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Changes in motor behavior are a known feature of chronic mechanical neck pain disorders. A significant positive association was observed between superficial muscle activity and pain intensity (P 0.003) strongest relationship between pain intensity and superficial muscle activity occurred at the final increment of the cranio-cervical flexion test (inner-range test position) for both the SCM and AS muscles (R 2 1 / 4 0.16)
Changes in motor behavior are a known feature of chronic mechanical neck pain disorders. A significant positive association was observed between superficial muscle activity and pain intensity (P 0.003) strongest relationship between pain intensity and superficial muscle activity occurred at the final increment of the cranio-cervical flexion test (inner-range test position) for both the SCM and AS muscles (R 2 1 / 4 0.16)
Changes in motor behavior are a known feature of chronic mechanical neck pain disorders. A significant positive association was observed between superficial muscle activity and pain intensity (P 0.003) strongest relationship between pain intensity and superficial muscle activity occurred at the final increment of the cranio-cervical flexion test (inner-range test position) for both the SCM and AS muscles (R 2 1 / 4 0.16)
The relationship between supercial muscle activity during the cranio-cervical
exion test and clinical features in patients with chronic neck pain Shaun OLeary a, b, * , Deborah Falla c, d , Gwendolen Jull a a NHMRC Centre for Clinical Research Excellence in Spinal Pain, Injury and Health, The University of Queensland, Brisbane, Australia b Physiotherapy Department, Royal Brisbane and Womens Hospital, Brisbane, Australia c Pain Clinic, Center for Anesthesiology, Emergency and Intensive Care Medicine, University Hospital Gttingen, Gttingen, Germany d Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Gttingen, Georg-August University, Gttingen, Germany a r t i c l e i n f o Article history: Received 6 October 2010 Received in revised form 9 December 2010 Accepted 11 February 2011 Keywords: Neck pain Electromyography Cervical exors a b s t r a c t Changes in motor behavior are a known feature of chronic mechanical neck pain disorders. This study examined the strength of the association between reported levels of pain and disability from 84 indi- viduals (63 women, 21 men) with chronic mechanical neck pain and levels of electromyographic activity recorded from supercial cervical exor (sternocleidomastoid; SCM and anterior scalene; AS) muscles during progressive stages of the cranio-cervical exion muscle test. A signicant positive association was observed between supercial muscle activity and pain intensity (P < 0.003), but not pain duration (P > 0.5) or perceived disability (P > 0.21). The strongest relationship between pain intensity and supercial muscle activity occurred at the nal increment of the cranio-cervical exion test (inner-range test position) for both the SCM and AS muscles (R 2 0.16). Although a positive and signicant rela- tionship between pain intensity and supercial muscle activity was shown, the relationship was only modest (16% explained variance), indicating that multiple factors contribute to the altered motor func- tion observed in individuals with chronic mechanical neck pain. 2011 Elsevier Ltd. All rights reserved. 1. Introduction Chronic mechanical neck pain (CMNP) is a nonspecic disorder that is characteristically aggravated by neck movement and activity (Bogduk, 1984) with a course marked by periods of remission and exacerbation (Cote et al., 2004). During any 6-month period 54% of adults suffer from CMNP (Cote et al., 1998) and only 6.3% of indi- viduals who suffered fromneck pain in the previous year are free of recurrence (Picavet andSchouten, 2003). It has beenspeculatedthat aberrant cervical motor behavior may contribute to the persistence of CMNPdue tofactors suchas the perpetual mechanical irritationof cervical structures and muscle fatigue (Panjabi, 1992; Jull et al., 2008b; Madeleine, 2010). Certainly within the literature there is mounting evidence of an association between CMNP and altered neuromuscular control (OLeary et al., 2009; Madeleine, 2010). One aspect of altered neuromuscular control that has been shown to be characteristic of CMNP is heightened activity of the supercial cervical exor muscles, namely the sternocleidomastoid and anterior scalene muscles. Elevated activity of these muscles has been observed in participants with neck pain during repetitive upper limbs tasks, (Falla et al., 2004a) as well as during specic muscle tests of cervical motor performance. In particular, height- ened activity of these muscles in individuals with neck pain compared to healthy controls have been reported in multiple studies that have utilized the Cranio-Cervical Flexion Test (CCFT) (Falla et al., 2004b; Jull et al., 2004b, 2007), which is a lowintensity graded test of cervical exor muscle performance (Jull et al., 2008a). Several reasoned hypotheses have been offered as to the underlying cause of the heightened activity of these supercial muscles. These hypotheses include factors such as compensatory mechanisms for coinciding decits in deep cervical exor function (Falla et al., 2004b), changes in muscle spindle sensitivity through sympa- thetic activation (Passatore and Roatta, 2006), reex-mediated adaptation of motor neuron discharges to pain (Sohn et al., 2000; Farina et al., 2004), alterations in cortical excitability and changes in the descending drive to muscles (Le Pera et al., 2001) as well as psychological distress (Bansevicius and Sjaastad, 1996; Nilsen et al., 2006). At this stage the exact mechanismunderlying the changes in * Corresponding author. NHMRC Centre for Clinical Research Excellence in Spinal Pain, Injury and Health, The University of Queensland, Brisbane, Australia. Tel.: 61 7 3636 2290; fax: 61 7 3365 2775. E-mail address: shaun_oleary@health.qld.gov.au (S. OLeary). Contents lists available at ScienceDirect Manual Therapy j ournal homepage: www. el sevi er. com/ mat h 1356-689X/$ e see front matter 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.math.2011.02.008 Manual Therapy 16 (2011) 452e455 neuromuscular control in relation to CMNP are unclear and are most likely multifaceted. What is also unclear is the relationship between changes in neuromuscular control and the severity of patient-reported sym- ptoms. While some studies infer a relationship between altered levels of muscle activation and discomfort in cervical spine disor- ders (Szeto et al., 2005; stensvik et al., 2009), there is generally a lack of studies examining the strength of the relationship between clinical symptoms and altered muscle activity. The purpose of this study was to examine the magnitude of the rela- tionship between reported levels of neck pain and disability and activation of the supercial cervical exor muscles during the CCFT inpatients with CMNP. It is anticipated that the ndings will further clarify the relationship between clinical symptoms and physical ndings in the assessment of CMNP that will further inform deci- sion making in the clinical management of this condition. 2. Methods 2.1. Design This was a cohort study utilizing individual participant data fromtwo previous trials conducted in our laboratory (OLeary et al., 2008; Jull et al., 2009). 2.2. Subjects Eighty-four volunteers (63women) withCMNP(age; meanSD; 37.5 12.1 yrs) participated in the study. Participants were included if theywereagedbetween18and60years, reporteda historyof neck pain of greater than six months duration, scored 5 points or greater out of a possible 50 points on the Neck Disability Index (NDI) (Vernon, 1996), and demonstrated positive ndings on a physical examination of the cervical spine (altered joint motion and painful reactivity to palpation) (Jull, 1994). Participants were excluded if theyhadundergone anexercise programtoconditionthe muscles of their neck or shoulder girdle in the preceding six months, if they experienced neck pain or headache from non-musculoskeletal causes or demonstrated neurological signs. Participants were recruited from the University and general community. Ethical clearance for the study was granted by the Universitys Medical Research Ethics Committee and the study was conducted in accordance with the declaration of Helsinki. Informed consent was obtained from each subject. 2.3. Measurements and procedures Following inclusion into the study, participants completed self- reported measurements of neck pain and disability followed by the measurements of supercial cervical exor muscle activity during an isometric cranio-cervical exion task. 2.3.1. Self-reported measurements of neck pain and disability Visual Analogue Scale (VAS): Participants were asked to indicate their average neck pain intensity over the previous week by placing a mark on a 100 mm line bordered at one end by the words no pain and the other end by the words worst pain ever (Kelly, 2001). Neck Disability Index (NDI): The NDI is a 10-item questionnaire relating to daily activities and cervical spine related pain. Each item is scored from 0 to 5, and the total score out of 50 points is summated (MacDermid et al., 2009). Duration of Neck Pain (DUR): The duration of the patients painful symptoms was recorded in months. 2.3.2. Cranio-cervical exion test (CCFT) Bipolar surface EMGsignals were detected fromthe sternal head of the sternocleidomastoid (SCM) and anterior scalene (AS) muscles bilaterally during the CCFT in accordance with an estab- lished protocol (Jull et al., 2008a). Pairs of electrodes (Grass Tech- nologies) were positioned 20 mm apart over the SCM and AS following skin preparation and using guidelines for electrode placement (Falla et al., 2002). EMG data were bandpass ltered between 20 and 450 Hz and sampled at 2048 Hz (ASE16 amplier, LISiN Centro di Bioingegneria, Italy) and converted to digital form by a 12-bit analog-to-digital converter. A reference electrode was placed around the right wrist. The CCFT was conducted using the standard clinical protocol (Jull et al., 2008a). Subjects were comfortably positioned in supine, crook lying with the head and neck in a mid-position and were instructed to perform a cranio-cervical exion action (anatomical action of the deep cervical exors). The task consisted of ve incremental movements of increasing cranio-cervical exion range of motion. Performance was guided by visual feedback from an air- lled pressure sensor (Stabilizer, Chattanooga Group Inc. USA) which was placed sub-occipitally behind the subjects neck and inated to a baseline pressure of 20 mmHg. The pressure sensor monitors the slight attening of the neck which occurs with the contraction of the longus capitis and longus colli muscles (Mayoux Benhamou et al., 1994). During the test, subjects were required to perform the gentle nodding motions of cranio-cervical exion that progressed in range to increase the pressure by ve incremental levels, with each increment representing 2 mmHg (22e30 mmHg). Subjects practiced targeting the ve test levels between 22 and 30 mmHg in two practice trials before the electrodes were applied. Following the application of electrodes participants performed a standardized manoeuvre for EMG normalization (reference voluntary contraction). This reference voluntary contraction inv- olved a head lift (cervical and cranio-cervical exion) just clear of the bed which was maintained for 10 s during which EMG data was recorded. One minute rest period was given before participants then performed the experimental CCFT condition during which EMG data was recorded. The experimental CCFT condition included all ve stages of the test (22e30 mmHg) with participants ins- tructed to maintain the pressure steady on each stage target for 10 s, and resting for 30 s between stages. For each of the incre- mental pressure levels tested, recording of EMG data commenced when it was observed by the investigator that the participant had reached the pressure target. A consistent starting point for each level tested was attained by ensuring the participant had returned to the neutral head/neck position which corresponded to the pre- ssure level reading of 20 mmHg. 2.4. Data management and statistical analysis To obtain a measure of EMG signal amplitude, the root mean square (RMS) of the EMGwas calculated fromintervals of 1 s during the 10 s contractions. The values of RMS were expressed as a per- centage of the maximumRMS value during the reference voluntary contraction (head lift). Because the RMS values for the left and right SCM or AS muscles did not differ statistically, the data were aver- aged across sides. Associations between changes in EMG RMS recorded from the SCM and AS muscles during the cranio-cervical exion test (5 factors: 22, 24, 26, 28, 30 mmHg increments) and pain and disability characteristics (VAS, DUR, NDI) were investigated using a repeated-measures ANOVA. Signicant associations between pain and disability characteristics and EMG RMS were the further eval- uated using multiple regression analyses which were performed S. OLeary et al. / Manual Therapy 16 (2011) 452e455 453 separately for the SCM and AS muscles. Signicance was set at P < 0.05. 3. Results Pain and disability characteristics (average standard devia- tion, range) of participants included a VAS score of 3.7 1.8, 0.9e9)/ 10 mm, an NDI score of 10.6 2.4, 5e16)/50 points, and a duration of symptoms of 7.6 6.9, 0.5e40) years. A signicant association was observed between the changes in SCM RMS recorded during the 5 stages of the test and the VAS measure (P < 0.001) but not the DUR (P 0.52) or NDI (P 0.67) measures. Similarly, changes in the AS RMS during the test showed a signicant association with the VAS measure (P 0.002) but not the DUR (P 0.82) or NDI (P 0.23) measures. As shown in Table 1, the regression analysis indicated that although the VAS measure was signicantly related to the RMS values of both muscles (SCM, AS) for all 5 stages of the test (P < 0.04), the R 2 values were largest for the nal increment of the test (30 mmHg) for both the SCM and AS muscles (R 2 0.16) as depicted in Fig. 1. 4. Discussion Heightened activity of muscles is commonly reported in studies involving participants with CMNP (Szeto et al., 2005; stensvik et al., 2009). Multiple studies have shown CMNP to be associated with heightened activity of the supercial cervical exor muscles (sternocleidomastoid and anterior scalene) during the CCFT (Falla et al., 2004b; Jull et al., 2004b, 2007). This study has shown, that in participants with CMNP, the level of supercial cervical exor muscle activity during the CCFT bears a positive relationship with the level of reported pain intensity. As depicted in Fig. 1, higher magnitudes of supercial cervical exor activity during the CCFT were observed in those participants with higher levels of reported pain intensity. This relationship was signicant for both the sternocleidomastoid and anterior scalene muscles. Experimental studies suggest that the reorganization of neuromuscular control in CMNP such as those observed in this study, may reect compensatory neural strategies, redistributing loads between muscles to sustain motor and force output to ach- ieve a task such as the CCFT (Ge et al., 2005; Falla et al., 2007). Its considered that in the long term, these neuromuscular adaptations may contribute to the persistence of painful cervical disorders due to factors such as muscle fatigability and prolonged mechanical irritation of cervical structures (Panjabi, 1992; Falla and Farina, 2005; Jull et al., 2008b; Madeleine, 2010). Caution needs to be taken in interpreting the ndings of this study. Although the relationship between pain intensity and supercial muscle activity was signicant, pain intensity only accounted for up to 16% of supercial muscle activity during the CCFT (Table 1). It is apparent that pain intensity is not the only factor impacting on alterations of neuromuscular control of the neck in patients with CMNP, the underlying mechanisms of which are likely to be multifaceted. Furthermore these ndings are only relevant for supercial muscle activity during the CCFT. Additional studies will need to be performed before inferences can be made of the rela- tionship between supercial muscle activity and pain during other activities of the cervical spine andupper limb. Notwithstanding this, these ndings support the notion that heightened activity of supercial cervical exor muscles is associatedwithneckpainwhich has underpinned recommendations for cervical neuromuscular evaluation in the clinical management of neck pain (Jull et al., 2004a). Furthermore the ndings lend support to clinical recom- mendations for minimizing supercial muscle activity when training cranio-cervical exion in the management of individuals with CMNP (Jull et al., 2008b). In contrast to the ndings for pain intensity, there was no relationship between supercial cervical exor activity during the CCFT and the duration of neck pain or the level of neck disability as measured using the NDI. The lack of correlation between muscle activity and duration of symptoms is not surprising. Previous studies have shown that heightened activity of the supercial cervical exor muscles occurs quickly (within 1 month) in patients with a whiplash injury following a motor vehicle accident (Sterling et al., 2003). Furthermore, increased activity of the sternocleido- mastoid has been observed immediately in healthy volunteers following physiological sympathetic activation elicited by the cold pressor test (Boudreau et al., 2010). Similarly, studies investigating experimentally induced muscle pain in healthy volunteers have shown immediate changes in neuromuscular control of the cervical spine, although the direction of response (increase or decrease in muscle activity) is variable and task-dependent (Falla et al., 2007). Table 1 Regression analysis results (B, P, and R 2 values) indicating the relationship between measures of pain intensity (Visual Analogue Scale) and normalized root mean square values for both the sternocleidomastoid and anterior scalene muscles. Sternocleidomastoid Anterior Scalene B P R 2 B P R 2 22 mmHg 0.05 0.02 0.07 0.04 0.03 0.06 24 mmHg 0.03 0.01 0.08 0.04 <0.001 0.14 26 mmHg 0.03 0.001 0.12 0.03 0.001 0.13 28 mmHg 0.02 0.002 0.11 0.02 0.002 0.11 30 mmHg 0.02 <0.001 0.16 0.02 <0.001 0.16 Fig. 1. Scatter plot of pain visual analogue scale (VAS) values and normalized root mean square values for the anterior scalene (A) and sternocleidomastoid (B) muscles recorded during the nal stage of the cranio-cervical exion test (30 mmHg). S. OLeary et al. / Manual Therapy 16 (2011) 452e455 454 It should be noted that the ndings of this study only relate to sternocleidomastoid and anterior scalene muscle activity. For a comprehensive evaluation of the relationship between painful symptoms and neuromuscular dysfunction, further studies need to evaluate other cervical muscles inpatients with neck pain. Similarly only one measure of pain intensity (average pain intensity over the previous week) was utilized in this study, future studies may wish to consider other pain intensity ratings (current, best, worst over the past 24 h) (Cleland et al., 2008) by which to examine the rel- ationship with physical ndings such as muscle activity. Further- more results can only be inferred for chronic neck pain of an insidious onset and not for neck pain of a traumatic onset such as that experienced by individuals with a whiplash injury. 5. Conclusion The ndings of this study support a relationship between neck pain and altered neuromuscular function. This study has shown that the magnitude of supercial muscle activity during the CCFT is related to the level of patient-reported pain intensity, not the duration of painful symptoms or the level of patient-reported neck disability. Although the relationship between supercial muscle activity and pain intensity was statistically signicant, it should be noted that the relationship was only modest and probably reects that there are multifaceted contributors to altered neuromuscular function associated with chronic mechanical neck pain. 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