DISABILITY AND REHABILITATION,

2004;

VOL.

26,

NO.

12, 712717

Neuromuscular eciency of the sternocleidomastoid and anterior scalene muscles in patients with chronic neck pain
D. FALLA{*, G. JULL{, S. EDWARDS{, K. KOH{ and A. RAINOLDI{}
{ Division of Physiotherapy, The University of Queensland, Brisbane, Queensland, Australia { Centro di Bioingegneria, Dip. di Elettronica, Politecnico di Torino, Italy } Department of Physical Medicine and Rehabilitation, University of Tor Vergata and Fondazione Don Gnocchi, Roma, Italy

Abstract Purpose: This study compared the neuromuscular eciency (NME) of the sternocleidomastoid (SCM) and anterior scalene (AS) muscles between 20 chronic neck pain patients and 20 asymptomatic controls. Method: Myoelectric signals were recorded from the sternal head of SCM and the AS muscles as subjects performed submaximal isometric cervical exion contractions at 25 and 50% of the maximum voluntary contraction (MVC). The NME was calculated as the ratio between MVC and the corresponding average rectied value of the EMG signal. Ultrasonography was used to measure subcutaneous tissue thickness over the SCM and AS to ensure that dierences did not exist between groups. Results: For both the SCM and AS muscles, NME was shown to be signicantly reduced in patients with neck pain at 25% MVC (p 5 0.05). Subcutaneous tissue thickness over the SCM and AS muscles was not dierent between groups. Conclusions: Reduced NME in the supercial cervical exor muscles in patients with neck pain may be a measurable altered muscle strategy for dysfunction in other muscles. This aberrant pattern of muscle activation appears to be most evident under conditions of low load. NME, when measured at 25% MVC, may be a useful objective measure for future investigation of muscle dysfunction in patients with neck pain.

Introduction Dysfunction of the muscle system has been found in patients with cervical spine disorders. Increased activity
* Author for correspondence; Division of Physiotherapy, The University of Queensland, St Lucia, Brisbane, Queensland, 4072, Australia. e-mail: d.falla@shrs.uq.edu.au

of the supercial cervical muscles has been documented in patients with neck pain of both insidious and traumatic (whiplash) origins using electromyography (EMG). Specically, patients with neck pain have demonstrated (a) increased activity of the upper trapezius (UT) muscle under conditions of mental load,1 (b) decreased ability to relax the UT muscles between repeated maximal isometric contractions of shoulder exion,2 (c) increased activity of the UT, sternocleidomastoid (SCM) and anterior scalene (AS) muscles during a repetitive upper limb functional task3 5 and (d) increased activity of the SCM muscle during a specic low load test of cranio-cervical exion.6 Increased activity of the supercial cervical muscles of patients with neck pain during performance of low load tasks could represent an altered motor control strategy to compensate for weakness or inhibition of the deep cervical muscles.6 This inecient pattern of muscle activation may play a role in the perpetuation of patient symptoms and initiate recurrent episodes of neck pain. Neuromuscular eciency (NME) can be dened as the quotient of force and the integrated EMG.7 Previous studies have demonstrated a trend towards reduction of the NME in the SCM8, 9 and AS9 muscles during cervical exion isometric contractions in neck pain patients. The small sample size (n = 10) used in these studies may account for the lack of statistical signicance despite an obvious trend. Furthermore, subcutaneous tissue thickness over the muscles was not measured. It is well documented that variability

Disability and Rehabilitation ISSN 09638288 print/ISSN 14645165 online # 2004 Taylor & Francis Ltd http://www.tandf.co.uk/journals DOI: 10.1080/09638280410001704287

Neuromuscular eciency in patients with chronic neck pain in tissue thickness between subjects may substantially alter estimates of EMG amplitude and therefore NME.10, 11 The purpose of this study was to compare the neuromuscular eciency of the supercial cervical exor muscles (SCM and AS) contracting at 25 and 50% of the maximum voluntary contraction (MVC) between patients with chronic neck pain and asymptomatic subjects. Ultrasonography was used to measure subcutaneous tissue thickness over the SCM and AS to ensure dierences in tissue thickness between groups did not bias the results. Real time ultrasonography Subcutaneous tissue thickness over the SCM and AS muscles was measured using a 5 MHz linear array transducer, positioned over the distal third of each muscle where subsequent EMG recordings would be made. A clear image of the muscle was obtained, captured and stored on the computer. An electronic ruler incorporated in the software was used to measure subcutaneous tissue thickness over each muscle. Electromyography Myoelectric signals were detected from the sternal head of SCM and the AS muscles using linear arrays of four electrodes (silver bars 10 mm apart, 5 mm long, and 1 mm diameter) in single dierential conguration.14 Signals were recorded from the right side in control subjects, as previous research has identied the absence of dominance eects for the right and left SCM and AS muscles in asymptomatic subjects.9 Signals were recorded on the side of greatest pain for the neck pain patients as less NME ipsilateral to the side of pain has been identied in patients with unilateral neck pain.15 The ground reference was strapped around the wrist. Signals were amplied (Gain = 2000), passed through a 10 450 Hz-bandwidth lter (40 db/decade slope on each side) and sampled at 2048 Hz (ASE16-16 channel amplier, LISiN Centro di Bioingegneria, Politecnico di Torino, Italy). The samples were digitized by a 12bit A/D converter and stored on a personal computer. Cervical exion force A custom designed cervical exion force-measuring device was anchored to a plinth. The aluminium frame housed two load cells (CCT Transducers, Torino, Italy) with a full scale of 250 N each (gure 1). Each force transducer was capable of recording both compression and tension, and by this means, the oset could be adjusted to accommodate for the weight of the subjects head. The subjects head rested on a padded head support and an adjustable Velcro strap was fastened across the forehead, acting to stabilize the head and provide resistance during cervical exion isometric contractions. With this design, the device was able to detect the force produced by the cervical exor muscles in the initial phase of contraction to counteract gravity before head lifting. The electrical signals from the load cells were amplied (MISO1, LISiN Centro di Bioingegneria, Politecnico di Torino, Italy) and relayed to a
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Methods
SUBJECTS

Twenty subjects with a history of chronic neck pain and 20 control subjects participated in this study. Subjects in the neck pain group (17 females, 3 males) were aged between 18 and 47 years (mean 29.0 + 6.8 years) and had a history of neck pain of greater than one year (mean 5.2 + 3.2 years). Subjects were excluded if they had either undergone cervical spine surgery, complained of any neurological signs or had participated in a neck exercise programme in the past 12 months. Asymptomatic subjects (16 females, 4 males) were aged between 21 and 51 years (mean 30.0 + 7.5 years) and were included if they were free of neck pain, had no past history of orthopaedic disorders aecting the neck and no history of neurological disorders. This study was approved by the Institutional Medical Research Ethics Committee and all procedures were conducted according to the Declaration of Helsinki.
INSTRUMENTATION AND MEASUREMENTS

Pain and disability measures The cervical spine was examined by a trained physiotherapist to conrm the presence or absence of cervical segmental pain and dysfunction in the neck pain patients and asymptomatic subjects respectively.12 Patients with neck pain completed the Neck Disability Index (NDI)13 and indicated their average intensity of neck pain on a 10 cm Numerical Rating Scale (NRS) anchored with no pain and the worst possible pain imaginable. The NDI (score out of a 50) was used to measure the patients perceived impairments resulting from their neck pain. Patients did not report pain at the time of testing.

D. Falla et al. subject to reach a higher amount of force in each subsequent trial. Rest intervals of 5 min were provided between each repetition. The highest value of force recorded over the three maximum contractions was selected as the reference MVC allowing sub-maximal targets to be set on the visual feedback display. The subjects skin was prepared by gentle local abrasion using medical sandpaper (3M Red DotTM, 3M Australia) and cleaned with an alcohol wipe prior to attachment of the surface electrodes, in accordance with recommendations for skin preparation.18 Electrode arrays were positioned over the distal portion of the SCM and AS muscles following published guidelines for electrode placement.19 A thin lm of conductive electrode gel was applied to the electrodes to ensure good electrode contact for the duration of the experiment. 1 The electrodes were xed using a Fixomull extensible dressing (BSN Medical Pty Ltd. Clayton, Victoria, Australia). Subjects were requested to perform a brief isometric cervical exion contraction (3 5 s) allowing the quality of the myoelectric signals to be evaluated according to the criteria outlined by Bergamo and colleagues.20 This included: (a) detection of propagating single motor unit action potentials, (b) absence of innervation zones and (c) estimation of mean values of the muscle bre conduction velocity within the physiological range. Orientation and position of the electrode arrays were altered until an optimal signal (in the sense dened above) was visible. The subject then performed submaximal cervical exion contractions at 25 and 50% MVC for 15 s using the visual display for feedback of the force output. A rest period of 5 min was given between each contraction. Data management The average rectied value (ARV) was calculated for 0.5 s epochs throughout each 15 s contraction. Linear regression was calculated over the 30 ARV estimates and the intercept with the Y axis (i.e., ARV estimate at time = 0) was selected as the reference value (the initial ARV). The neuromuscular eciency (NME) was calculated as the ratio between MVC and the corresponding initial ARV, measured in N/mV. Under this denition, NME could be considered as an estimate of the amount of electrical activity that each subject produced to reach a value of force. The dependent variables were the NME for SCM and AS at two levels of force: 25 and 50% MVC. The independent variables consisted of the two subject groups

Figure 1 Experimental Set-up: The subjects head rests on a padded head support of a custom designed cervical exion force-measuring device. An adjustable Velcro strap is fastened across the forehead acting to stabilize the head and provide resistance during cervical exion isometric contractions.

visual feedback device. This allowed sub-maximal targets to be set and provided the subject with feedback of the force level produced during contractions. Excellent repeatability (Intraclass Correlation Coecient = 92.5%) and good repeated measure precision (normalized standard error of the mean = 8.7%) have been demonstrated for repeated measures of cervical exion force obtained during maximum voluntary contractions using this device.16 Experimental procedure Subjects were positioned comfortably lying supine and the subcutaneous tissue thickness overlying the SCM and AS muscles was measured. Subjects were asked to perform a gentle head lift manoeuvre to conrm accurate positioning of the ultrasound transducer over each muscle where electrodes would be positioned and the subcutaneous tissue thickness was measured. Whilst positioned lying supine, subjects were asked to cross their arms over their chest. The starting position was standardized by placing the cranio-cervical and cervical spine in a mid-position such that the subjects forehead and chin were basically in the horizontal plane and an imaginary line, which extended from the tragus of the ear to bisect the neck longitudinally, was parallel to the plinth.6, 17 The vertical height of the force-measuring apparatus could be adjusted as required to achieve this position. Each subject performed three maximal isometric cervical exion contractions of 3 s duration. Verbal encouragement was provided to motivate the
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Neuromuscular eciency in patients with chronic neck pain with age and gender as covariates. The NME and MVC data did not conform to a normal distribution therefore log transformations were used prior to statistical analysis. Analysis of co-variance was used to identify whether between group dierences existed for the MVC and NME of SCM and AS at 25 and 50% MVC. Analysis of variance was used to identify whether dierences in subcutaneous tissue thickness existed between the two groups. All statistical analyses were performed using SPSS 10.0 for Windows. A value of p 5 0.05 was used as an indicator of statistical signicance. Results Table 1 presents the descriptive statistics for duration of pain, average intensity of pain rated on the NRS and perceived level of disability measured with the NDI for the neck pain group. There were no signicant dierences between groups for the subcutaneous tissue thickness measured over the SCM ((R): p = 0.642, (L): p = 0.623) and AS muscles ((R): p = 0.621, (L): p = 0.562). The MVCs recorded in the two groups were not statistically dierent (control subjects, 73.3 + 37.7 N; neck pain patients 66.9 + 18.1 N; p = 0.75). Table 2 presents the group neuromuscular eciency values (N/mV) (mean and 95% condence intervals) for the SCM and AS muscles. Between-group signicant dierences were identied for the NME of SCM (p 5 0.05) and AS (p 5 0.01) muscles contracting at 25% MVC. No significant dierence was identied between groups for the NME of SCM or AS contracting at 50% MVC (gure 2). Discussion This study identied less neuromuscular eciency for the SCM and AS muscles contracting at 25% MVC in the neck pain group. This result supports previous research, which has demonstrated a trend towards less NME of SCM and AS during sub-maximal cervical exion contractions in patients with neck pain.8, 9 Dierences in subcutaneous tissue thickness between groups can be a drawback associated with the assessment of NME9 however, no dierences in subcutaneous tissue thickness were present between the two subject groups in this study and therefore this factor did not bias our results. Reduced SCM and AS NME indicates that patients with neck pain required greater muscular electrical activity to produce an equivalent amount of force as compared to the asymptomatic subjects, or conversely, with a comparable amount of electrical activity, neck pain patients would produce a lower force output. The greater SCM and AS EMG activity recorded for the neck pain group could theoretically be attributed to (1) greater excitability of the motoneuronal pool, (2) modication of neural activation patterns accommodating for weakness or inhibition of another muscle, or (3) a combination of these mechanisms.

Table 1 Descriptive statistics for the patients with neck pain (n = 20). Duration of symptoms, average intensity of pain rated on numerical rating scales (NRS) and subjects perceived level of disability measured with the Neck Disability Index (NDI, score out of 50) Symptom Duration of pain (years) Average intensity of pain (NRS) NDI Mean + SD 5.2 + 3.2 5.0 + 1.9 11.5 + 3.3 Range 1.0 13.0 2.0 8.5 6.0 18.0

Table 2 Dierences between the mean and 95% condence intervals for the neuromuscular eciency (anti-log values) of the sternocleidomastoid (SCM) and anterior scalene (AS) muscles contracting at 25% and 50% of the maximum voluntary contraction (MVC) between neck pain patients and controls Control AS 25% MVC SCM 25% MVC AS 50% MVC SCM 50% MVC 1.101 (0.774 0.835) 0.792 (0.611 0.975) 0.587 (0.461 0.717) 0.438 (0.346 0.555) Patient 0.675 (0.543 0.839) 0.517 (0.399 0.671) 0.475 (0.381 0.593) 0.354 (0.280 0.449) P level 0.008 0.024 0.225 0.214

Figure 2 The mean and 95% condence intervals for the neuromuscular eciency (NME) of sternocleidomastoid (SCM) and anterior scalene (AS) muscles contracting at 25 and 50% of the maximum voluntary contraction (MVC). Signicantly less NME was identied for the SCM and AS at 25%MVC for the neck pain group. * indicates p 5 0.05.

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D. Falla et al. Nociceptive input can alter motoneuron pool net excitability, which in turn can modify motor unit recruitment and EMG amplitude.21 As summarized by Sjolander et al.,22 excitation of aerents from mechanoreceptors and nociceptors of cervical ligaments or joint capsules together with inammatory activation of chemosensitive nerve endings in injured cervical joints and/or muscles could increase the activation of the alpha motoneuron pool thus increasing reex-mediated muscle stiness.22 According to this theory, increased muscle stiness equates to increased resistance of a muscle to stretch,22 an observation commonly identied clinically in the supercial cervical muscles of patients with neck pain.23 Increased muscle stiness results in reduced muscle blood ow, which subsequently results in an accumulation of ions and metabolites.22 Accretion of metabolites within muscles further excites chemosensitive muscle aerents, which in turn results in additional excitation of the g-muscle spindle system and alpha motoneurons via reex actions on the g-motoneurons.22, 24 27 Larsson et al.28 identied lowered microcirculation in the upper trapezius muscle on the side of greatest pain compared to the less painful side in patients with chronic neck pain associated with trapezius myalgia, which supports this theory. Furthermore, greater upper trapezius EMG amplitude was recorded ipsilateral to the side of greatest pain during high intensity contractions. The microcirculation of the upper trapezius muscle was also signicantly reduced in the neck pain group compared to asymptomatic subjects. Moreover, the patient group demonstrated greater localized muscle fatigue characterized by greater modication of the mean spectral frequency of the EMG signal and a trend towards higher EMG activity. It was hypothesized that detection of increased EMG activity may indicate increased muscle tension secondary to impaired muscle microcirculation.28 Similar studies investigating the microcirculation of the SCM and AS muscles in patients with neck pain have not been conducted. However, greater myoelectric manifestations of SCM and AS muscle fatigue have been previously demonstrated in patients with neck pain characterized by greater initial values and slope of the mean spectral frequency compared to asymptomatic subjects.9 As known, lactate production and accumulation is considered one of the contributing factors for the decline in the conduction velocity and consequently the mean frequency during sustained isometric contractions.29 The second possible explanation for the results identied in this study is an alteration of neural activation
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patterns to compensate for inhibition or weakness of another muscle. As summarized by Edgerton and colleagues,21 some muscles can display reduced EMG activity whilst synergistic muscles are recruited to compensate for this weakness resulting in an abnormally high level of motoneuron activity. This compensation produces modications in the neural strategies of recruitment of motoneuron pools among muscles having comparable functions when completing prescribed motor tasks.21 In previous studies, patients with neck pain demonstrated impaired performance during a low load cranio-cervical exion taskthe anatomical action of the deep cervical exor muscles.6, 30 Neck pain patients demonstrated reduced deep cervical exor EMG with performance of this task and a reduced ability to hold progressively inner range positions of cranio-cervical exion,31 which has been shown to be associated with greater SCM EMG amplitude compared to control subjects.6, 32 It was hypothesized that the greater SCM EMG may represent a compensatory strategy for deep cervical muscle dysfunction.6 The greater EMG activity of the SCM and AS muscles identied for the neck pain group in this study may represent another measure of an altered muscle strategy to compensate for dysfunction in deep cervical exor muscles. It is notable that while the NME of the SCM and AS muscles was signicantly reduced at 25% MVC, there was no evidence to indicate less NME of the SCM and AS contracting at 50% MVC in the neck pain group. This result may reect greater problems in the muscles tonic system. There is some indication from muscle biopsy studies to suggest a relative loss of type I bres and increase of type II bres in the neck muscles of neck pain patients.33 This observation may provide some explanation for the dierential results identied between the two contraction forces. Alternatively, contractions at 25% MVC are more likely to reect loads on the cervical muscles that are commonly encountered functionally. The cervical exor muscles may be expected to contract ineciently in asymptomatic subjects at loads equivalent to 50% MVC or greater. Conclusion Patients with neck pain demonstrated less NME of the SCM and AS muscles at 25% MVC. Reduced NME in the supercial cervical exor muscles in patients with neck pain may be a measurable altered muscle strategy for dysfunction in other muscles. This aberrant pattern of muscle activation appears to be most detectable under conditions of low load. NME, when measured at 25% MVC, may be a useful objective

Neuromuscular eciency in patients with chronic neck pain measure for future investigation of muscle dysfunction in patients with neck pain.
16 Falla D, DallAlba P, Rainoldi A, Merletti R, Jull G. Repeatability of surface EMG variables in the sternocleidomastoid and anterior scalene muscles. European Journal of Applied Physiology 2002; 87: 542 549. 17 Falla D, Campbell C, Fagan A, Thompson D, Jull G. The relationship between upper cervical exion range of motion and pressure change during the cranio-cervical exion test. Manual Therapy 2003; 8: 92 96. 18 Hermens H J, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensor and sensor placement procedures. Journal of Electromyography and Kinesiology 2000; 5: 361 374. 19 Falla D, DallAlba P, Rainoldi A, Merletti R, Jull G. Identication of innervation zones of sternocleidomastoid and scalene Muscles: A basis for clinical and research electromyography applications. Clinical Neurophysiology 2002; 113: 57 63. 20 Bergamo R, Gazzoni M, Farina D, et al. Multichannel surface EMG of muscles of the hand and forearm. Proceedings of the Symposium on Muscular Disorders in Computer Users: Mechanism and model. Copenhagen, 1999; 198 202. 21 Edgerton VR, Wolf SL, Levendowski DJ, Roy RR. Theoretical basis for patterning EMG amplitudes to assess muscle dysfunction. Medicine and Science in Sports and Exercise 1996; 28: 744 751. 22 Sjolander P, Johansson H, Djupsjobacka M. Spinal and supraspinal eects of activity in ligament aerents. Journal of Electromyography and Kinesiology 2002; 12: 167 176. 23 Janda V. Muscles and motor control in cervicogenic disorders: Assessment and Management. In: R Grant (ed) Physical therapy of the cervical and thoracic spine. 2nd edn. New York: Churchill Livingstone, 1994; 195 216. 24 Djupsjobacka M, Johansson H, Bergenheim M. Inuences on the gamma-muscle spindle system from muscle aerents stimulated by increased intramuscular concentrations of arachidonic acid. Brain Research 1994; 663: 293 302. 25 Johansson H, Djupsjobacka M, Sjolander P. Inuences on the gamma-muscle spindle system from muscle aerents stimulated by KCl and lactic acid. Neuroscience Research 1993; 16: 49 57. 26 Johansson H, Sjolander P, Sojka P. Receptors in the knee joint ligaments and their role in the biomechanics of the joint. Critical Reviews in Biomedical Engineering 1991; 18: 341 368. 27 Wenngren BJ, Pederson J, Sjolander P, Bergenheim M, Johansson H. Bradykinin and muscle stretch alter contralateral cat neck muscle spindle output. Neuroscience Research 1998; 32: 119 129. 28 Larsson R, Oberg PA, Larsson SE. Changes of trapezius muscle blood ow and electromyography in chronic neck pain due to trapezius myalgia. Pain 1999; 79: 45 50. 29 Brody LR, Pollock MT, Roy S, Cj DL, Celli B. pH-induced eects on median frequency and conduction velocity of the myoelectric signal. Journal of Applied Physiology 1991; 71: 1878 1885. 30 Jull G, Barrett C, Magee R, Ho P. Further clinical clarication of the muscle dysfunction in cervical headache. Cephalalgia 1999; 19: 179 185. 31 Falla D, Jull G, Hodges P. Neck pain patients demonstrate reduced activation of the deep neck exor muscles during performance of the cranio-cervical exion test. Spine 2004 (in press). 32 Sterling M, Jull G, Wright A. Cervical mobilisation: concurrent eects on pain, sympathetic nervous system activity and motor activity. Manual Therapy 2001; 6: 72 81. 33 Uhlig Y, Weber BR, Grob D, Muntener M. Fiber composition and ber transformations in neck muscles of patients with dysfunction of the cervical spine. Journal of Orthopaedic Research 1995; 13: 240 249.

Acknowledgements This study was supported by a University of Queensland Small Grant.

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