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

  • Richard C. Hallgren and Jacob J Rowan
Published/Copyright: March 1, 2019
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The Journal of the American Osteopathic Association
From the journal The Journal of the American Osteopathic Association Volume 119 Issue 3

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.

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

Magnetic resonance (MR) imaging techniques have long been used to differentiate between normal muscle and muscle with fatty infiltrates1,2 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 al4,5 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 events6 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 al15 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 dynamics17 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 review19 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.

Methods

Study Population

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.

Collection of Image Slice Data

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.25

  2. 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.

Figure 1. For image slice data collection, the image plane was oriented approximately perpendicular to the long axes of the rectus capitis posterior minor (RCPm) muscles. A locator slice (red lines) was adjusted to pass through the superior aspect of the odontoid process of the axis (yellow dots) and the posterior arch of the atlas. Serial image data were collected superior and inferior to this locator slice.
Figure 1.

For image slice data collection, the image plane was oriented approximately perpendicular to the long axes of the rectus capitis posterior minor (RCPm) muscles. A locator slice (red lines) was adjusted to pass through the superior aspect of the odontoid process of the axis (yellow dots) and the posterior arch of the atlas. Serial 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.

Image 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.

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.
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.

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.

Statistical Analysis

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.

Results

Twenty-four people (18 men and 6 women) were originally enrolled in the study. After enrollment, it was found that 2 participants had violated the inclusion criteria, and both were excluded from the study. Data from an additional 4 participants were removed because of blurring of the images due to motion artifacts. An additional 5 participants were removed because their RCPm muscles were considered to be too small to obtain an accurate estimate of CSA or they had a significant number of outliers. Therefore, the data from 3 women and 10 men were analyzed in this study. The participants were a mean (SD) age of 24 (2) years, 178 (8) cm, 79 (12) kg, and had a BMI of 25 (4). These characteristics are similar to a population sample from 25-year-old women and women of 172 cm, 75 kg, and BMI of 25.29 All participants except 1 man were right-hand dominant.

Figure 3 shows 2 image slices for the same participant separated by more than 2 weeks. The left (red) and right (green) RCPm muscles are outlined in each image slice. The CSA of the left RCPm muscle on the 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 asymmetry that was commonly seen between the right and left RCPm muscles, with the left side typically having a larger CSA than the right. Fifty-two observations from the 13 participants were included in the analyses, and, thus, from the original 22 participants, 59% of the subsequent observations were kept and 41% were discarded.

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.
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.

Figure 4. Magnetic resonance image illustrating the asymmetry that was commonly seen between the right and left rectus capitis posterior minor muscles. The left side (red) typically had a larger cross-sectional area than the right side (green). The image is viewed from inferior to superior.
Figure 4.

Magnetic resonance image illustrating the asymmetry that was commonly seen between the right and left rectus capitis posterior minor muscles. The left side (red) typically had a larger cross-sectional area than the right side (green). The image is viewed from inferior to superior.

 Figure 5 shows box plots of the data. No significant difference was found between the CSA of either the right or the left RCPm muscles sampled at enrollment and 2 weeks after enrollment (all P>.05). The finding of no significant difference is consistent with our original assumption that asymptomatic participants would not have a significant change in skeletal muscle CSA over 2 weeks.

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.
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.

Discussion

Fatty infiltration of skeletal muscle results in a reduction in the total number of contractile elements and diminishes the capacity of these muscles to generate and sustain normal levels of force. Rectus capitis posterior minor muscles with fatty infiltration have been reported in patients with chronic headache associated with both nontraumatic events6 and traumatic events, such as rear-end motor vehicle crashes.7 Fatty infiltration would not be expected to directly result in headache, but it would weaken the 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 significant impact on the whole body.

After ruling out muscle disease and neurogenic atrophy, the 2 most common causes of fatty infiltration in skeletal muscles are tendon tear and disuse. A tendon tear is a common shoulder injury30 that results in 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 posterior arch of the atlas and have been shown to be forcibly stretched during whiplash-type motions resulting from a rear-end motor vehicle crash.36 It has been proposed but not proven that the passive load displacement properties of RCPm muscles puts them at risk of a strain injury during a rear-end motor vehicle crash.37 A connective tissue bridge is present between the RCPm muscles and the pain-sensitive spinal dura of the posterior cranial fossa.9,10 The spinal dura contains nociceptive fibers that feed into the cervical nerves, and the convergence of trigeminal and cervical afferents results in referred headache.38

A musculotendonous junction tear of the RCPm muscles could result in fatty infiltration that would be expected to compromise the functional relationship between these muscles and the pain-sensitive spinal dura. The spinal dura contain nociceptive fibers that feed into the cervical nerves of the trigeminocervical nucleus. Irritation of these fibers, specifically stretching, is known to result in headache12,14 and has been proposed to be a source of chronic headache.39 We suggest that the spinal dura becomes a source of head and neck pain when the functional integrity of the RCPm muscles are compromised, as might occur during a whiplash-type injury, and the restoration of the normal functional relationship between RCPm muscles and the spinal dura will result in a decrease in headache measures. The imaging protocol developed in this study provides the resolution that would allow 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 (Figure 6).

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.
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.

Fatty infiltration of the RCPm muscles could also be a consequence of disuse atrophy resulting from a forward head posture that is commonly associated with chronic, tension-type headache40-42 but is not seen in patients with migraine.43 Disuse atrophy would also be expected to reduce the functional capacity of the RCPm muscles. Reversal of disuse atrophy could be accomplished through an appropriate exercise program that selectively activates these muscles. A 2014 report15 showed 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. Lengthening of a muscle while it is activated is defined as an eccentric contraction. Eccentric contractions are known to strengthen muscle44 and to reduce forward head posture.45 We hypothesized that voluntary head retraction would strengthen RCPm muscles, as evidenced by an increase in the CSA of the contractile component of the muscles on MR imaging, and that this would be associated with a decrease in headache measures. By tracking CSA using our MR imaging protocol, researchers would be able to quantify the efficacy of treatment.

Significantly more data had to be discarded than originally anticipated, which made the final size of the study cohort the major limitation of the study. The primary reason for the small sample size resulted because of participant movement during MR imaging. To achieve an adequate resolution, the scan time was 8.5 minutes. Participant movement during the scan resulted in blurring of the images, reducing the ability to accurately draw an ROI around a muscle boundary. The small size of the RCPm muscles further exacerbates the difficulty of accurately drawing an ROI.

Conclusion

For a cohort of 3 women and 10 men, there was no statistically significant difference between values of muscle CSA sampled from right and left RCPm muscles taken at 2 points in time. Early assessment of dysfunction that compromises the functional integrity of the RCPm muscles could be a key factor in halting the progression from an acute to a chronic condition.

Author Contributions

Both authors provided substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; both authors drafted the article or revised it critically for important intellectual content; both authors gave final approval of the version of the article to be published; and both authors agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

From the Departments of Physical Medicine & Rehabilitation (Dr Hallgren) and Osteopathic Manipulative Medicine (Drs Hallgren and Rowan) at Michigan State University College of Osteopathic Medicine in East Lansing.
Financial Disclosures: None reported.
Support: None reported.

*Address correspondence to Richard C. Hallgren, PhD, Department of Physical Medicine & Rehabilitation, Michigan State University College of Osteopathic Medicine, 965 Wilson Rd, St B-411, West Fee Hall, East Lansing, MI 48824-1316. Email:

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Received: 2018-06-19
Accepted: 2018-07-02
Published Online: 2019-03-01
Published in Print: 2019-03-01

© 2019 American Osteopathic Association

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

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  3. OMT MINUTE
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  5. EDITORIAL
  6. Building on WVSOM's Mission of Education and Scholarly Activity
  7. ORIGINAL CONTRIBUTION
  8. Advancing Methods of Assessing Bone Quality to Expand Screening for Osteoporosis
  9. Assessment of Pulmonary Function After Osteopathic Manipulative Treatment vs Standard Pulmonary Rehabilitation in a Healthy Population
  10. BRIEF REPORT
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  12. Magnetic Resonance Imaging Parameters Selected for Optimal Visualization of the Occipitoatlantal Interspace
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https://doi.org/10.7556/jaoa.2019.028
Keywords for this article
MR imaging; myodural bridge; rectus capitis muscles; tendon tear
Creative Commons
BY-NC-ND 4.0

Articles in the same Issue

  1. SURF
  2. Point-of-Care Ultrasonography Integration in Undergraduate Medical Education: A Student-Driven Approach
  3. OMT MINUTE
  4. Muscle Energy for the Occipitoatlantal Joint
  5. EDITORIAL
  6. Building on WVSOM's Mission of Education and Scholarly Activity
  7. ORIGINAL CONTRIBUTION
  8. Advancing Methods of Assessing Bone Quality to Expand Screening for Osteoporosis
  9. Assessment of Pulmonary Function After Osteopathic Manipulative Treatment vs Standard Pulmonary Rehabilitation in a Healthy Population
  10. BRIEF REPORT
  11. Thermal and Mechanical Pain Thresholds of Women With Provoked Localized Vulvodynia: A Pilot Study
  12. Magnetic Resonance Imaging Parameters Selected for Optimal Visualization of the Occipitoatlantal Interspace
  13. Prior Knowledge of the Mediterranean Diet Is Associated With Dietary Adherence in Cardiac Patients
  14. JAOA/AACOM MEDICAL EDUCATION
  15. Nelson-Denny Reading Test Scores as a Predictor of Student Success in Osteopathic Medical Education
  16. Just Say Know to Drugs! A High School Pharmacology Enrichment Program for a Rural Population
  17. CASE REPORT
  18. Death of a Fetus With Myeloproliferative Disorder and Trisomy 21
  19. CLINICAL IMAGES
  20. Anemia Diagnosed by Head Computed Tomography
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