean� SE of the directional specificity in the surface EMG of the right and leftsternocleidomastoid (SCM) and splenius capitis (SC) obtained during the circularcontractions at both 15 (A) and 30 N (B) of force for the patients with neck pain andcontrol subjects.

R. Lindstrøm et al. / Manual Therapy 16 (2011) 80e8684

flexion and left lateral flexion, respectively, resulting in a total neckstrength which was 29.2% lower for the patient group. The strengthloss found in this study is similar to the results of several previousstudies. For example, Ylinen et al. (2004) reported a 29% force lossin patients with neck pain for both flexion and extension and Chiuand Lo (2002) found reductions in force of 17.8%, 25.9%, 13.3%, and16.3% for flexion, extension, right lateral flexion and left lateralflexion. However, there is a large variability in the results reportedin the literature and other studies showed greater reductions.Pearson et al. (2009) found a 52% reduction in force in patients withneck pain for flexion, 60% for left lateral flexion, 62% for right lateralflexion, and 66% for extension and Prushansky et al. (2005) repor-ted a 90% reduction of neck force in all directions. Variability of neckstrength in patients is presumably due to differences in patientpopulations (pain intensity, duration, cause of neck pain), but mayalso reflect varying degrees of neck muscle coactivation, which was

0 10 20 30 40

0

20

40

60

80

100

Neck Disability Index (0-50)

Sple

nius

Cap

itis

Aver

age

Rec

tifie

d Va

lue

(µV)

BA

Fig. 5. Scatter plot of the splenius capitis average rectified value obtained during the rampDisability Index (A) and average neck pain intensity rated on a visual analogue scale (B).

investigated in this study. Furthermore the general physical activitylevel of the patients may influence strength measurements andmay partially account for the reduced force output compared tocontrol subjects.

The sternocleidomastoid (Blouin et al., 2007; Falla et al., 2010)and most extensor muscles (Blouin et al., 2007) have well-definedpreferred directions of activation in healthy subjects, which wasconfirmed in this study. It has been shown that the directionalspecificity of sternocleidomastoid muscle activity is reduced inpatients with neck pain and is associated with reduced modula-tion of sternocleidomastoid motor unit discharge rate withmultidirectional force contractions (Falla et al., 2010). The resultsof the current study show that reduced specificity of activity is notunique to the sternocleidomastoid, since similar observationswere made for the splenius capitis muscle. Reduced specificity ofmuscle activity results mainly in increased activation of themuscle when acting as an antagonist (Fig. 3) and is consistent withthe increased antagonist activation of the extensors during theramped contraction. This suggests that increased antagonistactivity is a common feature associated with neck pain. Further-more, the results of this study show that increased levels of neckextensor antagonistic activity are associated with impaired neckstrength.

Increased neck muscle coactivation likely reflects reorganiza-tion of the motor control strategy potentially to enhance cervicalspine stability (Fernández-de-las-Peñas et al., 2008). Coactivationof the neck flexor and extensor muscles is considered a normalstrategy to increase stiffness of the spine (Cheng et al., 2008), forexample when a postural perturbation is applied to the trunk(Danna-Dos-Santos et al., 2007). Up to 80% of cervical spine stabilityis provided by the surrounding muscles (Panjabi, 1992), especiallythe deeper muscles with their smaller moment arms and attach-ments to adjacent vertebrae (Blouin et al., 2007). Weakness of thedeep cervical flexormuscles is known to be present in patients withneck pain and is associated with increased activity of superficialsynergists (Falla et al., 2003). Increased coactivation of neckmuscles may therefore indicate an attempt to enhance the stabilityof the neck. Fear of pain during maximal contractions (kinesi-ophobia) may also induce a strategy of increased neck musclecoactivation. Fear of pain during neck extension is thought to limitextensor force in patients with whiplash-induced neck pain whooften have injured posterior cervical spine structures (Prushanskyet al., 2005). However, a non-significant correlation betweenkinesiophobia and neck strength, and between pain catastrophiz-ing and neck strength was shown in patients with chronic whiplash(Pearson et al., 2009). Increased sternocleidomastoid and spleniusmuscle activity for the patient group may also be due to an

Sple

nius

Cap

itis

Aver

age

Rec

tifie

d Va

lue

(µV)

Average Neck Pain Intensity (0-10)2 4 6 8

0

20

40

60

80

100

ed cervical flexion contraction and the patients’ perceived disability rated on the Neck

100 200 300 400 500 600 700 800 9000

20

40

60

80

100

0 40 80 120 160 2000

20

40

60

80

100

Sple

nius

Cap

itis

Aver

age

Rec

tifie

d Va

lue

(µV)

Sple

nius

Cap

itis

Aver

age

Rec

tifie

d Va

lue

(µV)

BA

Neck Flexion Strength (N) Total Neck Strength (N)

Fig. 6. Scatter plot of the splenius capitis average rectified value obtained during the ramped cervical flexion contraction and the patients’ neck flexion strength (A) and total neckstrength (B).

R. Lindstrøm et al. / Manual Therapy 16 (2011) 80e86 85

increased sympatho-adrenal outflow as a consequence of pain.Increased activity of the sternocleidomastoid and splenius musclehas been observed in healthy volunteers following physiologicalsympathetic activation elicited by the cold pressor test (Boudreauet al., 2010).

Although increased coactivation of the neck muscles may bebeneficial in the presence of pain to increase cervical stability, asobserved in this study, it is associated with functional conse-quences, i.e. reduced neck strength. Furthermore, increased neckmuscle coactivation may contribute to recurrent pain by alteringthe load distribution on the spine and subsequently aggravatingthe patients’ condition. Coactivation of agonist/antagonistmuscles significantly increases spinal stiffness (Lee et al., 2006)and spinal compression which is considered sufficient to inducelumbar spine injuries and consequently low-back pain (van Dieénand Kingma, 2005) and may also be relevant in persistent neckpain disorders (Choi, 2003). Unique to this study, we showed thatthe degree of coactivation of the splenius capitis muscle ispositively correlated with the patients’ reported pain andperceived disability which supports this premise. Surprisingly,a similar relation was not observed for the sternocleidomastoidmuscle despite reduced specificity of sternocleidomastoidactivity and increased activation of the sternocleidomastoidmuscle during the ramped cervical extension contraction in thepatient group. This finding may be attributed to the greaterreduction in neck flexion strength for the patient group (31.7%less than controls) compared to extension (22.6% less thancontrols). That is, increased muscle coactivation may particularlyoccur in the directions of least strength.

5. Conclusion

Patients with neck pain have higher levels of coactivation of thesternocleidomastoid and splenius capitis muscles. Furthermore,increased coactivation is associated with reduced neck strengthand higher levels of pain and associated disability. These observa-tions indicate a relation between alterations in neuromuscularcontrol of the cervical spine in patients with neck pain and func-tional consequences including impaired motor performance andincreased levels of perceived disability.

Acknowledgements

Supported by the Danish Medical Research Council, Kiropra-ktorfonden, Denmark and Østifterne, Denmark.

References

Bovim G, Schrader H, Sand T. Neck pain in the general population. Spine 1994;19(12):1307e9.

Blouin J-S, Siegmund GP, Carpenter MG, Inglis JT. Neural control of superficial anddeep neck muscles in humans. Journal of Neurophysiology 2007;98:920e8.

Boudreau S, Farina D, Djupsjöbacka M, Falla D. Sympathetic activation impairsproprioceptive acuity of the neck. The XVIII International Conference of theSociety of Electrophysiology and Kinesiology (ISEK), Aalborg, 16e19 June 2010.

Cheng C-H, Lin K-H, Wang J-L. Co-contraction of cervical muscles during sagittaland coronal neck motions at different movement speeds. European Journal ofApplied Physiology 2008;103:647e54.

Choi H. Quantitative assessment of co-contraction in cervical muscles. MedicalEngineering & Physics 2003;25:133e40.

Chiu TT, Lo SK. Evaluation of cervical range of motion and isometric neck musclestrength: reliability and validity. Clinical Rehabilitation 2002;16:851e8.

Côté P, Cassidy D, Caroll L. The Saskatchewan health and back pain survey, theprevalence of neck pain and related disability in Saskatchewan adults. Spine1998;23(15):1689e98.

Côté P, Cassidy JD, Caroll LJ, Kristman V. The annual incidence and course of neckpain in the general population: a population-based cohort study. Pain2004;112:267e73.

Croft PR, Lewis M, Papageorgiou AC, Thomas E, Jayson MIV, Macfarlane GJ, et al. Riskfactors for neck pain: a longitudinal study in the general population. Pain2001;93:317e25.

Danna-Dos-Santos A, Degani AM, Latash ML. Anticipatory control of head posture.Clinical Neurophysiology 2007;118:1802e14.

van Dieén JH, Kingma I. Effects of antagonistic co-contraction on differencesbetween electromyography based and optimization based estimates of spinalforces. Ergonomics 2005;48(4):411e26.

Falla D, Dall’Alba P, Rainoldi A, Merletti R, Jull G. Repeatability of surface EMGvariables in the sternocleidomastoid and anterior scalene muscles. EuropeanJournal of Applied Physiology 2002;87:542e9.

Falla D, Jull G, Dall’Alba P, Rainoldi A, Merletti R. An electromyographic analysis ofthe deep cervical flexor muscles in performance of craniocervical flexion.Physical Therapy 2003;83(10):899e906.

Falla D, Lindstrøm R, Rechter L, Farina D. Effect of pain on modulation in dischargerate of sternocleidomastoid motor units with force direction. Clinical Neuro-physiology 2010;121(5):744e53.

Falla D, Rainoldi A, Merletti R, Jull G. Spatio-temporal evaluation of neck muscleactivation during postural perturbations in healthy subjects. Journal of Elec-tromyography and Kinesiology 2004a;14:463e74.

Falla D, Bilenkij G, Jull G. Patients with chronic neck pain demonstrate alteredpatterns of muscle activation during performance of a functional upper limbtask. Spine 2004b;29(13):1436e40.

Fernández-de-las-Peñas C, Falla D, Arendt-Nielsen L, Farina D. Cervical muscle co-activation in isometric contractions is enhanced in chronic tension-typeheadache patients. Cephalalgia 2008;28:744e51.

Ghaffari M, Alipour A, Farshad A, Yensen I, Vingard E. Incidence and recurrence ofdisabling low back pain and neck-shoulder pain. Spine 2006;31(21):2500e6.

Graven-Nielsen T, Svensson P, Arendt-Nielsen L. Effects of experimental muscle painon muscle activity and co-ordination during static and dynamic motor function.Electroencephalography and Clinical Neurophysiology 1997;105:156e64.

Guez M, Hildingsson C, Nilsson M, Toolanen G. The prevalence of neck pain:a population-based study from northern Sweden. Acta Orthopaedica Scandi-navica 2002;73(4):455e9.

Holmberg SA, Thelin AG. Primary care consultation, hospital admission, sickleave and disability pension owing to neck and low back pain: a 12-yearprospective cohort study in a rural population. BMC Musculoskeletal Disor-ders 2006;7:66.

R. Lindstrøm et al. / Manual Therapy 16 (2011) 80e8686

Johnston V, Jull G, Souvlis T, Jimmieson NL. Neck movement and muscle activitycharacteristics in female office workers with neck pain. Spine 2008;33(5):555e63.

Korthals-de Bos IBC, Hoving JL, van Tulder MW, Tutten-Van Molken MPMH, Ader HJ,de Vet HCW, et al. Cost effectiveness of physiotherapy, manual therapy, andgeneral practitioner care for neck pain: economic evaluation alongside a rand-omised controlled trial. British Medical Journal 2003;326:911e4.

Lee PJ, Rogers EL, Granata KP. Active trunk stiffness increases with co-contraction.Journal of Electromyography and Kinesiology 2006;16:51e7.

Niemeläinen R, Videman T, Battié C. Prevalence and characteristics of upper or mid-back pain in Finnish men. Spine 2006;31(16):1846e9.

O’Leary S, Falla D, Jull G, Vicenzino B. Muscle specificity in tests of cervicalflexor muscle performance. Journal of Electromyography and Kinesiology2007;17:35e40.

Panjabi MM. The stabilizing system of the spine. Part II. Neutral zone and instabilityhypothesis. Journal of Spinal Disorders 1992;5:390e7.

Pearson I, Reichert A, De Serres SJ, Dumas JP, Côté JN. Maximal voluntary isometricneck strength deficits in adults with whiplash-associated disorders and

association with pain and fear of movement. Journal of Sports and PhysicalTherapy 2009;39(3):179e87.

Picavet HSJ, Schouten JSAG. Musculoskeletal pain in the Netherlands: prevalences,consequences and risk groups, the DMC3-study. Pain 2003;102:167e78.

Prushansky T, Gepstein R, Gordon C, Dvir Z. Cervical muscles weakness in chronicwhiplash patients. Clinical Biomechanics 2005;20:794e8.

Szeto GPY, Straker LM, O’Sullivan PB. A comparison of symptomatic and asymp-tomatic office workers performing monotonous keyboard worke1: neck andshoulder muscle recruitment patterns. Manual Therapy 2005;10:270e80.

Vernon H, Mior S. The Neck Disability Index: a study of reliability and validity.Journal of Manipulative and Physiological Therapeutics 1991;14:409e15.

Webb R, Brammah T, Lunt M, Urwin M, Allison T, Symmons D. Prevalence andpredictors of intense, chronic, and disabling neck and pack pain in the UKgeneral population. Spine 2003;28(11):1195e202.

Ylinen J, Salo P, Nykänen M, Kautiainen H, Häkkinen A. Decreased isometric neckstrength in women with chronic neck pain and the repeatability of neckstrength measurements. Archives of Physical Medicine and Rehabilitation2004;85:1303e8.