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Evaluating Serratus Anterior Muscle Function in Neck Pain Using Muscle Functional Magnetic Resonance Imaging
EVALUATING SERRATUS ANTERIOR MUSCLE FUNCTION NECK PAIN USING MUSCLE FUNCTIONAL MAGNETIC RESONANCE IMAGING
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Blair Sheard, PT(Hons), a James Elliott, PT, PhD, b Barbara Cagnie, PT, PhD, c and Shaun O'Leary, PT, PhD d
ABSTRACT Objective: Muscle functional magnetic resonance imaging (mfMRI) quantifies exercise-induced alterations in soft-aqueous skeletal muscle as a surrogate measure of muscle activity. Because of its excellent spatiotemporal resolution, mfMRI can be used as a noninvasive evaluation of the function of muscles that are challenging to evaluate, such as the serratus anterior (SA) muscle. The purpose of this preliminary study was to investigate the feasibility of evaluating SA muscle function in individuals with neck pain compared with healthy controls using mfMRI. Methods: Muscle functional magnetic resonance imaging scans of the SA muscle were obtained before and immediately after an isometric upper limb exercise in 10 subjects with chronic ipsilateral mechanical neck pain and scapular dysfunction (scan on symptomatic side) and in 10 age- and sex-matched healthy subjects. Scans were recorded at 4 intervertebral levels (T6-7, T7-8, T8-9, and T9-10). Differences in water relaxation values (T2 relaxation) quantified from scans before and after exercise were calculated (T2 shift) as a measure of SA muscle activity at each level and compared between groups. Results: There were significant effects for level (P = .03) and significant group × level interactions (P = .04) but no significant main effect for group (P = .59). Post hoc tests revealed that significant differences in T2 shift values between levels were only evident in the healthy control group. Conclusions: This study demonstrated that despite some inherent challenges associated with imaging the SA muscle, mfMRI appears to have adequate spatiotemporal resolution to effectively evaluate SA muscle activity and function in healthy and clinical populations. (J Manipulative Physiol Ther 2012;35:629-635) Key Indexing Terms: Exercise; Functional MRI; Muscles; Neck Pain
he serratus anterior (SA) is a complex multidigitated muscle arising from the upper 8-9 ribs and inserting onto the medial border of the scapula from the superior to the inferior angle. 1 It consists of an upper, middle, and lower portion each contributing to control of the scapulae during upper limb tasks. 2 In this
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manner, SA is an important stability muscle of the scapulae as is evident by the presence of substantial winging following long thoracic nerve palsy. 3-6 Because of the significant role this muscle has in control of posture and motion of the scapulae, it is an important consideration in the assessment of patients with musculoskeletal disorders of
a Physiotherapist, Queensland Health, Queensland, Australia; formerly Physiotherapy Honors Student, School of Health and Rehabilitation Sciences, University of Queensland, Australia. b Assistant Professor, Northwestern University, Feinberg School of Medicine, Physical Therapy and Human Movement Sciences, Chicago, IL; formerly affiliated with National Health and Medical Research Council (NHMRC) funded Centre for Clinical Research Excellence (CCRE) (Spinal Pain, Injury and Health), The University of Queensland, Brisbane, Australia. c Postdoctoral Researcher and Lecturer, Department of Rehabilitation Sciences and Physiotherapy, Ghent University, Ghent, Belgium.
d Principal Research Fellow, Physiotherapy Department, Royal Brisbane and Womens Hospital, Queensland Health, and the NHMRC funded CCRE (Spinal Pain, Injury and Health), The University of Queensland, Brisbane, Australia. Submit requests for reprints to: Shaun O'Leary, PT, PhD, Physiotherapy Department, Royal Brisbane and Womens Hospital, Queensland Health, Royal Brisbane Post Office, 4029 Australia (e-mails: [email protected] [email protected]). Paper submitted May 25, 2012; in revised form September 21, 2012; accepted September 23, 2012. 0161-4754/$36.00 Copyright © 2012 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2012.09.008
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the upper quadrant. As such, impairment in SA function has been implicated in painful conditions of the cervical spine 7 and shoulder girdle. 8 However, for such an important muscle of the upper quadrant, investigations of its function and role in painful musculoskeletal conditions have been limited, which is likely reflective of the technical difficulties with accurately measuring the activity of this architecturally complex muscle. Although surface electromyography (EMG) is appropriate for the recording of other axioscapular muscles, the multiple thin digitations and small superficial regions accessible to electrode placement have made EMG recordings for the SA challenging. 7 Technical limitations associated with EMG, such as crosstalk (additional detection of signals from neighboring muscles), variable signaling through subcutaneous tissue, difficulty with accurate electrode placement, and the physical movement of muscle, demand the exploration of alternative methods to EMG. Muscle functional magnetic resonance imaging (MRI) (mfMRI) is one alternative noninvasive method for evaluating the activity and function of difficult to access muscles, 9-11 and the technique has shown to be comparable with EMG for quantifying muscle activity in response to exercise. 9,12,13 Generally speaking, mfMRI images are produced when a radiofrequency pulse excites hydrogen nuclei causing them to tip from the longitudinal to the transverse plane, whereby the generation of a recordable magnetic signal and image is created. When the radiofrequency pulse ceases and the nuclei begin to dephase in the transverse plane, there is a decay of the magnetic signal, which is equivalent to the “relaxation time.” 14 Muscle functional magnetic resonance imaging uses T2-weighted images that are sensitive to the relaxation time of muscle water (T2 [transverse] relaxation time). During exercise, there is an influx of fluid accompanied by an accumulation of various metabolic byproducts (phosphate, lactate, sodium) in the cytoplasm, 15 and their presence prolongs the relaxation time of muscle water. 14 The mfMRI technique is based on an increase in T2 relaxation time of soft-aqueous skeletal muscle following exercise. Specifically, exercise results in a slower decay of the muscle water signal with an attendant increase of signal intensity in the activated muscles (muscles look brighter) when compared with muscles imaged in a resting state. This difference in decay of signal is quantified as an observed T2 shift (difference between T2 relaxation values before and after exercise) that provides a noninvasive measure of muscle activation in response to exercise. 11 Although mfMRI has been previously used to investigate cervical muscle function in neck pain populations, 9,16-18 it has not been used to examine the function of axioscapular muscles such as SA. The aim of this study was to evaluate the feasibility of using mfMRI to investigate the function of the SA muscle by comparing changes in T2 relaxation (preupper to postupper limb
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isometric exercise) in individuals with and without chronic mechanical neck pain.
METHODS Subjects Twenty volunteers participated in the study including 10 individuals with mechanical neck pain (MNP) and clinical signs of scapular dysfunction (6 women and 4 men; mean [±SD] age, 28.2 ± 5.3 years) and age- and sex-matched healthy individuals (6 women and 4 men; mean [±SD] age, 24.9 ± 3.2 years). Participants were recruited through advertisements in local and university press. Participants were included in the MNP group if they reported neck pain of greater than 3 months duration, scored greater than or equal to 5 out of a possible 50 points on the Neck Disability Index, 19 demonstrated signs of dysfunction (altered motion, altered tissue compliance, pain provocation) on a manual examination of the cervical spine, 20 and demonstrated clinical signs of scapular dysfunction on the same side as the neck symptoms. Scapular dysfunction was rated on a clinical basis when winging of the medial scapular border (excessive internal scapula rotation) and/or visible inferior scapular angle (excessive anterior tilt) was observed in relaxed standing or during loaded isometric testing of the shoulder, as this is considered to be indicative of poor SA muscle function. 21 Participants were included in the control group if they reported no history of neck pain and demonstrated no positive signs of cervical spine or scapular dysfunction on a physical examination. Participants in the control group were matched to the participants with neck pain for age (within 5 years), sex, hand dominance, height (within 5cm), and weight (within 5 kg). Participants within an age range of 18 to 50 years were accepted for both groups to minimize any confounding effects of advanced degenerative changes in the cervical spine. Participants in both groups were excluded if they reported neck pain from nonmusculoskeletal causes or reported any history of traumatic neck pain or if they had any disorders of the shoulder girdle such as impingement syndromes or rotator cuff disorders. Participants were also excluded if they demonstrated signs of altered neural dynamics potentially affecting posture and movement of the shoulder girdle or neurologic signs of nerve conduction loss. In addition, participants were excluded if they had undertaken any specific training of the neck or shoulder girdle muscles during the previous 6 months. Participants also had to satisfy institutional MRI criteria via completion of a safety checklist to ensure their suitability for undergoing an MRI scan. Ethical approval for the study was granted by the University of Queensland Human Research Ethics Committee, and all procedures were conducted according
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Fig 1. Axial T2-weighted magnetic resonance image parallel to the T6-7 intervertebral disk in a healthy control. The SA muscle was identified at the level, and the Analyze software (v. 10.0) (AnalyzeDirect, Overland Park, KS) was used to establish the ROI (shaded white). to the Declaration of Helsinki. Participants provided informed consent.
MRI Measures Magnetic resonance imaging was performed on a 1.5T scanner (Siemens Sonata; Siemens Medical Solutions, Henkestr, Erlangen, Germany). A dedicated flexible cervical spine coil was used as a receiver coil. The subjects were placed in a comfortable and relaxed supine position with a pillow under their knees. The thorax was positioned neutral, without rotation, lateral flexion, or exaggerated kyphosis. Axial images of the thoracic spine were obtained at rest before the exercise protocol and repeated immediately after the exercise. An identical sagittal localizing sequence was performed for both scans to ensure a similar thoracic spine position between repeated images. Axial images parallel to the T6-T7 (Fig 1), T7-T8, T8-T9, and T9-T10 intervertebral disks with a slice thickness of 5 mm were obtained. These levels were chosen in an effort to capture the lower portions of the SA muscle. Calculation of T2 values for each muscle at each level was achieved via a turbo-spin echo sequence: repetition time, 2000 milliseconds; echo time, 10 to 161.6 milliseconds with steps of 10.1 milliseconds (16 echoes), field of view 196 × 154 mm, matrix 128 × 128, and a voxel size of 2 × 2 × 5 mm. Total acquisition time for each scan was 5 minutes and 12 seconds. Imaging procedures were identical for both the pre-exercise and postexercise scans, and images were coregistered to ensure accurate placement of the muscle region of interests (ROI). After scanning, the images were transferred to a computer for calculation of muscle T2 using ImageJ, a Java-based version of the public domain NIH Image
software (Research Services Branch, National Institutes of Health). Each transverse slice of the at the most cephalad portion of the intervertebral disc levels T6-T7, T7-T8, T8T9, and T9-T10 was used to create ROI over the muscle belly of SA on the side of neck pain or the matched side in the asymptomatic group (Fig 1). This occurred at each echo time for the pre-exercise and postexercise images. For all the ROIs, care was taken to avoid the inclusion of nonmuscular tissue such as fascia, interstitial tissues, and bone. Sixteen echoes were used in T2 calculation using a Simplex algorithm to fit the values from the specific slice in a T2 image volume to the exponential Sn = S0 exp(−TEn/ T2) (n = 1:16). The mean T2 value and its SD were derived for each ROI for scans taken pre-exercise and postexercise. The difference between the pre-exercise and post-exercise T2 values for each ROI was calculated and recorded as the T2 shift value, representing the measure of SA muscle activity for that ROI.
Exercise Protocol The exercise protocol was isometric shoulder elevation performed in standing using a purpose built dynamometer. As indicated in Figure 2, the participant performed the test against the application pad of the dynamometer equipped with a load cell (Transducer Techniques, Temecula, CA). Signals from this load cell were amplified (PM4-SG-2405E-A; Davidson Measurement, Pty, Ltd, Auburn NSW, Australia) and transmitted to a laptop computer. A custom written program (DAQ Factory Runtime; AzeoTech, Inc, Ashland, OR) converted the changes in voltage to produce the force applied as a measurement in Newtons (N), which was shown to the participant on a visual display unit. This permitted the participant to have continuous feedback of their force permitting the accurate performance of the
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Load cell providing feedback of required muscle force
Fig 2. Upper limb elevation exercise condition. The participant performs isometric elevation at 20% MVC (established at the preliminary session) in a plane 45° to the frontal plane. required exercise intensity (20% of maximal voluntary contraction [MVC]). To ensure consistency in protocol set-up between participants, a standardized process was followed, described here for testing of the left shoulder. The patient's trunk was positioned parallel to a wall (feet equidistant from the wall), and the base of the dynamometer, aligned at 45° from the wall and in contact with the left heel of the patient. This set-up ensured the application pad of the dynamometer contacted the arm perpendicularly when the arm was elevated in a plane 45° anterior to the frontal plane in a mild degree of elevation such that the arm was just off the thorax (Fig 2). This plane of elevation (45° to the frontal plane) was chosen for testing in contrast to the more conventional scapular plane (30° to the frontal plane) used in previous investigations of SA activity, 7 as we considered it more representative of the plane in which individuals use their arm functionally. To eliminate potential contribution by the elbow flexors, the application pad was positioned above the elbow. A standardized direction of effort was ensured between participants by instructing them to direct their abduction effort along the line of the application pad of the dynamometer using the anatomical position of the thumb to guide a consistent direction of force.
Procedure
Participants first attended a preliminary session where their MVC reference recordings for the exercise protocol (isometric abduction at 45° to the frontal plane) were undertaken using an identical set-up procedure to that used in the experimental session. The participant was asked to repeat 3 MVC trials with a 1-minute rest interval between repetitions with the highest value of the recorded trials used as the MVC reference value in the experimental session.
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An interval of at least 48 hours was provided between the preliminary and the experimental sessions to avoid the impact of confounding factors such as fatigue. Per institutional regulations, a general medical practitioner screened each subject to ensure their suitability for undergoing the serial MRI scans. The baseline scan was then performed (pre-exercise protocol). After the baseline scan, the participant performed the upper limb exercise protocol at an intensity of 20% of their MVC effort. Participants were asked to sustain the exercise intensity at 20% MVC effort as accurately as possible for 3 repetitions of 1-minute durations, each separated by 30-second rest intervals. Accuracy of exercise intensity was ensured with a visual display unit (Fig 2), and participants were also provided with standardized verbal instructions and encouragement to further ensure appropriate intensities of effort were attained. Immediately following the exercise, the second MRI scan (postexercise protocol) was performed.
STATISTICS Analysis was performed using the SPSS (version 18; IBM, NSW, Australia). Descriptive statistics (mean and SD) were calculated for demographic data and for the mfMRI measurements of T2 values (milliseconds) at preexercise and postexercise for each level measured in both groups. T2 shifts, defined as the difference between postexercise and pre-exercise T2 values, were used for statistical analysis to evaluate SA muscle activity. Baseline characteristics (age, T2 values at rest) were compared with an independent t test. A repeated measures general linear model was used to evaluate main effects for group (MNP, control) and level (T6-T7, T7-T8, T8-T9, and T9-T10) and group × level interactions, with a Bonferroni correction for multiple comparisons of the T2 shift (muscle activity) measures. Tests for simple effects were performed post hoc when indicated. Statistical significance was accepted at the .05 α level.
RESULTS There were no significant group differences in age (P N .1) or in T2 values at rest (pre-exercise protocol, P N .2) between the control and MNP group at any level evaluated. In 50% of cases, the right side was the test side (symptomatic side of neck), which was replicated in the control group. Data for T2 shifts (mean + 95% confidence interval) plotted by level and group are shown in Figure 3. There was a significant effect for level (P = .03) and significant group × level interaction (P = .04) but no significant main effect for group (P = .59). Tests of simple effects demonstrated that T2 shift values were significantly different between groups (higher in the MNP group) at the T6 level (P = .02) only.
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0.005
T2 Shift Values (milliseconds)
0.004 0.003 0.002 Control 0.001
Neck Pain
0 -0.001 -0.002 -0.003
T6-7
T7-8
T8-9
T9-10
Fig 3. Group mean T2 shift values (milliseconds) (95% confidence interval error bars) after the isometric abduction exercise for all levels of the SA muscle in the control and neck pain group. Asterisk denotes a significant between level (T6-7 and T9-10) difference in T2 shift values for the control group. Significant differences in T2 shift values between levels were evident only in the healthy control group and only between the T6 and T9 (P = .01) levels (Fig 3).
DISCUSSION The SA muscle, by virtue of its extensive attachments and multidigitated architecture, is a challenging muscle to evaluate functionally using conventional tools such as EMG. Exploration of alternative methods of evaluating SA function is, therefore, warranted. The mfMRI method used in this study provides enough resolution to detect and measure changes in SA muscle in response to exercise, highlighting its potential value as a complimentary method to EMG when studying the function of this important muscle of the upper quadrant. In comparison with EMG, which records electrical signals in muscles, mfMRI records metabolic events within the muscle that are associated with force production. 22 As such, the mfMRI measure avoids some of the technical issues of EMG such as crosstalk. 11 In particular, a novel aspect of this study was collecting images and recording data from the SA muscle near its attachment to the medial scapula border that have not, to date, been accessible with other measurement methods. This study has further highlighted one of the advantages of mfMRI in the noninvasive measurement of muscles that are otherwise difficult to accurately assess. 11 A notable finding of this study was the progressive increase in activity level (increasing T2 shift values) from the T6-7 level to the T9-10 level recorded for the SA muscle in the healthy participants in response to the resisted abduction exercise (Fig 3). This is perhaps reflective of the major contribution of the SA muscle to produce upward rotation and posterior tilt of the scapula augmented by the
higher concentration of SA muscle fibers present on the inferior aspects of the scapular angle. 23,24 Although SA muscle activity gradually increases with progressive elevation of upper limb range, 25 its lower fibers in particular are orientated to exert moments during both the initial (as replicated in the exercise protocol in this study) and later phases of elevation. 26 Potentially, the elevated levels of activity in the lower levels of SA examined in this study may be indicative of greater biomechanical demands of these lower portions of the muscle when performing elevation of the upper limb. This study has also indicated that the relative activity of the SA muscle at the different levels examined (T6-T7, T7T8, T8-T9, and T9-T10) during the shoulder elevation exercise may be disturbed in the neck pain group compared with the healthy controls as evident by the significant group × level interaction (P = .04). The main difference appeared to be heightened activity of the SA muscle recorded at the T6-T7 level in the participants with neck pain compared with the control group. These findings suggest a disturbance in the coordination between the upper and lower portions of SA examined, which could potentially contribute to clinical observations of scapular winging in this patient group. 3,4 These changes in scapular kinematics may contribute to the etiology of neck pain due to alterations in the length-tension relations of muscles that attach to the cervical spine such as trapezius and levator scapulae. 27,28 Irrespective of cause and effect, which at this stage is speculative, the findings of this study are consistent with previous reports of altered SA muscle coordination during upper limb tasks in patients with painful neck disorders. 7 Although the clinical inferences that can be made from this study are limited due to the relatively small sample size, the findings of this study add to the growing body of evidence of altered axioscapular
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muscle function in neck pain disorders 29-34 and support clinical recommendations for the evaluation of axioscapular muscle function in the management of neck pain. 35
Limitations There are some limitations of this study. Findings cannot be generalized to all patients with neck pain, as we included only those individuals exhibiting clinical signs of scapular dysfunction (winging). In addition, although we consider the sample size of this study (n = 20) adequate to satisfy the studies main aim of evaluating the feasibility of mfMRI in the measurement of SA muscle function, group comparisons between neck pain and controls may have been subjected to a risk of type 2 error. Another limitation is that although mfMRI measures have shown a strong relationship to other measures of muscle activity such as EMG 36-38 and force, 39 a “clinically relevant” magnitude of T2 shift is still unknown. Also from a technical measurement perspective, we cannot exclude the possibility of including fibers of the subscapularis muscle, as it is difficult to differentiate the fascial borders of these 2 muscles on T2weighted scans. However, careful attention to producing ROIs of the SA at each level was taken to minimize this risk. Future studies should also include a coregistered T1weighted scan as an anatomical reference.
CONCLUSION This study demonstrated that mfMRI appears to have adequate resolution to effectively evaluate SA muscle function in healthy and clinical populations despite some technical difficulties associated with the small cross sectional area of the SA. The method was able to (1) detect differences of recruitment in the upper and lower levels of the muscle in healthy individuals and (2) provide preliminary evidence of an exercise-induced reorganization between the different levels of the muscle in patients with mechanical neck pain. These findings warrant further investigation of this important muscle of the shoulder girdle in a larger cross-section of the neck pain population with and without specific patterns of scapular dysfunction. The study has provided justification for mfMRI as a viable method for measurement of SA muscle function.
Practical Application • The findings of this study indicate a change in behavior between the different recorded levels of SA in patients with mechanical neck pain and clinical signs of scapular dysfunction. • These findings suggest that the function of SA should be considered when assessing patients with chronic neck pain particularly when they demonstrate scapular winging.
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FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST Shaun O'Leary was supported by an NHMRC of Australia Research Training Fellowship and a Health Practitioner Research Fellowship (Queensland Health and University of Queensland [CCRE Spinal Pain, Injury and Health]). Barbara Cagnie is supported by the Research Foundation Flanders (FWO). James Elliott is supported by a NIH KL2 RR025740. No conflicts of interest were reported for this study.
REFERENCES 1. Moore KL, Dalley AF, Agur AMR. Clinically orientated anatomy 6th edition. Philadelphia: Lippincott Williams and Wilkins; 2009. 2. Hamada J, Igarashi E, Akita K, Mochizuki T. A cadaveric study of the serratus anterior muscle and the long thoracic nerve. J Shoulder Elbow Surg 2008;17:790-4. 3. Wiater JM, Flatow EL. Long thoracic nerve injury. Clin Orthop 1999;368:17-27. 4. Truong XT, Rippel DV. Orthotic devices for serratus anterior palsy: some biomechanical considerations. Arch Phys Med Rehabil 1979;60:66-9. 5. Perlmutter GS, Leffert RD. Results of transfer of the pectoralis major tendon to treat paralysis of the serratus anterior muscle. J Bone Joint Surg 1999;81:337-84. 6. Post M. Pectoralis major transfer for winging of the scapula. J Shoulder Elbow Surg 1995;4:1-9. 7. Helgadottir H, Kristjansson E, Einarsson E, Karduna A, Jonsson H. Altered activity of the serratus anterior during unilateral arm elevation in patients with cervical disorders. J Electromyogr Kinesiol 2011;21:947-53. 8. Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther 2000;80:276-91. 9. Cagnie B, Dickx N, Peeters I, Tuytens J, Achten E, Cambier D, et al. The use of functional MRI to evaluate cervical flexor activity during different cervical flexion exercises. J Appl Physiol 2008;104:230-5. 10. Dickx N, Cagnie B, Achten E, Vandemaele P, Parlevliet T, Danneels L. Changes in lumbar muscle activity because of induced muscle pain evaluated by muscle functional magnetic resonance imaging. Spine 2008;33:E983-9. 11. Cagnie B, Elliott JM, O'Leary S, D'Hooge R, Dickx N, Danneels LA. Muscle functional MRI as an imaging tool to evaluate muscle activity. J Orthop Sports Phys Ther 2011;41: 896-903. 12. Conley MS, Stone HS, Nimmons M, Dudley GA. Resistance training and human cervical muscle recruitment plasticity. J Appl Physiol 1997;83:2105-11. 13. Patten C, Meyer RA, Fleckenstein JL. T2 mapping of muscle. Semin Musculoskelet Radiol 2003;7:297-305. 14. Meyer R, Prior B. Functional magnetic resonance imaging of muscle. Exerc Sport Sci Rev 2000;28:89-92. 15. Fritz RC, Domroese ME, Carter GT. Physiological and anatomical basis of muscle magnetic resonance imaging. Phys Med Rehabil Clin N Am 2005;16:1033-51, x. 16. Elliott JM, O'Leary SP, Cagnie B, Durbridge G, Danneels L, Jull G. Craniocervical orientation affects muscle activation when exercising the cervical extensors in healthy subjects. Arch Phys Med Rehabil 2010;91:1418-22.
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17. 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;92:929-34. 18. Cagnie B, Dolphens M, Peeters I, Achten E, Cambier D, Danneels L. Use of muscle functional magnetic resonance imaging to compare cervical flexor activity between patients with whiplash-associated disorders and people who are healthy. Phys Ther 2010;90:1157-64. 19. Vernon H, Mior S. The neck disability index: a study of reliability and validity. J Manipulative Physiol Ther 1991;14: 409-15. 20. Jull G, Sterling M, Falla D, Treleaven J, O'Leary S. Whiplash, headache and neck pain: research based directions for physical therapies. Edinburgh: Elsevier; 2008. 21. Ludewig PM, Hoff MS, Osowski EE, Meschke SA, Rundquist PJ. Relative balance of serratus anterior and upper trapezius muscle activity during push-up exercises. Am J Sports Med 2004;32:484-93. 22. Kinugasa R, Kawakami Y, Fukunaga T. Quantitative assessment of skeletal muscle activation using muscle functional MRI. Magn Reson Imaging 2006;24:639-44. 23. Perry J. Muscle control of the shoulder. In: Rowe CR, editor. The Shoulder. New York: Churchill Livingstone Inc; 1988. p. 1-17. 24. Williams GR, Shakil M, Klimkiewicz J, Iannotti JP. Anatomy of the scapulothoracic articulation. Clin Orthop 1999;359: 237-46. 25. Bagg SD, Forrest WJ. Electromyographic study of the scapular rotators during arm abduction in the scapular plane. Am J Phys Med 1986;65:111-24. 26. Dvir Z, Berme N. The shoulder complex in elevation of the arm: a mechanism approach. J Biomech 1978;11:219-25. 27. Johnson G, Bogduk N, Nowitzke A, House D. Anatomy and actions of the trapezius muscle. Clin Biomech 1994;9: 44-50. 28. Oatis CA. Kinesiology: the mechanics and pathomechanics of human movement. Philadelphia: Lippincott Williams and Wilkins; 2004.
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29. Falla D, Bilenkij G, Jull G. Patients with chronic neck pain demonstrate altered patterns of muscle activation during performance of a functional upper limb task. Spine 2004;29: 1436-40. 30. Nederhand MJ, Ijzerman MJ, Hermens HJ, Baten CM, Zilvold G. Cervical muscle dysfunction in the chronic whiplash associated disorder grade II (WAD-II). Spine 2000;25: 1938-43. 31. Szeto G, Straker L, O'Sullivan P. A comparison of symptomatic and asymptomatic office workers performing monotonous keyboard work 1: neck and shoulder muscle recruitment patterns. Man Ther 2005;10:270-80. 32. Johnston V, Jull G, Souvlis T, Jimmieson N. Neck movement and muscle activity characteristics in office workers with neck pain. Spine 2008;33:555-63. 33. Wegner S, Jull G, O'Leary S, Johnston V. The effect of a scapular postural correction strategy on trapezius activity in patients with neck pain. Man Ther 2010;15:562-6. 34. Zakharova-Luneva E, Jull G, Johnston V, O'Leary S. Altered trapezius muscle behavior in individuals with neck pain and clinical signs of scapular dysfunction. J Manipulative Physiol Ther 2012;35:346-53. 35. Jull G, Sterling M, Falla D, Treleaven J, O'leary S. Whiplash, headache, and neck pain: research-based directions for physical therapies. Edinburgh: Churchill Livingstone; 2008. 36. Adams G, Duvoisin M, Dudley G. Magnetic resonance imaging and electromyography as indexes of muscle function. J Appl Physiol 1992;73:1578-83. 37. Kinugasa R, Akima H. Neuromuscular activation of triceps surae using muscle functional MRI and EMG. Med Sci Sports Exerc 2005;37:593-8. 38. Price TB, Kamen G, Damon BM, Knight CA, Applegate B, Gore JC, et al. Comparison of MRI with EMG to study muscle activity associated with dynamic plantar flexion. Magn Reson Imaging 2003;21:853-61. 39. Fisher M, Meyer R, Adams G, Foley J, Potchen E. Direct relationship between proton T2 and exercise intensity in skeletal muscle MR images. Invest Radiol 1990;25:480-5.
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Blair Sheard, PT(Hons), a James Elliott, PT, PhD, b Barbara Cagnie, PT, PhD, c and Shaun O'Leary, PT, PhD d
ABSTRACT Objective: Muscle functional magnetic resonance imaging (mfMRI) quantifies exercise-induced alterations in soft-aqueous skeletal muscle as a surrogate measure of muscle activity. Because of its excellent spatiotemporal resolution, mfMRI can be used as a noninvasive evaluation of the function of muscles that are challenging to evaluate, such as the serratus anterior (SA) muscle. The purpose of this preliminary study was to investigate the feasibility of evaluating SA muscle function in individuals with neck pain compared with healthy controls using mfMRI. Methods: Muscle functional magnetic resonance imaging scans of the SA muscle were obtained before and immediately after an isometric upper limb exercise in 10 subjects with chronic ipsilateral mechanical neck pain and scapular dysfunction (scan on symptomatic side) and in 10 age- and sex-matched healthy subjects. Scans were recorded at 4 intervertebral levels (T6-7, T7-8, T8-9, and T9-10). Differences in water relaxation values (T2 relaxation) quantified from scans before and after exercise were calculated (T2 shift) as a measure of SA muscle activity at each level and compared between groups. Results: There were significant effects for level (P = .03) and significant group × level interactions (P = .04) but no significant main effect for group (P = .59). Post hoc tests revealed that significant differences in T2 shift values between levels were only evident in the healthy control group. Conclusions: This study demonstrated that despite some inherent challenges associated with imaging the SA muscle, mfMRI appears to have adequate spatiotemporal resolution to effectively evaluate SA muscle activity and function in healthy and clinical populations. (J Manipulative Physiol Ther 2012;35:629-635) Key Indexing Terms: Exercise; Functional MRI; Muscles; Neck Pain
he serratus anterior (SA) is a complex multidigitated muscle arising from the upper 8-9 ribs and inserting onto the medial border of the scapula from the superior to the inferior angle. 1 It consists of an upper, middle, and lower portion each contributing to control of the scapulae during upper limb tasks. 2 In this
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manner, SA is an important stability muscle of the scapulae as is evident by the presence of substantial winging following long thoracic nerve palsy. 3-6 Because of the significant role this muscle has in control of posture and motion of the scapulae, it is an important consideration in the assessment of patients with musculoskeletal disorders of
a Physiotherapist, Queensland Health, Queensland, Australia; formerly Physiotherapy Honors Student, School of Health and Rehabilitation Sciences, University of Queensland, Australia. b Assistant Professor, Northwestern University, Feinberg School of Medicine, Physical Therapy and Human Movement Sciences, Chicago, IL; formerly affiliated with National Health and Medical Research Council (NHMRC) funded Centre for Clinical Research Excellence (CCRE) (Spinal Pain, Injury and Health), The University of Queensland, Brisbane, Australia. c Postdoctoral Researcher and Lecturer, Department of Rehabilitation Sciences and Physiotherapy, Ghent University, Ghent, Belgium.
d Principal Research Fellow, Physiotherapy Department, Royal Brisbane and Womens Hospital, Queensland Health, and the NHMRC funded CCRE (Spinal Pain, Injury and Health), The University of Queensland, Brisbane, Australia. Submit requests for reprints to: Shaun O'Leary, PT, PhD, Physiotherapy Department, Royal Brisbane and Womens Hospital, Queensland Health, Royal Brisbane Post Office, 4029 Australia (e-mails: [email protected] [email protected]). Paper submitted May 25, 2012; in revised form September 21, 2012; accepted September 23, 2012. 0161-4754/$36.00 Copyright © 2012 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2012.09.008
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the upper quadrant. As such, impairment in SA function has been implicated in painful conditions of the cervical spine 7 and shoulder girdle. 8 However, for such an important muscle of the upper quadrant, investigations of its function and role in painful musculoskeletal conditions have been limited, which is likely reflective of the technical difficulties with accurately measuring the activity of this architecturally complex muscle. Although surface electromyography (EMG) is appropriate for the recording of other axioscapular muscles, the multiple thin digitations and small superficial regions accessible to electrode placement have made EMG recordings for the SA challenging. 7 Technical limitations associated with EMG, such as crosstalk (additional detection of signals from neighboring muscles), variable signaling through subcutaneous tissue, difficulty with accurate electrode placement, and the physical movement of muscle, demand the exploration of alternative methods to EMG. Muscle functional magnetic resonance imaging (MRI) (mfMRI) is one alternative noninvasive method for evaluating the activity and function of difficult to access muscles, 9-11 and the technique has shown to be comparable with EMG for quantifying muscle activity in response to exercise. 9,12,13 Generally speaking, mfMRI images are produced when a radiofrequency pulse excites hydrogen nuclei causing them to tip from the longitudinal to the transverse plane, whereby the generation of a recordable magnetic signal and image is created. When the radiofrequency pulse ceases and the nuclei begin to dephase in the transverse plane, there is a decay of the magnetic signal, which is equivalent to the “relaxation time.” 14 Muscle functional magnetic resonance imaging uses T2-weighted images that are sensitive to the relaxation time of muscle water (T2 [transverse] relaxation time). During exercise, there is an influx of fluid accompanied by an accumulation of various metabolic byproducts (phosphate, lactate, sodium) in the cytoplasm, 15 and their presence prolongs the relaxation time of muscle water. 14 The mfMRI technique is based on an increase in T2 relaxation time of soft-aqueous skeletal muscle following exercise. Specifically, exercise results in a slower decay of the muscle water signal with an attendant increase of signal intensity in the activated muscles (muscles look brighter) when compared with muscles imaged in a resting state. This difference in decay of signal is quantified as an observed T2 shift (difference between T2 relaxation values before and after exercise) that provides a noninvasive measure of muscle activation in response to exercise. 11 Although mfMRI has been previously used to investigate cervical muscle function in neck pain populations, 9,16-18 it has not been used to examine the function of axioscapular muscles such as SA. The aim of this study was to evaluate the feasibility of using mfMRI to investigate the function of the SA muscle by comparing changes in T2 relaxation (preupper to postupper limb
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isometric exercise) in individuals with and without chronic mechanical neck pain.
METHODS Subjects Twenty volunteers participated in the study including 10 individuals with mechanical neck pain (MNP) and clinical signs of scapular dysfunction (6 women and 4 men; mean [±SD] age, 28.2 ± 5.3 years) and age- and sex-matched healthy individuals (6 women and 4 men; mean [±SD] age, 24.9 ± 3.2 years). Participants were recruited through advertisements in local and university press. Participants were included in the MNP group if they reported neck pain of greater than 3 months duration, scored greater than or equal to 5 out of a possible 50 points on the Neck Disability Index, 19 demonstrated signs of dysfunction (altered motion, altered tissue compliance, pain provocation) on a manual examination of the cervical spine, 20 and demonstrated clinical signs of scapular dysfunction on the same side as the neck symptoms. Scapular dysfunction was rated on a clinical basis when winging of the medial scapular border (excessive internal scapula rotation) and/or visible inferior scapular angle (excessive anterior tilt) was observed in relaxed standing or during loaded isometric testing of the shoulder, as this is considered to be indicative of poor SA muscle function. 21 Participants were included in the control group if they reported no history of neck pain and demonstrated no positive signs of cervical spine or scapular dysfunction on a physical examination. Participants in the control group were matched to the participants with neck pain for age (within 5 years), sex, hand dominance, height (within 5cm), and weight (within 5 kg). Participants within an age range of 18 to 50 years were accepted for both groups to minimize any confounding effects of advanced degenerative changes in the cervical spine. Participants in both groups were excluded if they reported neck pain from nonmusculoskeletal causes or reported any history of traumatic neck pain or if they had any disorders of the shoulder girdle such as impingement syndromes or rotator cuff disorders. Participants were also excluded if they demonstrated signs of altered neural dynamics potentially affecting posture and movement of the shoulder girdle or neurologic signs of nerve conduction loss. In addition, participants were excluded if they had undertaken any specific training of the neck or shoulder girdle muscles during the previous 6 months. Participants also had to satisfy institutional MRI criteria via completion of a safety checklist to ensure their suitability for undergoing an MRI scan. Ethical approval for the study was granted by the University of Queensland Human Research Ethics Committee, and all procedures were conducted according
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Fig 1. Axial T2-weighted magnetic resonance image parallel to the T6-7 intervertebral disk in a healthy control. The SA muscle was identified at the level, and the Analyze software (v. 10.0) (AnalyzeDirect, Overland Park, KS) was used to establish the ROI (shaded white). to the Declaration of Helsinki. Participants provided informed consent.
MRI Measures Magnetic resonance imaging was performed on a 1.5T scanner (Siemens Sonata; Siemens Medical Solutions, Henkestr, Erlangen, Germany). A dedicated flexible cervical spine coil was used as a receiver coil. The subjects were placed in a comfortable and relaxed supine position with a pillow under their knees. The thorax was positioned neutral, without rotation, lateral flexion, or exaggerated kyphosis. Axial images of the thoracic spine were obtained at rest before the exercise protocol and repeated immediately after the exercise. An identical sagittal localizing sequence was performed for both scans to ensure a similar thoracic spine position between repeated images. Axial images parallel to the T6-T7 (Fig 1), T7-T8, T8-T9, and T9-T10 intervertebral disks with a slice thickness of 5 mm were obtained. These levels were chosen in an effort to capture the lower portions of the SA muscle. Calculation of T2 values for each muscle at each level was achieved via a turbo-spin echo sequence: repetition time, 2000 milliseconds; echo time, 10 to 161.6 milliseconds with steps of 10.1 milliseconds (16 echoes), field of view 196 × 154 mm, matrix 128 × 128, and a voxel size of 2 × 2 × 5 mm. Total acquisition time for each scan was 5 minutes and 12 seconds. Imaging procedures were identical for both the pre-exercise and postexercise scans, and images were coregistered to ensure accurate placement of the muscle region of interests (ROI). After scanning, the images were transferred to a computer for calculation of muscle T2 using ImageJ, a Java-based version of the public domain NIH Image
software (Research Services Branch, National Institutes of Health). Each transverse slice of the at the most cephalad portion of the intervertebral disc levels T6-T7, T7-T8, T8T9, and T9-T10 was used to create ROI over the muscle belly of SA on the side of neck pain or the matched side in the asymptomatic group (Fig 1). This occurred at each echo time for the pre-exercise and postexercise images. For all the ROIs, care was taken to avoid the inclusion of nonmuscular tissue such as fascia, interstitial tissues, and bone. Sixteen echoes were used in T2 calculation using a Simplex algorithm to fit the values from the specific slice in a T2 image volume to the exponential Sn = S0 exp(−TEn/ T2) (n = 1:16). The mean T2 value and its SD were derived for each ROI for scans taken pre-exercise and postexercise. The difference between the pre-exercise and post-exercise T2 values for each ROI was calculated and recorded as the T2 shift value, representing the measure of SA muscle activity for that ROI.
Exercise Protocol The exercise protocol was isometric shoulder elevation performed in standing using a purpose built dynamometer. As indicated in Figure 2, the participant performed the test against the application pad of the dynamometer equipped with a load cell (Transducer Techniques, Temecula, CA). Signals from this load cell were amplified (PM4-SG-2405E-A; Davidson Measurement, Pty, Ltd, Auburn NSW, Australia) and transmitted to a laptop computer. A custom written program (DAQ Factory Runtime; AzeoTech, Inc, Ashland, OR) converted the changes in voltage to produce the force applied as a measurement in Newtons (N), which was shown to the participant on a visual display unit. This permitted the participant to have continuous feedback of their force permitting the accurate performance of the
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Load cell providing feedback of required muscle force
Fig 2. Upper limb elevation exercise condition. The participant performs isometric elevation at 20% MVC (established at the preliminary session) in a plane 45° to the frontal plane. required exercise intensity (20% of maximal voluntary contraction [MVC]). To ensure consistency in protocol set-up between participants, a standardized process was followed, described here for testing of the left shoulder. The patient's trunk was positioned parallel to a wall (feet equidistant from the wall), and the base of the dynamometer, aligned at 45° from the wall and in contact with the left heel of the patient. This set-up ensured the application pad of the dynamometer contacted the arm perpendicularly when the arm was elevated in a plane 45° anterior to the frontal plane in a mild degree of elevation such that the arm was just off the thorax (Fig 2). This plane of elevation (45° to the frontal plane) was chosen for testing in contrast to the more conventional scapular plane (30° to the frontal plane) used in previous investigations of SA activity, 7 as we considered it more representative of the plane in which individuals use their arm functionally. To eliminate potential contribution by the elbow flexors, the application pad was positioned above the elbow. A standardized direction of effort was ensured between participants by instructing them to direct their abduction effort along the line of the application pad of the dynamometer using the anatomical position of the thumb to guide a consistent direction of force.
Procedure
Participants first attended a preliminary session where their MVC reference recordings for the exercise protocol (isometric abduction at 45° to the frontal plane) were undertaken using an identical set-up procedure to that used in the experimental session. The participant was asked to repeat 3 MVC trials with a 1-minute rest interval between repetitions with the highest value of the recorded trials used as the MVC reference value in the experimental session.
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An interval of at least 48 hours was provided between the preliminary and the experimental sessions to avoid the impact of confounding factors such as fatigue. Per institutional regulations, a general medical practitioner screened each subject to ensure their suitability for undergoing the serial MRI scans. The baseline scan was then performed (pre-exercise protocol). After the baseline scan, the participant performed the upper limb exercise protocol at an intensity of 20% of their MVC effort. Participants were asked to sustain the exercise intensity at 20% MVC effort as accurately as possible for 3 repetitions of 1-minute durations, each separated by 30-second rest intervals. Accuracy of exercise intensity was ensured with a visual display unit (Fig 2), and participants were also provided with standardized verbal instructions and encouragement to further ensure appropriate intensities of effort were attained. Immediately following the exercise, the second MRI scan (postexercise protocol) was performed.
STATISTICS Analysis was performed using the SPSS (version 18; IBM, NSW, Australia). Descriptive statistics (mean and SD) were calculated for demographic data and for the mfMRI measurements of T2 values (milliseconds) at preexercise and postexercise for each level measured in both groups. T2 shifts, defined as the difference between postexercise and pre-exercise T2 values, were used for statistical analysis to evaluate SA muscle activity. Baseline characteristics (age, T2 values at rest) were compared with an independent t test. A repeated measures general linear model was used to evaluate main effects for group (MNP, control) and level (T6-T7, T7-T8, T8-T9, and T9-T10) and group × level interactions, with a Bonferroni correction for multiple comparisons of the T2 shift (muscle activity) measures. Tests for simple effects were performed post hoc when indicated. Statistical significance was accepted at the .05 α level.
RESULTS There were no significant group differences in age (P N .1) or in T2 values at rest (pre-exercise protocol, P N .2) between the control and MNP group at any level evaluated. In 50% of cases, the right side was the test side (symptomatic side of neck), which was replicated in the control group. Data for T2 shifts (mean + 95% confidence interval) plotted by level and group are shown in Figure 3. There was a significant effect for level (P = .03) and significant group × level interaction (P = .04) but no significant main effect for group (P = .59). Tests of simple effects demonstrated that T2 shift values were significantly different between groups (higher in the MNP group) at the T6 level (P = .02) only.
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*
0.005
T2 Shift Values (milliseconds)
0.004 0.003 0.002 Control 0.001
Neck Pain
0 -0.001 -0.002 -0.003
T6-7
T7-8
T8-9
T9-10
Fig 3. Group mean T2 shift values (milliseconds) (95% confidence interval error bars) after the isometric abduction exercise for all levels of the SA muscle in the control and neck pain group. Asterisk denotes a significant between level (T6-7 and T9-10) difference in T2 shift values for the control group. Significant differences in T2 shift values between levels were evident only in the healthy control group and only between the T6 and T9 (P = .01) levels (Fig 3).
DISCUSSION The SA muscle, by virtue of its extensive attachments and multidigitated architecture, is a challenging muscle to evaluate functionally using conventional tools such as EMG. Exploration of alternative methods of evaluating SA function is, therefore, warranted. The mfMRI method used in this study provides enough resolution to detect and measure changes in SA muscle in response to exercise, highlighting its potential value as a complimentary method to EMG when studying the function of this important muscle of the upper quadrant. In comparison with EMG, which records electrical signals in muscles, mfMRI records metabolic events within the muscle that are associated with force production. 22 As such, the mfMRI measure avoids some of the technical issues of EMG such as crosstalk. 11 In particular, a novel aspect of this study was collecting images and recording data from the SA muscle near its attachment to the medial scapula border that have not, to date, been accessible with other measurement methods. This study has further highlighted one of the advantages of mfMRI in the noninvasive measurement of muscles that are otherwise difficult to accurately assess. 11 A notable finding of this study was the progressive increase in activity level (increasing T2 shift values) from the T6-7 level to the T9-10 level recorded for the SA muscle in the healthy participants in response to the resisted abduction exercise (Fig 3). This is perhaps reflective of the major contribution of the SA muscle to produce upward rotation and posterior tilt of the scapula augmented by the
higher concentration of SA muscle fibers present on the inferior aspects of the scapular angle. 23,24 Although SA muscle activity gradually increases with progressive elevation of upper limb range, 25 its lower fibers in particular are orientated to exert moments during both the initial (as replicated in the exercise protocol in this study) and later phases of elevation. 26 Potentially, the elevated levels of activity in the lower levels of SA examined in this study may be indicative of greater biomechanical demands of these lower portions of the muscle when performing elevation of the upper limb. This study has also indicated that the relative activity of the SA muscle at the different levels examined (T6-T7, T7T8, T8-T9, and T9-T10) during the shoulder elevation exercise may be disturbed in the neck pain group compared with the healthy controls as evident by the significant group × level interaction (P = .04). The main difference appeared to be heightened activity of the SA muscle recorded at the T6-T7 level in the participants with neck pain compared with the control group. These findings suggest a disturbance in the coordination between the upper and lower portions of SA examined, which could potentially contribute to clinical observations of scapular winging in this patient group. 3,4 These changes in scapular kinematics may contribute to the etiology of neck pain due to alterations in the length-tension relations of muscles that attach to the cervical spine such as trapezius and levator scapulae. 27,28 Irrespective of cause and effect, which at this stage is speculative, the findings of this study are consistent with previous reports of altered SA muscle coordination during upper limb tasks in patients with painful neck disorders. 7 Although the clinical inferences that can be made from this study are limited due to the relatively small sample size, the findings of this study add to the growing body of evidence of altered axioscapular
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muscle function in neck pain disorders 29-34 and support clinical recommendations for the evaluation of axioscapular muscle function in the management of neck pain. 35
Limitations There are some limitations of this study. Findings cannot be generalized to all patients with neck pain, as we included only those individuals exhibiting clinical signs of scapular dysfunction (winging). In addition, although we consider the sample size of this study (n = 20) adequate to satisfy the studies main aim of evaluating the feasibility of mfMRI in the measurement of SA muscle function, group comparisons between neck pain and controls may have been subjected to a risk of type 2 error. Another limitation is that although mfMRI measures have shown a strong relationship to other measures of muscle activity such as EMG 36-38 and force, 39 a “clinically relevant” magnitude of T2 shift is still unknown. Also from a technical measurement perspective, we cannot exclude the possibility of including fibers of the subscapularis muscle, as it is difficult to differentiate the fascial borders of these 2 muscles on T2weighted scans. However, careful attention to producing ROIs of the SA at each level was taken to minimize this risk. Future studies should also include a coregistered T1weighted scan as an anatomical reference.
CONCLUSION This study demonstrated that mfMRI appears to have adequate resolution to effectively evaluate SA muscle function in healthy and clinical populations despite some technical difficulties associated with the small cross sectional area of the SA. The method was able to (1) detect differences of recruitment in the upper and lower levels of the muscle in healthy individuals and (2) provide preliminary evidence of an exercise-induced reorganization between the different levels of the muscle in patients with mechanical neck pain. These findings warrant further investigation of this important muscle of the shoulder girdle in a larger cross-section of the neck pain population with and without specific patterns of scapular dysfunction. The study has provided justification for mfMRI as a viable method for measurement of SA muscle function.
Practical Application • The findings of this study indicate a change in behavior between the different recorded levels of SA in patients with mechanical neck pain and clinical signs of scapular dysfunction. • These findings suggest that the function of SA should be considered when assessing patients with chronic neck pain particularly when they demonstrate scapular winging.
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FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST Shaun O'Leary was supported by an NHMRC of Australia Research Training Fellowship and a Health Practitioner Research Fellowship (Queensland Health and University of Queensland [CCRE Spinal Pain, Injury and Health]). Barbara Cagnie is supported by the Research Foundation Flanders (FWO). James Elliott is supported by a NIH KL2 RR025740. No conflicts of interest were reported for this study.
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