Ultrasonographic Analysis of the Neck Flexor Muscles in Patients with Chronic Neck Pain and Changes After Cervical Spine Mobilization

ULTRASONOGRAPHIC ANALYSIS OF THE NECK FLEXOR MUSCLES IN PATIENTS WITH CHRONIC NECK PAIN AND CHANGES AFTER CERVICAL SPINE MOBILIZATION Fabianna R. Jesus-Moraleida, PT, MSc, a Paulo H. Ferreira, PT, PhD, b Leani S.M. Pereira, PT, PhD, c Cristiane M. Vasconcelos, PT, MSc, a and Manuela L. Ferreira, PT, PhD d

ABSTRACT Objective: The purpose of this study was to analyze changes in the recruitment of the muscles longus colli (Lco) and sternocledomastoid (SCM) as measured by ultrasonography in patients with chronic neck pain before and immediately after a single cervical Maitland's posterior-anterior central mobilization technique. Methods: This was a cross-sectional, case-control research design study. Ultrasonographic images of Lco and SCM were taken in 31 patients with chronic neck pain and matched controls during the 5 phases of the craniocervical flexion test before and after a Maitland's posterior-anterior central mobilization session at the cervical spine. Changes in muscle thickness during the test were calculated to infer muscle recruitment. Separate analysis of variance models for each muscle was built. Results: Both groups showed increases in Lco and SCM recruitment between phases (F = 7.95, P b .001; F = 21.29, P b .001), with patients with chronic neck pain demonstrating lesser increases for Lco changes in thickness compared with controls, mainly at phase 5 (−0.09, P = .004; 95% confidence interval [CI], 0.03-0.15). After the mobilization, Lco recruitment increased more significantly in patients with chronic neck pain, and previous difference between groups in phase 5 was no longer significant (−0.07, P = .07; 95% CI, −0.14 to 0.01). The SCM recruitment decreased in phase 1 for patients with chronic neck pain (P = .01; 95% CI, −0.06 to −0.01). Conclusion: Cervical mobilization appeared to modulate neck muscles function by increasing deep muscle and reducing superficial muscles recruitment. (J Manipulative Physiol Ther 2011;34:514-524) Key Indexing Terms: Neck Pain; Neck Muscles; Spinal Manipulation

a

PhD Candidate, Department of Physical Therapy, School of Physical Education, Physical Therapy and Occupational Therapy, Universidade Federal de Minas Gerais, Belo Horizonte MG, Brazil. b Lecturer, Discipline of Physiotherapy, Faculty of Health Sciences, The University of Sydney, Sydney, Australia. c Associate Professor, Department of Physical Therapy, School of Physical Education, Physical Therapy and Occupational Therapy, Universidade Federal de Minas Gerais, Belo Horizonte MG, Brazil. d Research Fellow, The George Institute for International Health, The University of Sydney, Sydney, Australia. This project was conducted at the Pain and Inflammation Rehabilitation Laboratory, Physical Therapy Department, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil, and was part of Fabianna R. Jesus-Moraleida's masters degree. Submit requests for reprints to: Paulo H. Ferreira, PT, PhD, 75 East st Lidcombe, PO Box 170 Lidcombe NSW, Australia 1825 (e-mail: [email protected]). Paper submitted April 6, 2011; in revised form June 6, 2011; accepted July 5, 2011. 0161-4754/$36.00 Copyright © 2011 by National University of Health Sciences. doi:10.1016/j.jmpt.2011.08.006

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eck pain is a common condition worldwide with an estimated lifetime prevalence of approximately 70%. 1 Most cases result in chronic pain, of which 5% develop high levels of pain and disability. 1 Work-related physical and psychosocial demands 2-4 are important risk factors for chronic neck pain, being these complaints associated with substantial health costs and work absenteeism. 5-8 Recent research shows that chronic neck pain sufferers present changes in the recruitment of the neck muscles. 9-12 Significant reductions in the recruitment, endurance, and delays in feedfoward activity of the deep cervical flexors (DCFs)—longus colli (Lco) and longus capitis (Lca)— have been associated with the persistence of neck pain and disabilitiy. 13-16 Thus, different approaches have been developed to assess and train DCF muscles, as an attempt to increase their ability to provide segmental support and stability to the neck. 17,18 Interventions aimed at altering DCF muscles recruitment have been found to be effective in chronic neck pain, and increases on the recruitment of these muscles have been found to be associated with

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improvements on postural control, pain, and disability level. 19-21 Spinal manipulative therapy (SMT), which include both manipulation and mobilization techniques of the spine, is a widely used treatment in patients with chronic neck pain, and it has been shown to reduce pain and disability in this population. 22-24 However, the exact mechanism of action explaining improvements in neck pain associated with SMT is still unclear. Although cervical SMT has been found to be associated with transitory reduction on upper limb motoneuron excitability 25 and improvements on upper limb muscles electromyography (EMG) activity, 26,27 data from neck muscle recruitment are scarce. It has been suggested that SMT could potentially be associated with changes in cervical flexor muscle recruitment. 28 Sterling et al 28 observed that cervical mobilization produced significant pain reduction, increased pressure pain threshold, sympathoexcitatory effects, increased skin conductance, and decreased activity of the cervical superficial flexor muscle sternocleidomastoid (SCM) during an upper cervical flexion task in patients with chronic neck pain when compared with placebo or control conditions. These findings have been used to hypothesize a facilitation effect of SMT on DCF activity via a central pain control mechanism evoked. 28 However, no studies investigating effects of SMT on DCF recruitment pattern have been identified. Objective and direct measures of DCF are required both in experimental and clinical settings to assess and train recruitment of these muscles as well as to examine the possible neuromuscular responses associated with treatment. Falla et al 29 have developed a protocol using EMG electrodes fixed via the nose to the posterior oropharyngeal wall to examine DCF activity. 10,29 Magnetic resonance imaging (MRI) has also been used to detect changes in a cross-sectional area of Lco, Lca, and SCM 30,31 in healthy participants. Nevertheless, these tools are neither easily accessible nor applicable to rehabilitation practice because of the invasiveness, costs, and need for special training. Ultrasonography is currently used as a measurement of trunk muscle recruitment during static and dynamic tasks. 32-34 It offers the advantage of being accessible, practical, less costly, and yet reliable and valid, particularly for deep layer muscles under low isometric submaximal contractions. 33 Although ultrasonography is frequently the instrument of choice to assess trunk muscle recruitment, 34-37 there are only few studies using this tool to assess deep cervical extensors in neck pain patients 38,39 and Lco changes in thickness in asymptomatic volunteers. 40,41 Jesus et al 41 developed a protocol using ultrasonographic measurement of muscle recruitment based on the craniocervical flexion test (CCFT) and have shown progressive changes in Lco and SCM thickness during the subsequent phases of the CCFT in asymptomatic people. 41

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Table 1. Demographic data for neck pain and control groups (N = 62) Sex Age, y Body mass, kg Height, cm NDI PPI

Neck pain (n = 31)

Control (n = 31)

P

26 women, 5 men 29.65 (8.79) 62.78 (16.47) 166.9 (10.6) 9.77 (3.34) 1.23 (0.76)

26 women, 5 men 29.68 (9.01) 57.80 (9.98) 166.15 (8.4) N/A

NA .99 .16 .76 N/A N/A

Mean and SD are shown. N/A, not applicable; NDI, Neck Disability Index; PPI, Present Pain Index.

To our knowledge, there are no studies that have assessed the ability of ultrasound to discriminate asymptomatic patients and patients with neck pain or identify possible effects of therapeutic interventions such as cervical spine mobilization on neck flexor muscle recruitment. The aims of this study were to investigate 1. the test-retest reliability of an ultrasonography protocol used to measure the recruitment of Lco and SCM; 2. the changes in the recruitment of Lco and SCM measured by ultrasonography in patients with chronic neck pain and asymptomatic controls; and 3. the immediate effects of a single cervical spine Maitland's posterior-anterior central mobilization session on Lco and SCM recruitment in patients with chronic neck pain and asymptomatic controls.

METHODS Participants Thirty-one participants reporting chronic neck pain and 31 controls of similar age and same sex were recruited for this study. This sample size provided an 80% chance of detecting a difference of 8% in Lco thickness during the CCFT between groups at a 5% level of significance. The effect size of 8% in Lco thickness was based on the observed difference between participants with neck pain and controls from pilot data. Groups were similar for age, body mass, and height (Table 1). To be included in the comparison (control) group, participants had to be free from neck complaints at the time of the study and had no history of neck pain that restricted function or caused them to have time off work. Participants were excluded if they presented with any systemic neurologic disorder or incapacitating pain elsewhere in the spine or shoulders. Participants were included in the chronic neck pain (case) group if they had chronic and incapacitating nonspecific neck pain, defined as continuous or recurrent pain in the neck area lasting for at least 3 months without specific cause, with or without pain referral to the arm, and no signs of

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Fig 1. Ultrasound measurement of neck muscles recruitment. The location of the measurements are indicated in the right panel by the dashed lines. neurologic deficit. Only participants with a Neck Disability Index score equal or greater than 5/50 were included. 42 Patients with cervicogenic headache were included if they also presented with neck pain. Exclusion criteria for the chronic neck pain group were spinal and/or neck surgery in the past 12 months; a diagnosis of serious spine pathology (inflammatory spondyloarthropathies, fracture, or infection), neurologic deficit, or nerve root compromise (diagnosed by at least 2 positive tests of the following: reflex, dermatome, and myotome tests); a diagnosis of a systemic condition such as diabetes or immune system disorders that affect inert tissue; continuous use of analgesic or anti-inflammatory drugs during the 48 hours preceding the test; current or previous (up to 3 months before testing) participation in a neck treatment program; inability to tolerate a Maitland's grade III mobilization technique during data collection; and symptoms of depression as shown by a score equal or greater than 20/63 on the Beck Depression Inventory. 43 For descriptive purposes, disability and pain from the neck pain group were assessed using the Brazilian Portuguese version of the Neck Disability Index 44 and the McGill Pain Questionnaire, 45 respectively. Present Pain Index from McGill Pain Questionnaire was calculated. Ethical approval was granted by the Federal University of Minas Gerais Ethics Committee (ETIC 358/08), and written informed consent was obtained from all participants.

Ultrasonography Ultrasonographic analysis of the cervical muscle recruitment was performed using a protocol developed by Jesus et al. 41 In this protocol, ultrasonographic images are recorded for Lco and SCM both during resting and muscle contractions. The protocol has shown to detect increments in Lco and SCM recruitment levels in asymptomatic participants during the CCFT (F = 24.070, P b .001). 41

Recordings of Lco and SCM were made unilaterally (right side) using the Siemens Sonoline SL-1 Ultrasound (Bayswater Victoria, Australia). A 7.5-MHz transducer was positioned longitudinally in the anterior neck, in parallel with the trachea's orientation and approximately 5 cm from its midline, to allow proper visualization of the muscles being investigated, the right carotid artery, and the vertebral lamina (Fig 1).

Procedure Before the main study, intrarater reliability (intraclass correlation coefficient [ICC], 3.1) of ultrasonographic images for the Lco and SCM average cross-sectional values, at all test levels, was determined in 10 chronic neck pain group participants. Data were collected in 2 different sessions, 1 week apart. Intraclass correlation coefficient values for Lco muscle thickness across the 5 phases of the test ranged from 0.77 to 0.91, and for SCM, from 0.75 to 0.94, demonstrating excellent reliability. 46 Participants were positioned in supine with the knees bent and the arms lying along the trunk. The head and neck were placed in a standardized position so that the participant's forehead and chin were horizontal and in midposition. The pressure biofeedback unit (Chattanooga Group, Hixon, TN), a valid tool to assess and manage deep neck flexor recruitment dysfunction, 47 was placed suboccipitally and inflated to 20 mm Hg in resting. Participants were instructed to perform a nodding movement, representing the CCFT 47 in 5 incremental levels of pressure: 22, 24, 26, 28, and 30 mm Hg (phases 1, 2, 3, 4, and 5, respectively). Participants performed the action at each different level of pressure holding the target pressure for 10 seconds, with 30 seconds of rest between levels. Feedback of pressure level was provided via a manometer visible to the volunteer and to the therapist who instructed the participants (Fig 2). To guarantee the accuracy of the test, the examiner taught the

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Fig 2. Experimental setup. The locations of the ultrasound transducer and the pressure biofeedback unit are indicated by the numbers 1 and 2, respectively.

maneuver passively to each participant and also provided instructions about normal breathing pattern and positioning of the tongue (at the roof of the mouth) while performing the head action. Neck retraction, jaw protrusion, or visual increase in superficial muscle tenderness was verbally discouraged during data collection. 48

Data Analysis Ultrasonographic images were recorded by the assessor at the baseline resting phase and at the end of each successive stage. Images were then coded and randomly analyzed. A grid was placed over each image, and measures of muscle thickness were made at sites 1 and 3 cm for Lco and 1 and 2 cm to the right of the midline for the SCM. These locations were chosen based on the sites for best visualization and most consistent measurements for each muscle boundary, and their mean value was considered. Changes in thickness during the CCFT were expressed as a proportion of muscle thickness at rest, the result being an inference of muscle recruitment. 33

Cervical Spine Mobilization Session For this study, we selected a Maitland's cervical mobilization technique. After the performance of the CCFT, an experienced manual therapist applied a specific large amplitude (Maitland grade III) oscillatory mobilization technique to the spinous process of C5/6, being this cervical segment elected for all participants. Each participant was positioned in the same position as during CCFT, and the manual therapist stood at the end of the plinth,

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Fig 3. Mobilization session setup. The arrow indicates the posterior-anterior direction in which the manual therapist applies the central vertebral pressure. behind the participant's head, placing his hands at the segment elected and applying using his index fingers a posterior-anterior central pressure 49 to the articular pillar of C5/6 (Fig 3). The technique was repeated 3 times for 60 seconds with oscillations at 1 Hz, with a 1-minute interval between each. Although it is unlikely that C5/6 was the symptomatic level in all participants, we considered that the standardization of the technique was appropriate because literature reports that although attempts are made to focus the technique to a target segment, stress will be applied at different cervical segments as well, and movement will occur over several levels. 50 Moreover, Aquino et al 51 have shown that patients report significant decreases in pain even when mobilizing nonpainful spinal segments. Ultrasonographic images were recorded subsequently after the mobilization session.

Statistical Analysis Initially, ultrasonographic data were analyzed using a 2way analysis of variance (ANOVA) with between-factors being groups (participants with chronic neck pain vs controls) and within-factor being CCFT phases (1-5) using data from the pretreatment condition. Subsequently, to analyze the effect of the cervical spine mobilization session on the recruitment of neck muscles, we chose the most discriminatory phases of the CCFT for Lco and SCM muscles and built separate ANOVA models for each muscle, with within-factor being condition (pre– and post–cervical spine mobilization session) and betweenfactor being groups. Post hoc testing was undertaken with Fisher tests when significant main or interaction effects

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Fig 4. Mean and 95% CI for recruitment of the neck muscles measured by ultrasound. Results are expressed as proportion of baseline (changes in muscle thickness) for chronic neck pain patients (●) and controls (□).⁎P b .05. were identified. Statistical analysis was performed using Statistica software (version 7.0) (Statsoft Russia, Moscow, Russia), and α level was set at .05. Data were coded so that the statistician was blinded to group allocation.

RESULTS Changes in Muscle Recruitment During CCFT The mean and 95% confidence interval (CI) of Lco and SCM recruitment as a proportion of baseline values for participants with chronic neck pain and controls during the CCFT are shown in Figure 4. There was an increase in Lco and SCM thickness with each progressive CCFT phase in both groups (F = 7.95, P b .001; F = 21.29, P b .001). Main effects and interactions for each muscle are shown in Table 2. Longus colli mean and SD for percentage increase across all phases of CCFT were 0.09 (0.05) and 0.13 (0.06) for participants with chronic neck pain and controls, respectively (P = .006). For SCM, no difference between groups was observed, the percentage increase being 0.10 (0.09) and 0.09 (0.05) for patients with chronic neck pain and controls, respectively (P = .75).

Longus Colli Muscle Recruitment During the CCFT, a significant effect was observed for Lco change in thickness between participants with chronic neck pain and controls (F = 7.95, P b .001) and across all CCFT phases (F = 45.13, P b .001). Post hoc analysis revealed that when participants in the control group performed CCFT, there was a linear increase in Lco thickness with the incremental phases of the test (Fig 4). The most significant differences on mean proportion of Lco thickness (N0.05) were seen between phases 3 and 1 (0.08; P b .001; 95% CI, 0.05-0.11), 4 and 1 (0.13; P b .001; 95% CI, 0.03-0.08), 2 (0.10; P b .001; 95% CI, 0.07-0.12), and 5 and 1(0.17; P b .001; 95% CI, 0.15-

Table 2. Main effects and interactions for Lco and SCM comparison between groups and between phases Lco Main effect/interaction Group Phases Group phases ⁎

SCM

Fa

P

F

P

7.94 45.12 8.17

.001 ⁎ b.001 ⁎ b.001 ⁎

0.19 14.28 0.41

.67 b.001 ⁎ .80

a

Phases. ⁎ P b .05.

0.20), 2 (0.14; P b .001; 95% CI, 0.11-0.17), and 3 (0.10; P b .001; 95% CI, 0.02-0.08). In participants with chronic neck pain, there was also a linear but smaller increase in Lco thickness in comparison with those in the control group (Fig 4). Changes in mean proportion of Lco thickness were most significantly different between phases 4 and 1 (0.06; P b .001; 95% CI, 0.03-0.08) and between phases 5 and 1(0.08; P b .001; 95% CI, 0.05-0.11). Differences between groups were statistically significant (P b .05) at higher phases of the test (phases 4 and 5) with controls showing significantly higher recruitment values than participants with chronic neck pain. Mean proportion difference between controls and participants with chronic neck pain on phase 4 was 0.07 (P = .02; 95% CI, 0.01-0.13) and 0.09 on phase 5 (P = .004; 95% CI, 0.03-0.15).

Sternocledomastoid Muscle Recruitment No significant effects were observed for SCM recruitment between groups or interaction between phases and groups (Table 2). The ANOVA analysis only showed a significant effect across CCFT phases (F = 21.29; P b .001). For patients with chronic neck pain, the most significant differences were found between phases 5 and 1 (0.08; P b .001; 95% CI, 0.05-0.11), 2 (0.07; P b .001; 95% CI, 0.040.10), and 3 (0.06; P b .001; 95% CI, 0.03-0.09).

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Fig 5. Mean and 95% CI for recruitment of the neck muscles during phase 5 before and after the manual therapy procedure. Results are expressed as proportion of baseline (changes in muscle thickness) for chronic neck pain patients (●) and controls (□).⁎P b .05.

For controls, the most relevant differences in SCM proportion of thickness were found between phase 5 and 1 (0.10; P b .001; 95% CI, 0.06-0.13) and 2 (0.08; P b .001; 95% CI, 0.05-0.11).

information regarding Lco and SCM function using a feasible instrument that could potentially be used in the clinical setting both to assess and to provide feedback for training of neck muscles in patients with neck pain.

Changes in Recruitment After Cervical Spine Mobilization Session

Ultrasonography Measurement of Muscle Thickness Reliability

The most discriminatory phases of the CCFT for Lco and SCM were based on visual and quantitative analysis (Fig 4). For Lco, phase 5 was selected, and for SCM, phase 1 was the one chosen to investigate the effect of cervical spine mobilization session on neck muscles recruitment.

Longus colli Muscle Recruitment After the technique, no main effects were observed for phase 5 of the test (F = 1.17; P = .28). A main interaction was detected for groups (F = 9.25; P = .01). Longus colli recruitment was greater for controls than for patients with chronic neck pain on phase 5, but the identified betweengroup difference was no longer significant postintervention (P = .07; 95% CI, −0.14 to 0.01) (Fig 5).

Sternocledomastoid Muscle Recruitment After the mobilization technique, a main effect was found for pre- and postconditions recruitment for phase 1 (F = 5.09; P = .03). A significant decrease in recruitment in comparison with baseline was identified for participants with chronic neck pain (P = .01; 95% CI, −0.06 to −0.01) but not for controls.

DISCUSSION Results of the present study corroborate the evidence that patients with chronic neck pain have altered patterns of neck flexor muscle synergy. Our data also provide useful

Extensive assessment of the recruitment of deep neck flexors has been performed in patients with chronic neck pain and in healthy participants. 10 , 52-55 Several studies have been published using EMG activity of these muscles as a method of detecting dysfunctions related to these muscles in whiplash and mechanical neck pain sufferers. 13,15 In the present study, ultrasound imaging has been used as a noninvasive tool to measure muscle recruitment in patients with chronic neck pain. To our knowledge, this is the first study to document ultrasonographic changes in muscle thickness for Lco and SCM during CCFT. Test-retest intrarater reliability (ICC, 3.1) of the Lco and SCM thickness measurement across all CCFT phases was overall excellent (Lco, 0.77-0.91; SCM, 0.75-0.94). Cagnie et al 40 revealed poorer results when using ultrasonography to measure Lco cross-sectional area (ICC, 0.68-0.71). The authors argued that a single measurement of a muscle increases errors in its measurement, thus influencing the agreement of ultrasound images. On the other hand, Javanshir et al 56 observed better values for Lco anterior-posterior dimension reliability (ICC, 0.77). It should be noted that the protocol used in the aforementioned study was performed positioning the transducer perpendicular to the anterior neck, and it only measured ultrasonographic measures of Lco during the resting positioning of the muscle. In our study, we tested the reliability of both Lco and SCM thickness visualized by ultrasonography using average measures that are known to increase the reliability of a

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measurement and throughout all CCFT phases, in which both muscles are required to actively perform their actions.

Craniocervical Flexion Test Consistent with previous data, 17,29 our results showed that CCFT progressively challenges Lco and SCM muscles. The CCFT was developed by Jull et al, 47 aiming to be a low–load-specific test to assess and treat Lco and Lca impairments. The method was conceptualized based on the anatomical action of these muscles, 57 and it has been shown that individuals with neck pain and cervicogenic headache have poor performance of the test. 47 In our previous study, 41 we developed a protocol to detect changes specifically in Lco thickness across stages of the test. In asymptomatic volunteers, the mean change in Lco thickness across the phases of the test was 14%. Our present study showed similar results, with Lco mean change in thickness from resting being 13%. A recent study 40 has tested the validity of a protocol using a realtime ultrasound with a 12-MHz transducer positioned parallel to trachea's orientation to detect increases in Lco thickness during CCFT, comparing it to MRI images. The protocol was tested only in asymptomatic participants, with large variability found between ultrasonography and MRI data. However, the results are not comparable with our data, as in the first study, each volunteer performed only 1 CCFT phase. In our study, every participant performed all 5 phases of the test, with each executed phase being compared between patients with chronic neck pain and controls.

Discrimination Between Patients with Chronic Neck Pain and Controls Present data reinforce the current knowledge that patients with chronic neck pain have less ability to sustain deep neck flexor contraction during the CCFT. 13-15 Similar to the results obtained by Falla et al, 13 patients with chronic neck pain showed reduced Lco recruitment in the final stages of CCFT, which represents outer ranges of craniocervical flexion that supports the evidence that there is an altered strategy of spinal control in chronic pain. 58 It is advocated that pain leads to impairment in optimal joint control that is performed by myofascial tissue, especially those low-load tonic muscles that support the segment and adjust the continuous tension of passive components of this system that allows functional stability. 59 It seems that pain leads to a cycle involving deep muscle atrophy and antagonist overuse in an attempt to control segmental movement, leading to further altered patterns of muscle activity and motor planning. 35,36,52 Being Lco an essential muscle for provision of head and cervical support and having an important density of muscle spindles, 60 a change in its role could potentially put the cervical spine at risk to overstress of contractile, inert, and

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osseous tissues, resulting in abnormal interaction of this segment with the environment. Compromising deep muscles' fine-tuning function would encourage the development of strategies to decrease spinal motion such as coactivation or antagonist overuse to prevent further injury on the spine. 61 These strategies increase the compression of spinal elements 62 leading to degeneration and persistence of pain. The protocol used in this study did not identify any statistical differences for SCM recruitment between groups, although a trend was seen toward greater increases on SCM recruitment for the chronic neck pain group, which confirms the results of Falla et al. 13 Several studies have shown that, in patients with chronic neck pain, there is a greater activity of superficial neck flexors. 13,15 Jull et al 15 showed that, in the presence of neck pain of a mechanical or whiplash origin, SCM had higher measures of EMG signal amplitude during each stage of the test compared with controls, with significantly greater shortfalls from the pressure targets in all test stages (all P b .05). A possible explanation to justify the absence of significant differences in SCM recruitment between groups in our study is that the transducer had to be partially positioned over the SCM muscle parallel to Lco orientation to permit proper visualization of both Lco and SCM muscles. This position may have restricted the visualization of the greater SCM muscle cross-sectional area. Because no studies assessing ultrasonographic measurements of SCM in CCFT were found, to this point, it is not known if greater amounts of SCM EMG activity are accompanied by greater changes in thickness in patients with chronic neck pain. Thus, the position that was developed to allow the best Lco assessment in each participant could be partially responsible for the high levels of variability found for SCM in both groups. Another possible reason for this lack of difference between groups is that CCFT aims primarily the recruitment of DCFs, and therefore, more significant changes in muscle thickness would be seen in this muscle group. Moreover, given that the sample calculation was based for Lco muscle only as this is the main aim of CCFT, this could have underpowered the study for SCM.

Effects of Cervical Spine Mobilization Session The results of this study indicate that both Lco and SCM recruitment during CCFT performance can be altered by a large amplitude cervical mobilization, with significant changes occurring only in neck pain participants. Several SMT, which include mobilization techniques, mechanisms can be linked to this finding. Some studies reported that cervical manipulative therapy can alter spinal muscle motoneurons excitability, 25,27 whereas others associate SMT to increases on sympathetic nervous system activity 28,63,64 and upper limb muscles activity enhancement. 26

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No study was found to directly contrast our results, for this is the first study to use ultrasonography to assess changes in muscle thickness after manual therapy interventions in neck muscles. However, like Sterling et al, 28 we have also shown a reduction in SCM recruitment with mobilization that could indirectly represent the occurrence of increased recruitment of neck flexors as seen in healthy participants. The inexistence of differences in Lco recruitment in phase 5 between groups after the mobilization session could also reflect facilitation of its recruitment in final stages of the test, which could, in turn, assist its original role in supporting the cervical curvature. Bialosky et al 65 proposed a model in which SMT would be a trigger to initiate a cascade of neurophysiologic responses based on spinal, supraspinal, and peripheral mechanisms that could be responsible for therapeutic outcomes. According to this model, different responses attached to specific mechanisms such as reflex attenuation, periaquedutal gray stimulation (related to the pain modulatory circuit), neuromuscular responses, and stimuli of the peripheral nervous system inhibiting inflammatory mediators and also the interaction between them would turn to the observed clinical effect. Notably, the literature suggests that descending inhibitory pathways from periaquedutal gray are involved in SMT hypoalgesic effects and associated with increased sympathetic activity and changes in neuromuscular responses. 28,64 Furthermore, mecanorreceptors stimulation through SMT is thought to modify α motoneuron excitability levels leading to an increase in muscle activity. 27 There is still some divergence on neuromuscular findings involving SMT, demonstrating both enhance 66 and reduction in superficial spinal muscles activity. 28,67 Current evidence shows consistency for coexisting hypoalgesia, sympathetic nervous system excitation, and motor function alterations, suggesting a central nervous system participation in coordinating SMT effects. 68 Thus, changes in ultrasonographic measurement of neck muscles recruitment could reflect changes occurring in one of these factors. However, the present data do not allow any conclusions on which mechanism contributes the most. Most studies on neuromuscular effects of cervical SMT are performed using high-velocity manipulative therapy. 25,27,66,67 In our study, however, we have applied a low-velocity, large amplitude mobilization at the cervical joint. Joint mobilization is largely used in clinical practice and does not have as many risks attached to it as manipulation does, 69-74 with reports of similar effects. 75 Leaver et al 75 showed that patients with neck pain who received 4 neck manipulation sessions over 2 weeks did not experience a faster recovery compared with 4 neck mobilization sessions over 2 weeks. Another important factor to consider is that the application of manual therapy to a nonspecific painful segment showed significant changes in muscle recruitment for the patients with chronic

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neck pain in this study, suggesting that the mechanism of pain control and motor function related to SMT effects may be global and not related to 1 specific segment. 51

Limitations One limitation of our study was the size of the transducer. For 2 participants, the transducer was too large for the size of their necks, which affected their ability to perform the tests during the training period of the trial. Moreover, because of the type of transducer used, it was difficult to accurately determine the entire Lco inferior boundary in a small portion of participants. Another limitation is that our sample mean age is younger than 30 years, and the extrapolation of the results of this study to a general adult and elderly populations should be viewed cautiously. In our study, the therapist who applied the mobilization technique in all patients knew their condition of presence or absence of pain at the time of data collection, and this fact could potentially affect the application of the technique; however, the type of technique, the grade of Maitland's technique applied, the frequency chosen, and the segment selected for it were all standardized, so all participants received the exactly equal intervention regardless of the group they belonged to (chronic neck pain or controls). Finally, the results are based on a single mobilization session, and long-term effects of spinal mobilization on the activity of cervical muscles are not known.

CONCLUSION This study has shown the ability of the ultrasonography to detect changes in neck flexors thickness, mainly the Lco muscle, discriminating people with and without chronic neck pain. Cervical spine mobilization is associated with immediate changes in neck flexor muscle recruitment in patients with chronic neck pain; however, long-term effects are still unknown.

Practical Applications • Ultrasonography is a feasible tool to assess neck flexor muscles recruitment and is valid to discriminate chronic neck pain patients from controls. • Changes in neck flexor muscles recruitment occurred after a single cervical spine mobilization therapy session being more pronounced in chronic neck pain patients. • The ability of ultrasonography to detect longterm changes in neck muscles recruitment after a cervical spine mobilization therapy has yet to be investigated.

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FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST No funding sources or conflicts of interest were reported for this study.

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