BRIEF REPORT

Magnetic Resonance Imaging Parameters Selected for Optimal Visualization of the Occipitoatlantal Interspace

Richard C. Hallgren, PhD; Jacob J Rowan, DO

From the Departments of Context: Disorders of the rectus capitis posterior minor (RCPm) muscles have been Physical Medicine & associated with chronic headache. Magnetic resonance (MR) imaging protocols cur- Rehabilitation (Dr Hallgren) and Osteopathic Manipulative rently used in clinical settings do not result in image sets that can be used to Medicine (Drs Hallgren and adequately visualize the integrity of occipitoatlantal structures or to definitively Rowan) at Michigan State quantify time-dependent functional morphologic changes. University College of Osteopathic Medicine in East Objective: To develop an MR imaging protocol that provides the superior image Lansing. quality needed to visualize occipitoatlantal soft tissue structures and quantify time- Financial Disclosures: dependent pathologic changes. None reported. Methods: Asymptomatic participants were recruited from the Michigan State Support: None reported. University College of Osteopathic Medicine student body. Magnetic resonance Address correspondence to imaging data were collected from each participant at enrollment and 2 weeks after Richard C. Hallgren, PhD, enrollment using a 3T magnet. A conventional spin-echo pulse sequence was used Department of Physical Medicine & Rehabilitation, to construct 24 axial, T1-weighted images with the following measurement para- Michigan State University meters: repetition time, 467 milliseconds; echo time, 13.5 milliseconds; number of College of Osteopathic excitations, 4; slice thickness, 3.0 mm; and in-plane resolution, 0.625×0.625 mm. Medicine, 965 Wilson Rd, St B-411, West Fee Hall, Image planes were aligned approximately perpendicular to the long axes of the East Lansing, MI 48824-1316. RCPm muscles to facilitate the authors’ ability to accurately draw regions of interest fi Email: [email protected] around the speci c muscle boundaries. Cross-sectional area (CSA) of the right and left RCPm muscles was quantified for each participant at the 2 points in time. The Submitted fi May 9, 2018; null hypothesis was that there would be no signi cant difference between mean revision received values of muscle CSA collected at enrollment and 2 weeks after enrollment for a June 19, 2018; given participant and a given side of his or her body. accepted July 2, 2018. Results: Thirteen participants were enrolled. No significant difference was found between mean values of either right or left RCPm muscle CSA for any of the parti- cipants measured at enrollment and 2 weeks after enrollment (all P>.05).

Conclusion: The protocol achieves the superior image quality necessary to compare the functional form of occipitoatlantal structures at progressive points in time.

J Am Osteopath Assoc. 2019;119(3):173-182 doi:10.7556/jaoa.2019.028

Keywords: MR imaging, myodural bridge, rectus capitis muscles, tendon tear

agnetic resonance (MR) imaging techniques have long been used to differ- entiate between normal muscle and muscle with fatty infiltrates1,2 and to M quantify changes in muscle volume and cross-sectional area (CSA) after

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exercise.3 However, sufficient test/retest reliability has nerves. The convergence of trigeminal and cervical only been achieved for muscles with relatively large afferents and irritation of these fibers (eg, stretching) volumes. results in referred headache.11-14 To our knowledge, Hallgren et al4,5 were the first to The functional relationship between RCPm muscles use MR images to report on morphologic changes and the spinal dura is not currently known. However, within rectus capitis posterior minor (RCPm) muscles in 2014, Hallgren et al15 reported that voluntary head in patients with chronic head and neck pain. The RCPm retraction results in a significant increase in electromyo- muscles are a pair of small muscles that arise from the graphy activity as RCPm muscles are stretched during posterior tubercle on the posterior arch of C1 and insert posterior movement of the head within the sagittal into the occipital bone inferior to the inferior nuchal plane without rotation. Atrophy of the RCPm muscles line and lateral to the midline. Rectus capitis posterior would be expected to compromise the functional minor muscles are unique because they are the only relationship between these muscles and the pain- muscles that attach to the posterior arch of the atlas. sensitive spinal dura and is thought to result in abnor- Fatty infiltration of RCPm muscles on MR imaging has mal levels of tension within the dura.16 Head movement been reported in patients with chronic headache asso- is proposed to be an important contributor to cerebro- ciated with both nontraumatic events6 and traumatic spinal fluid dynamics17 that are regulated by forces events such as rear-end motor vehicle crashes.7 generated from structures within the occipitoatlantal Atrophy, as evidenced by increased fatty infiltration interspace.18 over time, has been shown to be predictive of chronic Early detection of fatty infiltration of RCPm muscles whiplash-associated disorders.8 The cause of fatty might be beneficial in the assessment and management infiltration of RCPm muscle in patients with whiplash- of a muscle injury that could progress from an acute to associated disorders is unknown, but it could be a chronic condition. A systematic review19 revealed that expected that it would result from disuse atrophy, single study populations with neck pain showed a sig- neurogenic atrophy, or a tendon tear. Fatty infiltration nificant association between fatty infiltration in cervical would not be expected to directly result in headache, muscles and persistent neck disability. However, the but it would weaken the RCPm muscles and comprom- review failed to conclude that there is an association ise their ability to function normally. A key tenet of between dysfunction of the cervical spine on MR osteopathic medicine is that structure and function are imaging and clinically important outcomes such as reciprocally interrelated and that dysfunction in one pain and disability. The failure was attributed to the het- part of the body can have a negative effect on other erogeneity of the studies reviewed, the relatively small parts of the body. Loss of the functional capacity of sample size of the populations that were studied, and even a small component (eg, the RCPm muscles) the variety of imaging protocols that were used. should not automatically be assumed to have an insig- Unfortunately, the standard MR protocol that is nificant impact on the whole body. Fatty infiltration of commonly used for imaging the cervical spine is not RCPm muscles would result in a reduction in the total adequate to visualize fine structures within the occipi- number of contractile elements and would diminish toatlantal interspace,20 and customized protocols have the capacity of these muscles to generate and sustain not been shown to be adequate for accessing the normal levels of force. temporal development of fatty infiltration.18 A connective tissue bridge is found between the I set out to develop an MR imaging protocol that RCPm muscles and the pain-sensitive spinal dura would provide the superior image quality necessary to mater of the posterior cranial fossa.9,10 The spinal dura reliably quantify the progression of fatty infiltration contains nociceptive fibers that feed into the cervical over time. The analytic strategy was based on the

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assumption that asymptomatic participants would not scanned using a General Electric Medical Systems have a significant change in skeletal muscle CSA over Signa HDxt 3.0-T scanner. A conventional spin-echo 2 weeks. To test this hypothesis, image resolution suffi- pulse sequence was used to construct 2 image sets cient to resolve fine structures within the occipitoatlan- consisting of: tal interspace and the ability to ensure registration of RCPm muscles between image sets collected at 2 ▪ 14 sagittal, T2-weighted images with measurement points in time was needed. For this discussion, registra- parameters of repetition time, 5250 milliseconds; tion refers to the alignment and overlay of MR image echo time, 100 milliseconds; slice thickness, 2.5 mm; data from a specific point in time with the participant’s and in-plane resolution, 0.43×0.43 mm. own MR image data from another point in time. ▪ 24 axial, T1-weighted images with measurement parameters of repetition time, 467 milliseconds; echo time, 13.5 milliseconds; number of excitations, 4; Methods slice thickness, 3.0 mm; and in-plane resolution, Study Population 0.625×0.625 mm. An email advertisement was used to recruit potential participants from the second-year student population The sagittal image set was used to define the orienta- of the Michigan State University (MSU) College of tion of the axial image planes from which muscle CSA Osteopathic Medicine. Participants were required to be would be quantified. The scan parameters and the free of head and neck pain; be free of significant orientation of the axial image planes were selected to motion restrictions; have had no surgical procedures in optimize our ability to manually draw regions of inter- the region of the upper cervical spine; and have not est (ROI) around RCPm muscle boundaries.22-24 An been involved in a motor vehicle crash within the past in-plane resolution of 0.625×0.625 mm was deemed 30 days. The age of participants was limited to sufficient to resolve structures within the posterior between 20 and 40 years because a progressive loss of atlantoaxial interspace. The acquisition time was muscle mass has been reported to occur at approxi- approximately 8.5 minutes. The following steps were mately 50 years of age.21 The study was approved by taken to ensure image intensities were quantified the MSU Institutional Review Board. within the same region of soft tissue at progressive The research protocol was reviewed with each poten- points in time: tial participant. Participation required willingness to complete 2 MR imaging scans, spaced approximately 1. Each participant was to complete a baseline scan 2 weeks apart. Participants were to be compensated followed by a second scan performed at least 2 $150 at the completion of the second scan. However, weeks later. The uniqueness of this protocol ensures compensation was not conditional upon completion of that accurate registration of the axial image sets the study. To be enrolled in the study, potential partici- taken at the 2 points in time can be achieved. This pants were required to sign an institutional review level of accuracy is necessary when CSA is to be board–approved informed consent form. Participant calculated at the same location in 3-dimensional metrics of sex (1=woman, 0=man), age, height, (3D) space for both points in time. Participants were weight, and body mass index (BMI) were recorded. positioned in the magnet so that their forehead was parallel to the table to approximate a neutral head Collection of Image Slice Data posture.25 Magnetic resonance imaging data were collected at the 2. A locator slice was adjusted to pass through both MSU Department of Radiology. Participants were the superior aspect of the odontoid process of the

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axis (C2) and the posterior arch of the atlas (C1) about an oblique axis with Analyze 12.0 (AnalyzeDirect) (Figure 1 [yellow dots]).4 Serial slice image data to increase 3D space registration accuracy before were collected superior and inferior to this locator data analysis. slice. Image Analysis Since the RCPm muscles are closely aligned to the Analysis of the CSA data for each muscle began by midline, the positioning protocol allowed image planes selecting a slice level that was representative of the to be aligned approximately perpendicular to the long central portion of the muscle. Using the Analyze 12.0 axis of both the right and left muscles. Accurate ROI software, an ROI was manually drawn around the can be drawn around specific muscle boundaries by fascial border of both the left and right RCPm aligning the image plane approximately perpendicular muscles. The software was then used to calculate the to the long axes of the RCPm muscles.26,27 descriptive statistics of pixels contained within the Placement of the image plane relative to the long axis ROI. Because the focus of this study was to track patho- of the RCPm muscles is facilitated by using anatomical logic changes over time, the strategy to manually draw landmarks unique to each participant and is critical to an ROI enabled each participant to be their own obtain a good approximation for overlaying data from control and allowed us to see whether the muscle CSA the 2 scans. Unique anatomical landmarks assist with at a specific location in 3D space had changed in time accurate positioning of the image plane when a partici- relative to the baseline value. pant is scanned at progressive points in time. A degree Manually drawing ROI to obtain muscle CSA has of accuracy is necessary when CSA is calculated at the been shown to have high levels of intrarater and inter- same locations in 3D space for both points in time to rater reliability, which indicates a high level of repeat- obtain meaningful CSA values that track abnormal ability.28 The protocol orients the image plane progression. Additionally, image data for both the approximately perpendicular to the long axes of the right and left side of each participant were reformatted RCPm muscles (Figure 1) and enables the accurate drawing of an ROI around the specificmuscle boundary. Two axial scans of the same patient are shown in Figure 2. The left image is representative of the image that would be expected using a standard clinical proto- col, and the right image is representative of the image produced using the protocol in this study. The image produced using this study’s protocol results in a sharper boundary between the RCPm muscles and the connective tissues that surround them compared with the standard clinical protocol. A preliminary analysis of the data revealed that 4 Figure 1. men had movement artifacts in at least 1 of the 2 scans For image slice data collection, the image plane was fi oriented approximately perpendicular to the long axes of the that was suf cient to degrade the image set(s) to be rectus capitis posterior minor (RCPm) muscles. A locator unusable. Unusable was defined as image sets that slice (red lines) was adjusted to pass through the superior were significantly degraded by movement artifact (blur- aspect of the odontoid process of the axis (yellow dots) and the posterior arch of the atlas. Serial image data were ring) that resulted in an indistinct boundary between collected superior and inferior to this locator slice. active (muscle) and passive (fatty) tissues.

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AB

Figure 2. Two axial scans of the same patient demonstrate the difference in clarity in images produced using the standard imaging protocol (A) and this study’s protocol (B). The image produced using this study’s protocol resulted in a sharper boundary between the rectus capitis posterior minor (RCPm) muscles and the connective tissues that surround them.

Statistical Analysis Participants that had a significant number of data The data in a repeated-measures analysis should have a points that were marked as outliers were removed from normal distribution and no significant outliers to be the final analysis. considered valid. Using SPSS Statistics for Windows, Version 24 (IBM Corp), a Shapiro-Wilk Test confirmed that the 4 samples of CSA data (left/right RCPm, first Results scan/second scan) had normal distributions. Twenty-four people (18 men and 6 women) were origin- The cohort was then divided into 2 groups (women ally enrolled in the study. After enrollment, it was found and men) because gender differences were suspected that 2 participants had violated the inclusion criteria, and to potentially affect CSA. A 1-way analysis of variance both were excluded from the study. Data from an add- wasusedtotestforasignificant difference between itional 4 participants were removed because of blurring height, weight, and mean values of CSA for the left of the images due to motion artifacts. An additional 5 and right RCPm muscles between women and men. A participants were removed because their RCPm muscles significant difference (P<.05) was found between were considered to be too small to obtain an accurate women and men for weight and mean values of CSA, estimate of CSA or they had a significant number of out- but no significant difference was found in height. liers. Therefore, the data from 3 women and 10 men Finally, a multivariate repeated-measures analysis of were analyzed in this study. The participants were a variance was used to test the null hypothesis and deter- mean (SD) age of 24 (2) years, 178 (8) cm, 79 (12) kg, mine whether there was a within-person effect. The null and had a BMI of 25 (4). These characteristics are hypothesis was that no significant difference would be similar to a population sample from 25-year-old women found between mean values of CSA collected from the and women of 172 cm, 75 kg, and BMI of 25.29 All par- left and right RCPm at 2 points in time for both women ticipants except 1 man were right-hand dominant. and men. The data sets were checked for outliers using Figure 3 shows 2 image slices for the same partici- the Explore tool in the AnalyzeDirect software. pant separated by more than 2 weeks. The left (red)

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A B

Figure 3. Magnetic resonance images for the same participant separated by more than 2 weeks demonstrate the left rectus capitis posterior minor (RCPm) (red) and right RCPm (green) muscles that are outlined in each image slice. The cross sectional area (CSA) of the left RCPm muscle on the initial scan (A) was equal to 228 pixels. The CSA of the left RCPm muscle on the follow-up scan (B) was equal to 230 pixels.

and right (green) RCPm muscles are outlined in each would not have a significant change in skeletal muscle image slice. The CSA of the left RCPm muscle on the CSA over 2 weeks. baseline scan (A) was equal to 228 pixels. The CSA of the left RCPm muscle on the follow-up scan (B) was equal to 230 pixels. Figure 4 illustrates the asym- Discussion metry that was commonly seen between the right and Fatty infiltration of skeletal muscle results in a reduc- left RCPm muscles, with the left side typically having tion in the total number of contractile elements and a larger CSA than the right. Fifty-two observations diminishes the capacity of these muscles to generate from the 13 participants were included in the analyses, and sustain normal levels of force. Rectus capitis pos- and, thus, from the original 22 participants, 59% of the terior minor muscles with fatty infiltration have been subsequent observations were kept and 41% were reported in patients with chronic headache associated discarded. with both nontraumatic events6 and traumatic events, Figure 5 shows box plots of the data. No significant such as rear-end motor vehicle crashes.7 Fatty infiltra- difference was found between the CSA of either the tion would not be expected to directly result in right or the left RCPm muscles sampled at enrollment headache, but it would weaken the muscles and com- and 2 weeks after enrollment (all P>.05). The finding promise their ability to function normally. A key tenet of no significant difference is consistent with our of osteopathic medicine is that structure and function original assumption that asymptomatic participants are reciprocally interrelated and that dysfunction in one

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irreversible fatty infiltration and loss of function that is directly related to the extent of the lesion31 and the time between injury and surgical intervention.32,33 Surgically repairing the tear has been shown to halt the progression of fatty infiltration in the supraspinatus muscle.34 A tendon tear has not been previously associated with fatty infiltration of RCPm muscles, but such an injury is not inconsistent with the kinematic response of the head during a rear-end motor vehicle crash.35 The RCPm muscles attach to the occiput and the pos-

Figure 4. terior arch of the atlas and have been shown to be for- Magnetic resonance image illustrating the asymmetry that cibly stretched during whiplash-type motions resulting was commonly seen between the right and left rectus 36 capitis posterior minor muscles. The left side (red) typically from a rear-end motor vehicle crash. It has been pro- had a larger cross-sectional area than the right side (green). posed but not proven that the passive load displacement The image is viewed from inferior to superior. properties of RCPm muscles puts them at risk of a strain injury during a rear-end motor vehicle crash.37 part of the body can have a significant impact on the A connective tissue bridge is present between the whole body. RCPm muscles and the pain-sensitive spinal dura of After ruling out muscle disease and neurogenic the posterior cranial fossa.9,10 The spinal dura contains atrophy, the 2 most common causes of fatty infiltration nociceptive fibers that feed into the cervical nerves, in skeletal muscles are tendon tear and disuse. A tendon and the convergence of trigeminal and cervical affer- tear is a common shoulder injury30 that results in ents results in referred headache.38

Left RCPm Right RCPm

400

300 CSA

200

100

Enrollment Sample after Enrollment Sample after Sample 2 weeks Sample 2 weeks Repeated Sample

Figure 5. The box plot demonstrates the 52 observations from the 13 participants that were included in the analyses. From the original 22 participants, 50% of the subsequent observations were kept and 41% were discarded. Abbreviations: CSA, cross- sectional area; RCPm, rectus capitis posterior minor.

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A musculotendonous junction tear of the RCPm forward head posture that is commonly associated with muscles could result in fatty infiltration that would be chronic, tension-type headache40-42 but is not seen in expected to compromise the functional relationship patients with migraine.43 Disuse atrophy would also be between these muscles and the pain-sensitive spinal expected to reduce the functional capacity of the RCPm dura. The spinal dura contain nociceptive fibers that muscles. Reversal of disuse atrophy could be accom- feed into the cervical nerves of the trigeminocervical plished through an appropriate exercise program that nucleus. Irritation of these fibers, specifically stretching, selectively activates these muscles. A 2014 report15 is known to result in headache12,14 and has been pro- showed that voluntary head retraction results in a sig- posedtobeasourceofchronicheadache.39 We nificant increase in electromyography activity as suggest that the spinal dura becomes a source of head RCPm muscles are stretched during posterior move- and neck pain when the functional integrity of the ment of the head within the sagittal plane without rota- RCPm muscles are compromised, as might occur tion. Lengthening of a muscle while it is activated is during a whiplash-type injury, and the restoration of defined as an eccentric contraction. Eccentric contrac- the normal functional relationship between RCPm tions are known to strengthen muscle44 and to reduce muscles and the spinal dura will result in a decrease in forward head posture.45 We hypothesized that volun- headache measures. The imaging protocol developed tary head retraction would strengthen RCPm muscles, in this study provides the resolution that would allow as evidenced by an increase in the CSA of the contract- visualization of a disruption of the myotendinous junc- ile component of the muscles on MR imaging, and that tion following a rear-end motor vehicle crash and could this would be associated with a decrease in headache facilitate rapid surgical intervention, which might halt measures. By tracking CSA using our MR imaging the progression of chronic head and neck pain protocol, researchers would be able to quantify the (Figure 6). efficacy of treatment. Fatty infiltration of the RCPm muscles could also be Significantly more data had to be discarded than a consequence of disuse atrophy resulting from a originally anticipated, which made the final size of

Figure 6. Magnetic resonance images demonstrating the resolution that the imaging protocol developed in this study can provide. The protocol would allow for the visualization of a disruption of the myotendinous junction following a rear-end motor vehicle crash and could facilitate rapid surgical intervention, which might halt the progression of chronic head and neck pain. Abbreviation: RCPm, rectus capitis posterior minor.

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the study cohort the major limitation of the study. The posterior minor muscle with active trigger points in chronic tension-type headache: a pilot study. Am J Phys Med Rehab. 2008;87(3):197-203. primary reason for the small sample size resulted doi:10.1097/PHM.0b013e3181619766 because of participant movement during MR imaging. 7. Elliott JM. Are there implications for morphological changes in neck To achieve an adequate resolution, the scan time was muscles after whiplash injury? Spine. 2011;36 (25 suppl):S205-S210. doi:10.1097/BRS.0b013e3182387f57 8.5 minutes. Participant movement during the scan 8. Elliott JM, Courtnet DM, Rademaker A, Pinto D, Sterling MM, Parrish resulted in blurring of the images, reducing the ability TB. The rapid and progressive degeneration of the cervical multifidus fi to accurately draw an ROI around a muscle boundary. in whiplash: an MRI study of fatty in ltration. Spine. 2015;40(12): E694-E700. doi:10.1097/BRS.0000000000000891 The small size of the RCPm muscles further exacer- 9. Hack GD, Koritzer RT, Robinson WL, Hallgren RC, Greenman PE. bates the difficulty of accurately drawing an ROI. Anatomic relationship between the rectus capitis posterior minor muscle and the dura mater. Spine. 1995;20(23):2484-2486.

10. Palomeque-del-Cerro L, Arraez-Aybar LA, Rodriguez-Blanco C, Guzman-Garcia R, Menendez-Aparicio M, Oliva-Pascual-Vaca A. A Conclusion systematic review of the soft-tissue connections between neck For a cohort of 3 women and 10 men, there was no stat- muscles and dura mater: the myodural bridge. Spine. 2017;42 (1):49-54. doi:10.1097/BRS.0000000000001655 istically significant difference between values of muscle 11. Bogduk N. The neck and headaches. Neurol Clin N Am. 2004;22 CSA sampled from right and left RCPm muscles taken (1):151-171. at 2 points in time. Early assessment of dysfunction that 12. Fakhran S, Qu C, Alhilali LM. Effect of the suboccipital musculature on symptom severity and recovery after mild traumatic brain injury. AJNR compromises the functional integrity of the RCPm Am J Neuroradiol. 2016;37(8):1556-1560. doi:10.3174/ajnr.A4730 muscles could be a key factor in halting the progression 13. Hack GD, Hallgren RC. Chronic headache relief after section of from an acute to a chronic condition. suboccipital muscle dural connections: a case report. Headache. 2004;44(1):84-89.

14. Rennie C, Haffajee MR, Ebrahim MA. The sinuvertebral nerves at the Author Contributions craniovertebral junction: a microdissection study. Clin Anat. 2013;26 Both authors provided substantial contributions to conception (3):357-366. doi:10.1002/ca.22105 and design, acquisition of data, or analysis and interpretation of 15. Hallgren RC, Rowan JJ, Bai P, Pierce SJ, Shafer-Crane GA, Prokop LL. data; both authors drafted the article or revised it critically for Activation of rectus capitis posterior major muscles during voluntary fi important intellectual content; both authors gave nal approval retraction of the head in asymptomatic subjects. J Manipulative Physiol of the version of the article to be published; and both authors Ther. 2014;37(6):433-440. doi:10.1016/j.jmpt.2014.07.002 agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of 16. Enix DE, Scali F, Pontell ME. The cervical myodural bridge, a review the work are appropriately investigated and resolved. of literature and clinical implications. J Can Chiropr Assoc. 2014;58 (2):184-192.

References 17. Xu Q, Yu SB, Zheng N,et al. Head movement, an important contributor to human cerebrospinal fluid circulation. Sci Rep. 2016;6:31787. 1. Fisher MR, Dooms GC, Hricak H, Reinhold C, Higgins CB. Magnetic doi:10.1038/srep31787 resonance imaging of the normal and pathologic muscular system. 18. Yuan XY, Yu SB, Liu C, et al. Correlation between chronic headaches Mag Res Imag. 1986;4(6):491-496. and the rectus capitis posterior minor muscle: a comparative analysis 2. Fleckenstein J, Peshock RM, Lewis SF, Haller RG. Magnetic of cross-sectional trail. Cephalagia. 2017;37(1):1051-1056. resonance imaging of muscle injury and atrophy in glycolytic doi:10.1177/0333102416664775 myopathies. Muscle Nerve. 1989;12(10):849-855. 19. Hill L, Aboud D, Elliott J,et al. Do findings identified on magnetic 3. Roman WJ, Fleckenstein J, Stray-Gundersen J, Always SE, Peshock resonance imaging predict future neck pain? A systematic review. R, Gonyea WJ. Adaptation in the elbow flexors of elderly males after Spine J. 2018;18(5):880-891. doi:10.1016/j.spinee.2018.01.025 heavy-resistance training. J Appl Physiol. 1993;74(2):750-754. 20. Demetrious J. Post-traumatic upper cervical subluxation visualization doi:10.1152/jappl.1993.74.2.750 by MRI: a case report. Chiropr Osteop. 2007;15(20):1-7. doi:10.1186 4. Hallgren RC, Greenman PE, Meyer RC, Rechtien JJ. MRI of normal /1746-1340-15-20 and pathological muscle of the upper cervical spine. J Clin Eng. 21. Faulkner JA, Larkin LM, Claflin, Brooks SV. Age-related changes in 1993;18(5):433-439. the structure and function of skeletal muscles. Clin Exp Pharmacol 5. Hallgren RC, Greenman PE, Rechtien JJ. Atrophy of suboccipital Physiol. 2007;34(11):1091-1096. doi:10.1111/j.1440-1681.2007.04752 muscles in patients with chronic pain: a pilot study. J Am Osteopath 22. Elliott JM, Galloway GJ, Jull GA, Noteboom JT, Centeno CJ, Gibbon Assoc. 1994;94(12):1032-1038. WW. Magnetic resonance imaging analysis of the upper cervical spine 6. Fernandez-de-las-Peñas C, Cuadrado ML, Arendt-Nielsen L,Ge HY, extensor musculature in an asymptomatic cohort: an index of fat within Pareja JA. Association of cross-sectional area of the rectus capitis muscle. Clin Radiol. 2005;60(3):355-363. doi:10.1016/j.crad.2004.08.013

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