Abstract
Context:
Disorders of the rectus capitis posterior minor (RCPm) muscles have been associated with chronic headache. Magnetic resonance (MR) imaging protocols currently used in clinical settings do not result in image sets that can be used to adequately visualize the integrity of occipitoatlantal structures or to definitively quantify time-dependent functional morphologic changes.
Objective:
To develop an MR imaging protocol that provides the superior image quality needed to visualize occipitoatlantal soft tissue structures and quantify time-dependent pathologic changes.
Methods:
Asymptomatic participants were recruited from the Michigan State University College of Osteopathic Medicine student body. Magnetic resonance imaging data were collected from each participant at enrollment and 2 weeks after enrollment using a 3T magnet. A conventional spin-echo pulse sequence was used to construct 24 axial, T1-weighted images with the following measurement parameters: repetition time, 467 milliseconds; echo time, 13.5 milliseconds; number of excitations, 4; slice thickness, 3.0 mm; and in-plane resolution, 0.625×0.625 mm. Image planes were aligned approximately perpendicular to the long axes of the RCPm muscles to facilitate the authors' ability to accurately draw regions of interest around the specific 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 null hypothesis was that there would be no significant difference between mean values of muscle CSA collected at enrollment and 2 weeks after enrollment for a given participant and a given side of his or her body.
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 participants 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.
Magnetic resonance (MR) imaging techniques have long been used to differentiate between normal muscle and muscle with fatty infiltrates
1,2 and to quantify changes in muscle volume and cross-sectional area (CSA) after exercise.
3 However, sufficient test/retest reliability has only been achieved for muscles with relatively large volumes.
To our knowledge, Hallgren et al
4,5 were the first to use MR images to report on morphologic changes within rectus capitis posterior minor (RCPm) muscles in patients with chronic head and neck pain. The RCPm muscles are a pair of small muscles that arise from the posterior tubercle on the posterior arch of C1 and insert into the occipital bone inferior to the inferior nuchal line and lateral to the midline. Rectus capitis posterior minor muscles are unique because they are the only muscles that attach to the posterior arch of the atlas. Fatty infiltration of RCPm muscles on MR imaging has been reported in patients with chronic headache associated with both nontraumatic events
6 and traumatic events such as rear-end motor vehicle crashes.
7
Atrophy, as evidenced by increased fatty infiltration over time, has been shown to be predictive of chronic whiplash-associated disorders.
8 The cause of fatty infiltration of RCPm muscle in patients with whiplash-associated disorders is unknown, but it could be expected that it would result from disuse atrophy, neurogenic atrophy, or a tendon tear. Fatty infiltration would not be expected to directly result in headache, but it would weaken the RCPm muscles and compromise their ability to function normally. A key tenet of osteopathic medicine is that structure and function are reciprocally interrelated and that dysfunction in one part of the body can have a negative effect on other parts of the body. Loss of the functional capacity of even a small component (eg, the RCPm muscles) should not automatically be assumed to have an insignificant impact on the whole body. Fatty infiltration of RCPm muscles would result in a reduction in the total number of contractile elements and would diminish the capacity of these muscles to generate and sustain normal levels of force.
A connective tissue bridge is found between the RCPm muscles and the pain-sensitive spinal dura mater of the posterior cranial fossa.
9,10 The spinal dura contains nociceptive fibers that feed into the cervical nerves. The convergence of trigeminal and cervical afferents and irritation of these fibers (eg, stretching) results in referred headache.
11-14
The functional relationship between RCPm muscles and the spinal dura is not currently known. However, in 2014, Hallgren et al
15 reported that voluntary head retraction results in a significant increase in electromyography activity as RCPm muscles are stretched during posterior movement of the head within the sagittal plane without rotation. Atrophy of the RCPm muscles would be expected to compromise the functional relationship between these muscles and the pain-sensitive spinal dura and is thought to result in abnormal levels of tension within the dura.
16 Head movement is proposed to be an important contributor to cerebrospinal fluid dynamics
17 that are regulated by forces generated from structures within the occipitoatlantal interspace.
18
Early detection of fatty infiltration of RCPm muscles might be beneficial in the assessment and management of a muscle injury that could progress from an acute to a chronic condition. A systematic review
19 revealed that single study populations with neck pain showed a significant association between fatty infiltration in cervical muscles and persistent neck disability. However, the review failed to conclude that there is an association between dysfunction of the cervical spine on MR imaging and clinically important outcomes such as pain and disability. The failure was attributed to the heterogeneity of the studies reviewed, the relatively small sample size of the populations that were studied, and the variety of imaging protocols that were used. Unfortunately, the standard MR protocol that is commonly used for imaging the cervical spine is not adequate to visualize fine structures within the occipitoatlantal interspace,
20 and customized protocols have not been shown to be adequate for accessing the temporal development of fatty infiltration.
18
I set out to develop an MR imaging protocol that would provide the superior image quality necessary to reliably quantify the progression of fatty infiltration over time. The analytic strategy was based on the assumption that asymptomatic participants would not have a significant change in skeletal muscle CSA over 2 weeks. To test this hypothesis, image resolution sufficient to resolve fine structures within the occipitoatlantal interspace and the ability to ensure registration of RCPm muscles between image sets collected at 2 points in time was needed. For this discussion, registration refers to the alignment and overlay of MR image data from a specific point in time with the participant's own MR image data from another point in time.
An email advertisement was used to recruit potential participants from the second-year student population of the Michigan State University (MSU) College of Osteopathic Medicine. Participants were required to be free of head and neck pain; be free of significant motion restrictions; have had no surgical procedures in the region of the upper cervical spine; and have not been involved in a motor vehicle crash within the past 30 days. The age of participants was limited to between 20 and 40 years because a progressive loss of muscle mass has been reported to occur at approximately 50 years of age.
21 The study was approved by the MSU Institutional Review Board.
The research protocol was reviewed with each potential participant. Participation required willingness to complete 2 MR imaging scans, spaced approximately 2 weeks apart. Participants were to be compensated $150 at the completion of the second scan. However, compensation was not conditional upon completion of the study. To be enrolled in the study, potential participants were required to sign an institutional review board–approved informed consent form. Participant metrics of sex (1=woman, 0=man), age, height, weight, and body mass index (BMI) were recorded.
Magnetic resonance imaging data were collected at the MSU Department of Radiology. Participants were scanned using a General Electric Medical Systems Signa HDxt 3.0-T scanner. A conventional spin-echo pulse sequence was used to construct 2 image sets consisting of:
■ 14 sagittal, T2-weighted images with measurement parameters of repetition time, 5250 milliseconds; echo time, 100 milliseconds; slice thickness, 2.5 mm; and in-plane resolution, 0.43×0.43 mm.
■ 24 axial, T1-weighted images with measurement parameters of repetition time, 467 milliseconds; echo time, 13.5 milliseconds; number of excitations, 4; slice thickness, 3.0 mm; and in-plane resolution, 0.625×0.625 mm.
The sagittal image set was used to define the orientation of the axial image planes from which muscle CSA would be quantified. The scan parameters and the orientation of the axial image planes were selected to optimize our ability to manually draw regions of interest (ROI) around RCPm muscle boundaries.
22-24 An in-plane resolution of 0.625×0.625 mm was deemed sufficient to resolve structures within the posterior atlantoaxial interspace. The acquisition time was approximately 8.5 minutes. The following steps were taken to ensure image intensities were quantified within the same region of soft tissue at progressive points in time:
1. Each participant was to complete a baseline scan followed by a second scan performed at least 2 weeks later. The uniqueness of this protocol ensures that accurate registration of the axial image sets taken at the 2 points in time can be achieved. This level of accuracy is necessary when CSA is to be calculated at the same location in 3-dimensional (3D) space for both points in time. Participants were positioned in the magnet so that their forehead was parallel to the table to approximate a neutral head posture.
252. A locator slice was adjusted to pass through both the superior aspect of the odontoid process of the axis (C2) and the posterior arch of the atlas (C1) (
Figure 1 [yellow dots]).
4 Serial slice image data were collected superior and inferior to this locator slice.
Since the RCPm muscles are closely aligned to the midline, the positioning protocol allowed image planes to be aligned approximately perpendicular to the long axis of both the right and left muscles. Accurate ROI can be drawn around specific muscle boundaries by aligning the image plane approximately perpendicular to the long axes of the RCPm muscles.
26,27
Placement of the image plane relative to the long axis of the RCPm muscles is facilitated by using anatomical landmarks unique to each participant and is critical to obtain a good approximation for overlaying data from the 2 scans. Unique anatomical landmarks assist with accurate positioning of the image plane when a participant is scanned at progressive points in time. A degree of accuracy is necessary when CSA is calculated at the same locations in 3D space for both points in time to obtain meaningful CSA values that track abnormal progression. Additionally, image data for both the right and left side of each participant were reformatted about an oblique axis with Analyze 12.0 (AnalyzeDirect) to increase 3D space registration accuracy before data analysis.
Analysis of the CSA data for each muscle began by selecting a slice level that was representative of the central portion of the muscle. Using the Analyze 12.0 software, an ROI was manually drawn around the fascial border of both the left and right RCPm muscles. The software was then used to calculate the descriptive statistics of pixels contained within the ROI. Because the focus of this study was to track pathologic changes over time, the strategy to manually draw an ROI enabled each participant to be their own control and allowed us to see whether the muscle CSA at a specific location in 3D space had changed in time relative to the baseline value.
Manually drawing ROI to obtain muscle CSA has been shown to have high levels of intrarater and interrater reliability, which indicates a high level of repeatability.
28 The protocol orients the image plane approximately perpendicular to the long axes of the RCPm muscles (
Figure 1) and enables the accurate drawing of an ROI around the specific muscle 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 protocol, 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 men had movement artifacts in at least 1 of the 2 scans that was sufficient to degrade the image set(s) to be unusable. Unusable was defined as image sets that were significantly degraded by movement artifact (blurring) that resulted in an indistinct boundary between active (muscle) and passive (fatty) tissues.
The data in a repeated-measures analysis should have a normal distribution and no significant outliers to be 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 scan/second scan) had normal distributions.
The cohort was then divided into 2 groups (women and men) because gender differences were suspected to potentially affect CSA. A 1-way analysis of variance was used to test for a significant difference between height, weight, and mean values of CSA for the left and right RCPm muscles between women and men. A significant difference (P<.05) was found between women and men for weight and mean values of CSA, but no significant difference was found in height.
Finally, a multivariate repeated-measures analysis of variance was used to test the null hypothesis and determine whether there was a within-person effect. The null hypothesis was that no significant difference would be found between mean values of CSA collected from the left and right RCPm at 2 points in time for both women and men. The data sets were checked for outliers using the Explore tool in the AnalyzeDirect software. Participants that had a significant number of data points that were marked as outliers were removed from the final analysis.