IMPAIRMENT IN MUSCLE function is a feature of chronic

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1 929 ORIGINAL ARTICLE Is There Altered Activity of the Extensor Muscles in Chronic Mechanical Neck Pain? A Functional Magnetic Resonance Imaging Study Shaun O Leary, PT, PhD, Barbara Cagnie, PT, PhD, Ashton Reeve, BSc, Gwendolen Jull, PT, PhD, James M. Elliott, PT, PhD ABSTRACT. O Leary S, Cagnie B, Reeve A, Jull G, Elliott JM. Is there altered activity of the extensor muscles in chronic mechanical neck pain? A functional magnetic resonance imaging study. Arch Phys Med Rehabil 2011;92: Objective: To compare the pattern of neck extensor muscle use in participants with chronic mechanical neck pain to that of healthy controls during 2 different extension exercises by use of muscle functional magnetic resonance imaging (mfmri). Design: Cross-sectional. Setting: University laboratory. Participants: Data recorded from subjects with chronic mechanical neck pain (n 12; 10 women, 2 men) were compared with previously recorded data from healthy subjects (n 11; 7 men, 4 women). Interventions: Not applicable. Main Outcome Measures: mfmri measures of shifts in T2 relaxation were made for the multifidus, semispinalis cervicis, semispinalis capitis, and splenius capitis muscles, at C2-3, C5-6, and C7-T1 levels, prior and immediately after 2 different exercises: cervical extension in craniocervical neutral (CCN) and cervical extension in craniocervical extension. T2 shift values (difference between pre- and postexercise T2 relaxation values) for each muscle and exercise condition were used for analysis. Results: While there were observed differences in differential activation of the extensor muscles in participants with mechanical neck pain compared with controls, these differences were only evident for the CCN exercise condition and were only observed for 3 out of the 7 muscle regions of interest during this exercise. Conclusions: Results of this study suggest some alteration in the differential activation of the cervical extensors in patients with mechanical neck pain and indicate that further investigation of this muscle group in mechanical neck pain disorders is warranted. Key Words: Cervical vertebrae; Exercise; Magnetic resonance imaging; Rehabilitation by the American Congress of Rehabilitation Medicine IMPAIRMENT IN MUSCLE function is a feature of chronic mechanical neck pain and has been implicated as a significant factor in the maintenance of this disorder that is characterized by periods of remission and exacerbation. 1 Impairments of the cervical extensor muscles have been identified in patients with mechanical neck pain disorders 2-6 and exercise to train and improve their performance is advocated in management. 7 However, there is a paucity of studies investigating their role in mechanical neck pain. Further information on the topic could be useful to better inform decision making in the clinical management of neck pain. Studies investigating the neck extensor muscles in patients with mechanical neck pain have observed changes in their physical structure, including alterations in cross-sectional area, 3,5,8 and changes in fiber type. 9 Studies have also identified deficiencies in extensor muscle strength 10,11 and endurance 12,13 in patients with neck pain compared with healthy subjects. However, while clinical evidence exists for the flexors, 14,15 there has been little exploration into the effect of painful neck disorders on the differential activation of the extensor muscles. Within the multiple layers of the cervical extensor muscle group, there is a distinct division between the superficial cervical muscles (splenius capitis [SpC] and semispinalis capitis [SCa]), which span the entire cervical spine and the deeper layered muscles (semispinalis cervicis [SCe] and the multifidus [Mul]), which span only the typical cervical vertebrae (C2-7). While imaging studies have attempted to quantify changes in cervical extensor muscle activity in response to exercise, 16,17 no studies to date have compared the activity patterns of the different cervical extensor muscles in patients with and without chronic mechanical neck pain disorders. It is therefore pertinent to compare the differential activity of the extensors in From the Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, Division of Physiotherapy (O Leary, Jull), the Centre for Advanced Imaging (Reeve, Elliott), and the Centre of National Research on Disability and Rehabilitation Medicine (Reeve, Elliott), The University of Queensland, Brisbane, QLD, Australia; the Physiotherapy Department, Royal Brisbane and Women s Hospital, Brisbane, QLD, Australia (O Leary); Department of Rehabilitation Sciences and Physiotherapy, Ghent University, Ghent, Belgium (Cagnie). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Reprint requests to Shaun O Leary, PT, PhD, Principal Research Fellow, Physiotherapy Dept, Royal Brisbane and Womens Hospital, Royal Brisbane Post Office, Brisbane, QLD, 4029 Australia, shaun_oleary@health.qld.gov.au. Published online April 29, 2011 at /11/ $36.00/0 doi: /j.apmr BMI CCE CCN mfmri MRI Mul MVC ROI SCa SCe SpC List of Abbreviations body mass index craniocervical extension craniocervical neutral muscle functional magnetic resonance imaging magnetic resonance imaging multifidus maximal voluntary contraction region of interest semispinalis capitis semispinalis cervicis splenius capitis

2 930 EXTENSOR ACTIVITY IN NECK PAIN, O Leary people with and without mechanical neck pain. Varied morphologic changes have been shown to occur in the presence of neck pain, 18 and it is thus plausible to also expect variable changes in motor output in the presence of pain. Muscle functional magnetic resonance imaging (mfmri) is a useful method to noninvasively evaluate muscle activity of multiple-layered cervical extensor muscles. 19 The mfmri method is based on an increase in T2 relaxation time of muscle water after exercise. Specifically, there is a slower decay of the muscle water signal in response to exercise, causing an enhancement in signal intensity of the activated muscles on T2-weighted images (appears brighter) that can be quantified. 20 Changes in the T2 value recorded from the pre- and postexercise image are calculated and referred to as the T2 shift permitting quantification of activity levels of specific muscles in response to exercise. Accordingly, T2 shift measures have shown to be concordant with other measures of muscle activity (eg, electromyography and dynamometry measures of force 24 ) and have shown high measurement reliability with intraclass correlation coefficients ranging from 0.87 to ,25,26 The purpose of this study was to compare the activity of the cervical extensor muscles in patients with mechanical neck pain to that of healthy controls during 2 different cervical exercise conditions using an mfmri method. We hypothesized that there would be evidence of altered activity of the multilayered extensor muscles in patients with mechanical neck pain compared with healthy controls. It was anticipated that the findings would enhance our understanding of motor impairments in mechanical neck pain disorders. METHODS Participants Twelve volunteers with chronic mechanical neck pain participated in the study including, 10 women (mean age SD, y) and 2 men (mean age SD, y). The group mean age SD was years and the group mean body mass index (BMI) SD was kg/m 2. Participants were recruited via advertising throughout the local community. Data for the 12 participants with mechanical neck pain were compared with data recorded from 11 healthy participants from our previous study using identical methodology. 19 The control group comprised 4 women (mean age SD, y) and 7 men (mean age SD, y) with a group mean age SD of years and group mean BMI SD of kg/m 2. Chronic mechanical neck pain was classified as persistent pain of 3 months or longer stemming from the cervical spine, with a neck disability index score of 10 points or more out of a possible 50 points, and signs of dysfunction (restrictions in mobility, pain provocation) on a physical examination of the cervical spine 27 performed by an experienced musculoskeletal physical therapist. Potential participants in both groups were excluded if they were outside the 18 to 55 years age bracket, experienced neck pain from a traumatic incident (eg, a whiplash injury), had known neurologic, metabolic, or systemic disorders, or had participated in any program of exercises designed to improve the performance of the cervical or shoulder girdle muscles in the previous 6 months. Participants were also excluded if they presented with any contraindications for magnetic resonance imaging (MRI) (eg, cardiac pacemaker, implanted or irremovable metals, claustrophobia, cochlear implant, or pregnancy). Three potential subjects from the mechanical neck pain group Fig 1. Dynamometry method used to perform the (A) cervical extension in CCN, and (B) cervical extension in CCE exercises. Reprinted from Elliott et al. 19 had to be excluded after initial assessment: 2 due to neurologic signs and 1 after divulging a previous neck trauma incident. The institutional medical ethics committee granted ethical approval. Written informed consent was obtained from all subjects prior to inclusion. Magnetic Resonance Imaging All procedures followed in this study have been published previously 19 but are described again briefly in this article. All images were acquired on a 1.5T scanner a with a flexible neck array coil from the manufacturer, which was used as the receiver coil. Subjects were instructed to lie supine and were positioned so that their cervical spine maintained a neutral position without rotation, lateral flexion, or exaggerated lordosis. This was determined visually by establishing a horizontal line from the forehead to the chin that remained parallel to the scanner bed. A pillow was placed under the knees for comfort. Three scans were performed on each patient: 1 at rest (baseline) and 1 after each of 2 exercise conditions. Each scanning procedure was identical. A sagittal localizing sequence was initially conducted to determine axial slice positions. Axial images with a slice thickness of 5mm were then acquired parallel to the C2-3, C5-6, and C7-T1 intervertebral disks. At each level, the Mul, SCe, SCa, and SpC muscles were investigated. A multi-spin echo sequence was used for T2 calculation: repetition time (TR) 2000 milliseconds; echo time (TE) 10 to milliseconds in steps of 10.1 milliseconds (totaling 16 echoes); field of view mm; matrix ; voxel size 2 2 5mm; total acquisition time 5 minutes 12 seconds. Exercise Protocol Exercises were performed in prone using a purpose built dynamometer (fig 1). Exercises were identical with respect to relative load (20% of maximal voluntary contraction (MVC)), repetitions (3 repetitions), duration (60s duration), and rest period between repetitions (30s rest period). The difference was the orientation of the craniocervical spine during the performance of the exercise. In this manner, the exercises performed in this study comprised: (1) cervical extension in craniocervical neutral (CCN) and (2) cervical extension in craniocervical extension (CCE). Cervical extension in CCN. Participants were positioned prone with their head and neck in a neutral position so that the mass of the head was supported by resting the chin on the end

3 EXTENSOR ACTIVITY IN NECK PAIN, O Leary 931 Table 1: T2 Values SD (ms) at Rest and After Each Exercise Condition (Cervical Extension in CCN, Cervical Extension in CCE) Calculated for All Muscles (Mul/SCe, SpC, SCa) and Levels in the Control 20 and MNP Group Muscle Group/ Vertebral Level Rest CECCN CECCE Controls MNP Controls MNP Controls MNP Mul/SCe C C C7-T SpC C C C7-T SCa C Abbreviations: CECCE, cervical extension in cranio-cervical extension; CECCN, cervical extension in cranio-cervical neutral; MNP, mechanical neck pain. of the plinth, which minimized activity of the cervical extensors between test repetitions (see fig 1A). The computer displaying the visual feedback of exercise intensity was positioned on the floor directly below their line of sight. The pad of the dynamometer was then lowered in contact with the external occipital protuberance. Participants were instructed to extend their neck by pushing the back of their head into the pad of the dynamometer. A neutral craniocervical posture was encouraged by instructing the participant to maintain visual focus on the display graph immediately below them. Cervical extension in CCE. Participants performed the same exercise maneuver as for the CCN exercise with the exception that the head/neck orientation was maintained in 15 of CCE (as indicated by an inclinometer attached to the participant s head) for the duration of the exercise (see fig 1B). The investigator manually assisted the participant into the correct degree of CCE immediately before the performance of each repetition. Maintenance of the extended craniocervical orientation was encouraged by the participant maintaining focus on the visual display, which was now positioned forward on the floor compared to its location during the CCN exercise. Procedure Participants attended a preliminary session 48 hours prior to the experimental session in order to establish their MVC values for both exercise conditions. The order of testing was alternated between participants. Testing consisted of a standardized warm-up, followed by 3 MVC trials with a rest period of 60 seconds between trials. The maximum recording of the 3 MVC trials was used as the MVC score for the experimental session. A 5-minute rest period was allowed between MVC trials for the CCN and CCE conditions. During the experimental session, each participant first underwent final screening by a medical practitioner to ensure MRI suitability before undergoing the baseline (rest) MRI scans. Immediately after the baseline scan, each participant performed the first of the 2 isometric extension exercises (identical order to that performed during MVC trials) directly outside the magnet room. The second MRI scan was performed immediately after completion of the first exercise session. The participant then rested for a minimum of 45 minutes before performing the second extension exercise. Immediately after, they underwent the third and final MRI scan. A rest period of at least 45 minutes was required to allow for the baseline recovery of the shifts in T2 relaxation. 28 Accurate performance of the required 20% MVC effort during both exercises was ensured via real time visual feedback of the contraction effort displayed on the computer screen. Participants were encouraged to completely relax their neck muscles during the rest periods between repetitions with their jaw and head supported on the padded edge of the bed. Data Processing All T2 shift calculations were performed on axial images using ImageJ. b The Mul, SCe, SCa, and SpC muscles were targeted at each of C2-3, C5-6, and C7-T1 levels. ROIs were developed around each of the muscles at each level, with 2 exceptions: (1) the SCa muscle could not be distinguished at the C5-6 or C7-T1 levels and no ROIs for this muscle at this level were included; and (2) the boundaries of the Mul and SCe muscles were not consistently separable and consequently, these muscles were grouped as 1 region of interest (ROI). Care was taken to avoid the inclusion of nonmuscular tissue (eg, fat, fascia, or blood vessels) in all ROIs. Sixteen echoes were used to calculate T2 values for each muscular ROI. Statistical Analysis Analysis was performed using the SPSS statistical software (version 18). c Descriptive statistics (mean SD) were calculated for demographic data and the mfmri measurements of T2 values (ms) at rest and after exercise for each muscle group. T2 shifts, defined as T2 values after exercise minus T2 values at rest, were used for statistical analysis. Group characteristics at baseline (age, BMI) and T2 values at rest were compared with an independent t test. A repeated-measures general linear model was used to evaluate group differences (mechanical neck pain, control) for the T2 shift measures recorded for both exercise conditions (CCN, CCE) at each of the muscles (Mul/SCe, SpC, SCa) at the respective levels evaluated (C2-3, C5-6, C7-T1) with a Bonferroni correction for multiple comparisons. To account for regional differences in muscles, separate models were used for each of the levels. Tests for simple effects were performed post hoc when indicated. Statistical significance was accepted at the 0.05 alpha level. RESULTS Table 1 displays the T2 values at rest and after exercise calculated for all muscles and levels in the chronic mechanical neck pain and healthy control groups. There were no significant differences in group characteristics at baseline (age, P 0.26; BMI, P 0.74) or in T2 values at rest between the control and mechanical neck pain group, except for the SpC muscle at the

4 932 EXTENSOR ACTIVITY IN NECK PAIN, O Leary Fig 2. Group mean T2 shift values (ms) (95% confidence interval error bars) after the (A) cervical extension in cranio-cervical neutral exercise, and (B) cervical extension in cranio-cervical extension exercise, conditions for all muscles (Mul/SCe, SpC, SCa), and levels in the control and mechanical neck pain group. *Significant group differences (P<.05) for the specific exercise condition. C7-T1 level (P 0.003). To account for this, the T2 rest values for the SpC muscle at the C7-T1 level were included as a covariate for analyses of this muscle at this level. Data for T2 shifts (mean 95% confidence interval) plotted by muscle, level, and group are shown in figure 2. Multifidus/Semispinalis Cervicis There was no significant main effect for group (P 0.11) for the Mul/SCe T2 shift values although the group exercise interaction approached significance (P 0.08). In response, post hoc tests were performed and demonstrated that T2 shift values recorded from the Mul/SCe muscles pre-post CCN exercise condition were significantly lower for the mechanical neck pain group at both the C5-6 (P 0.03) and C7-T1 level (P 0.04) when compared with the control group, whereas there were no significant differences at the C2-3 level (P 0.95) (see fig 2A). No significant between group differences in Mul/SCe muscle T2 shift values were observed for the CCE exercise condition (P 0.27) (see fig 2B). Splenius Capitis There was a significant main effect for group for the SpC muscle at the C7-T1 level (P 0.03), but not for the C2-3 or C5-6 levels (P 0.08). There was also a significant group exercise interaction at the C5-6 level (P 0.02), but not at the C2-3 or C7-T1 levels (P 0.48). Post hoc tests revealed the mechanical neck pain group to have significantly lower SpC muscle T2 shift values than the healthy controls at the C7-T1 level (P 0.03) in response to the CCN exercise, and in contrast displayed a nonsignificant trend for greater T2 shifts than healthy controls at the C2-3 level (P 0.07) (see fig 2A). No differences were observed at the C5-6 level (P 0.12). No significant between group differences in SpC muscle T2 shift values were observed for the CCE exercise condition (P 0.3) (see fig 2B). Semispinalis Capitis No significant main effects for group (P 0.71) or group exercise interaction (P 0.86) were observed for the SCa muscle T2 shift values. DISCUSSION This study suggests some alteration in the differential activation of the cervical extensor muscles in patients with mechanical neck pain in response to a cervical extension exercise compared with healthy controls using mfmri. The response, however, was dependent on the type of exercise performed. As indicated in figure 2, post hoc tests revealed that differences were only evident for the CCN exercise condition, and were only seen in 3 of the 7 muscle ROIs examined during the CCN exercise. When compared with healthy controls, the mechanical neck pain group recorded lower T2 shift values for the SpC muscles at C7-T1 and the Mul/SCe muscles at C5-6 and C7-T1, indicating some reduction in muscle activity at these lowermost levels measured (see fig 2A) in patients with mechanical neck pain. This only occurred during the CCN exercise condition. The findings observed in this study suggest that the differential activation of the cervical extensors in mechanical neck pain warrants further investigation in larger crosssectional studies to further define their role in mechanical neck pain. One interesting observation was the generalized reduced activity in muscles situated low in the cervical spine (Mul/SCe, C5-6, C7-T1; SpC, C7-T1) in the patients with mechanical neck pain compared with healthy controls when performing the CCN extension exercise (see fig 2A). As no group differences were noted for the CCE exercise, these differences may reflect the biomechanical properties of the CCN exercise. With the craniocervical region maintained in neutral during the exercise, pushing the back of the head into the resistive surface should induce extension moments focused toward the lower-cervical region in contrast to the upper-cervical region. 19 This perhaps exposes deficiencies of the muscles low in the cervical spine and may indicate that low-cervical extensor function may be an issue in some patients with mechanical neck pain. The tendency for reduced activity of the deep Mul/SCe extensor muscles in the mechanical neck pain group during the CCN exercise condition are consistent with reports of reduced deep cervical flexor muscle activity in patients with painful neck disorders 15,26 adding some weight to the body of evidence indicating dysfunction of the deep sleeve of muscles that envelope the cervical vertebral column (anterior and posterior) 29,30 in mechanical neck pain. The relevance of dysfunction of this muscular deep sleeve in mechanical neck pain is magnified when one considers that it is estimated that muscles account for approximately 80% of the mechanical stability of the cervical spine. 31 While mechanisms proposed to underlie changes in motor activity observed in painful cervical disorders (eg, changes in cortical excitability, 32 reflex-mediated responses, 33,34 sympathetic activation, 35 psychologic drivers 36,37 ) remain unclear, it is considered that aberrant motor behavior could result in mechanical irritation to sensitive cervical structures and muscular fatigue. 7,38-40 The findings of the study also suggest that as an assessment method, the CCN exercise may be a better approach than the

5 EXTENSOR ACTIVITY IN NECK PAIN, O Leary 933 CCE exercise for exposing deficiencies in extensor function in patients with mechanical neck pain. Accordingly, some patients with mechanical neck pain may need to retrain the function of these muscles by performing this exercise maneuver. No differences in T2 shifts were observed between the groups for the CCE exercise condition for any of the muscles examined (P 0.27). We demonstrated in a previous study that these 2 exercise conditions differ in muscle activation pattern with the CCE exercise inducing higher levels of SCa muscle activity in comparison to the CCN condition. Unfortunately, due to issues with image quality in this study, measures for T2 shifts for the SCa muscle at the C5-6 level were not available for the group with mechanical neck pain. Further studies are now required to establish whether these changes in muscle activation patterns observed in this study can be correlated to changes in other common elements of extensor muscle function, such as deficits in extensor strength and endurance Study Limitations There are some limitations to this study. One potential challenge with mfmri is that across subjects there may be considerable variability in the activity-dependent T2 response. We have minimized these issues by limiting our between-group analyses to within single muscles and within specific vertebral levels. Additionally, while validity studies have indicated a strong linear relationship between mfmri measures and other measures of muscle activity, such as electromyography and force, 24 the magnitude of T2 shift required to justify clinical significance is still not known. There was also a relatively small sample used in the study (due to the cost of MRI), which potentially may result in type 2 error. The men/women ratio was not similar in both groups; however, there was no effect of sex (P 0.40), which is in accordance with previous studies. 26 It should also be noted that conclusions based on this data can only be extrapolated to a population of patients with chronic insidious onset mechanical neck pain. Potential participants with a history of traumatic neck injury such as whiplashassociated disorders were excluded from this study. CONCLUSIONS In this study, mfmri recordings of T2 shifts induced in cervical extensor muscles were compared between participants with chronic nontraumatic mechanical neck pain and healthy controls after the performance of exercises for the neck extensor muscles. Compared with the healthy controls, less activity was observed in the Mul/SCe and SpC muscles low in the cervical spine during the CCN exercise condition. 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