444  |  june 2011  |  volume 41  |  number 6  |  journal of orthopaedic & sports physical therapy

[ resident’s case problem ]

The conservative management of neck pain and cervicogenic headache involves physical examination of the lower and upper cervical spine. Clinical evaluation of the upper cervical spine is focused on the assessment

of dynamic movements that occur between the occiput, atlas, and axis, a region referred to as the craniocervical junction (CCJ).

Functional Anatomical ConsiderationsThe occipital-atlanto-axial joints of the CCJ are the most complex joints of the

TT STUDY DESIGN: Resident’s case problem.

TT BACKGROUND: Patients often present to physical therapists with chief complaints of neck pain, occipital headache, and dizziness associated with a past history of cervical spine injury. These symptoms may be associated with various cervical spine conditions, including craniocervical junction (CCJ) hypermobility.

TT DIAGNOSIS: This report reviews the history, physical exam, and diagnostic imaging findings of a patient with the above symptoms. This patient, who had a history of multiple cervical spine injuries, was examined with 2 manual therapy provocative tests: the Sharp-Purser test, which is intended to stress the transverse ligament and odontoid, and the modified lateral shear test, which is intended to stress the alar ligaments. The lateral shear test was perceived as demonstrat-ing excessive mobility and a soft end feel, with a “shift” of C1 on C2. Stress cervical radiographs, obtained using open-mouth projections in neutral, left, and right cervical lateral flexion, revealed a 3-mm lateral offset of the right lateral mass of C1 on C2. MRI evaluation of the lower cervical spine did not reveal any significant disc derangement; however, images of the soft tissues of the cranio-

cervical junction were not obtained. Based on the examination and imaging studies, the patient was determined to have a previously undiagnosed hypermobility of the atlantoaxial joint.

TT DISCUSSION: The patient was advised to avoid rotational manipulation and end range lateral flexion stretching exercises. Axial traction manipu-lation techniques, midrange stabilization exercises, and postural advice appeared to provide good relief of symptoms. Physical therapists should consider the possibility of CCJ hypermobility in the frontal plane when examining the cervical spine in patients with chronic neck pain, headache, and a past history of trauma. The lateral shear test and stress radiography may provide simple screening tests for occult CCJ hypermobility; however, the reliability and validity of these tests is lacking. Further research on diagnosis and management of CCJ hypermobility is warranted.

TT LEVEL OF EVIDENCE: Differential diagnosis, level 4. J Orthop Sports Phys Ther 2011;41(6):444-457. doi:10.2519/jospt.2011.3305

TT KEY WORDS: alar ligament, cervical spine, manual therapy, transverse ligament

1Student (at the time of this case), Doctoral of Physical Therapy Program, University of Pittsburgh, School of Health and Rehabilitation Sciences, Pittsburgh, PA; Chiropractor, private practice, Charleroi, PA. 2Assistant Professor, University of Pittsburgh, School of Health and Rehabilitation Sciences, Department of Physical Therapy, Pittsburgh, PA. 3Instructor, University of Pittsburgh, School of Health and Rehabilitation Sciences, Department of Physical Therapy, Pittsburgh, PA. Address correspondence to Dr K. Sean Mathers, DC, CSCS, PO Box 142, Charleroi, PA 15022. E-mail: sean2001dc@hotmail.com

K. SEAN MATHERS, DC, CSCS1 • MICHAEL SCHNEIDER, DC, PhD2 • MICHAEL TIMKO, PT, MS, FAAOMPT3

Occult Hypermobility of the Craniocervical Junction: A Case Report and Review

SUPPLEMENTAL VIDEO ONLINE

axial skeleton, both anatomically and ki-nematically. The CCJ is best thought of as 2 distinct joint complexes: the occipi-

toatlantal (C0-1) joint complex and the atlantoaxial (C1-2) joint complex. The C0-1 complex con-sists of cup-shaped articulations in the sagittal and frontal planes, allowing for mostly flexion/ex-

tension and lateral flexion, but resisting rotational motion.58 White and Panjabi61 indicate that there is almost no percep-tible axial rotational motion at the C0-1 complex. In contrast, the C1-2 joint com-plex is designed primarily for rotation, with as much as 50% of total cervical ro-tation taking place at this level.58 Very lit-tle to no lateral flexion occurs at the C1-2 complex under normal circumstances.

The suboccipital muscle group, con-sisting of the rectus capitis posterior major and minor, and the superior and inferior oblique, produces active move-ment and provides proprioception and stabilization to the CCJ.38 Andary et al1 demonstrated the presence of muscle atrophy and fatty infiltration of the rec-tus capitis posterior minor on MRI in patients with chronic whiplash injuries. In 2006, Elliott et al12 published a paper examining 113 female subjects (79 with whiplash-associated disorders and 34 healthy controls) and found significantly greater fatty infiltration in the cervical ex-tensors, especially in the deeper muscles of the upper cervical spine. The largest amounts of intramuscular fat were found in the rectus capitis posterior minor and major and the deep cervical multifidii

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journal of orthopaedic & sports physical therapy | volume 41 | number 6 | june 2011 | 445

muscles. In addition to the suboccipital musculature, the levator scapulae, with their attachments to the transverse pro-cesses of C1 through C4, may also provide ancillary muscular stabilization and pro-prioceptive input for the CCJ.

The CCJ contains 2 unique and spe-cialized ligaments that are important stabilizers of the C1-2 articulation: the cruciform ligament and the paired alar ligaments. The transverse portion (FIGURE 1) of the cruciform ligament com-plex is a broad horizontal ligament that runs posterior and across the odontoid process of the axis and restrains the ante-rior displacement of C1 on C2.7 There are also some vertical fibers that attach to the occiput above, and to the vertebral body of C2 below, leading to the composite name of cruciform ligament of the atlas. Essentially, the transverse ligament acts as the primary passive restraint of C1 dis-placement in the sagittal plane.10

There is a pair of alar ligaments (right and left), which both arise from the su-perior aspect of the odontoid process, with 2 distinct attachment sites. The at-lantal attachment blends into the C1-2 joint capsule and the lateral mass of the atlas, and the occipital attachment is con-nected to the occipital condyle (FIGURE 2). The alar ligaments are important pas-sive restraints to axial rotation motions of the atlas on the axis,45,50,63 along with the accessory atlantoaxial ligaments.66 The right alar ligament restrains left axial rotation and vice versa. During lateral flexion, the occipital portion of the alar ligament on the ipsilateral side is relaxed, while the atlantal portion is stretched. Partially due to these differ-ences in stretching forces between the occipital and atlantal portions of the alar ligaments, the spinous process of C2 nor-mally moves contralateral to the side of lateral flexion.23 Thus the alar ligaments

are considered to be important passive restraints to excessive rotation and lateral flexion of the CCJ.10,11,63 Panjabi et al43,44 found that cutting the alar ligaments caused increased motion between C1 and C2 in multiple planes of motion.

Hypermobility/Instability of the CCJ ComplexThis emphasis on descriptions of the transverse and alar ligaments is not meant to imply that they are the only passive restraints of the CCJ. Other structures, including the tectorial mem-brane and accessory atlantoaxial liga-ments, are well recognized passive soft tissue restraints of the CCJ complex.66 The integrity of any of these tissues can be compromised by either (1) acute dis-ruption/tear, or (2) chronic degeneration. Clinicians should be concerned whenever a clinical assessment reveals excessive movement or hypermobility of the CCJ.

Although some mild amount of ex-cessive mobility may be considered within normal limits, moderate to se-vere amounts of hypermobility may lead to mechanical instability, with severe medical consequences. Mild to moder-ate instability of the CCJ is thought to be associated with symptoms of suboc-cipital pain, dizziness, headache, and upper extremity paresthesia.4,36 Severe CCJ instability can lead to catastrophic consequences, including disturbances of bowel/bladder control, impaired gait, motor incoordination, sensory loss, and the extreme instance of death from spinal cord compression.37,49

For these reasons, clinicians who treat patients with neck pain and dysfunction need to carefully consider the possibil-ity of CCJ hypermobility and instabil-ity before considering a treatment plan that includes end range mobilization or stretching techniques involving the CCJ. Clinicians should be cautious when intro-ducing a mechanical force to the CCJ in patients who present with hypermobility of the occiput-C1-2 joint complex. These would include any position or movement known to place excessive stress on the

FIGURE 1. Posterior view of the upper cervical region depicting the anatomy of the transverse ligament. Also note the superior portion of the alar ligaments. From Cramer GD, Darby SA. Basic and Clinical Anatomy of the Spine, Spinal Cord, and ANS. 2nd ed. St Louis, MO: Mosby; 2005. Used with permission from Elsevier Ltd.

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[ resident’s case problem ]ligaments and passive tissue restraints of the CCJ. Appropriate modifications in manual therapy or stretching techniques can be made if the clinician is aware of any underlying CCJ hypermobility.

The literature discusses 3 primary conditions that could contribute to dis-ruption of the overall strength and integ-rity of the transverse and alar ligaments: (1) Down’s syndrome, (2) rheumatoid arthritis, and (3) cervical spine trauma. Down’s syndrome is a genetic disorder involving an extra chromosome that is known to cause abnormalities of liga-ment integrity, including changes in the collagen matrix of the transverse liga-ment of the atlas. Although rare, some cases of death in individuals with Down’s syndrome have been reported due to spi-nal cord compression during physical trauma or sporting injuries, presumably from undetected instability of the CCJ.49

Rheumatoid arthritis is an autoim-mune disease that causes inflammation of various periarticular soft tissues, spe-cifically the upper cervical ligaments and the synovial membranes of the joint cap-sules between the occiput, C1, and C2. Up to one third of patients with rheumatoid arthritis may show degenerative/erosive changes in cervical spine joints upon ra-diographic evaluation.15

Lastly, the ligaments of the CCJ can be acutely damaged in some individuals following a motor vehicle collision and other types of physical injury.42,60 One hypothesis is that the alar ligaments are more likely to be sprained during auto accidents in which the head is rotated to one side during impact.9,28,34 It has been noted that the alar ligaments could be ir-reversibly stretched after trauma, as they consist chiefly of inelastic collagen fibers potentially leading to chronic occult hy-permobility of the CCJ region.3

Diagnostic ConsiderationsPhysical examination procedures, stress radiography, and specialized upper cervi-cal MRI techniques can be used as diag-nostic tests for hypermobility of the CCJ.

Two physical examination procedures

have been developed to screen for CCJ hypermobility: the Sharp-Purser test and the lateral shear test.35 Both tests are based on the premise that manual overpressure applied to lax ligaments will lead to the palpatory sense of exces-sive segmental motion, assessed with the Sharp-Purser test as abnormal flexion movement of the atlas and with the lat-eral shear test as abnormal lateral trans-lation of the atlas. The Sharp-Purser test explores the integrity of the transverse ligament in the sagittal plane and is per-formed by placing one hand over the pa-tient’s forehead, while the thumb of the other hand is placed over the C2 spinous process for stabilization. The patient is asked to flex the head on the neck, while the examiner applies a posteriorly di-rected force on the forehead. The test is considered positive if there is backward movement of the head, which may be ac-companied by a “clunk.” The backward movement indicates that the subluxation of C1, produced by the slight forward flexion of the neck, has been reduced. The test has demonstrated a sensitivity of 0.69, a specificity of 0.96, and positive and negative likelihood ratios of 17.25 and 0.32, respectively, when compared with a radiographic reference standard in patients with rheumatoid arthritis.57

The lateral shear test screens for the integrity of the alar ligaments in the fron-tal plane. It is performed with the patient lying supine, while the examiner places the metacarpophalangeal joint of the sec-ond digit against the transverse process of the atlas on one side and the metacar-pophalangeal joint of the second digit of the contralateral hand on the transverse process of the axis on the opposite side. The 2 metacarpophalangeal joints are pushed toward one another, causing a shear force of C1 across C2. The test is considered positive when the examiner feels an increased transitory “shift,” or motion, between the 2 bones and/or patient symptoms are provoked by the maneuver.16 There are no reliability or validity data for the lateral shear test. Aspinall3 provides a comprehensive de-scription of additional testing techniques to assess CCJ hypermobility.

During examination of the individual in this particular case, the lateral shear test was modified from the description above. The examiner palpated the trans-verse process of C1 with the distal pha-lanx of the second digit of both hands. Overpressure was applied to one side, and a shift of the contralateral transverse process was assessed with palpation us-ing the contralateral digit. Kaale et al27

FIGURE 2. Posterior view with transverse ligament removed, showing the alar ligaments. Note that the atlantal part of the alar ligaments blends into an attachment with the C1-2 joint capsule. From Cramer GD, Darby SA. Basic and Clinical Anatomy of the Spine, Spinal Cord, and ANS. 2nd ed. 2005. St Louis, MO: Mosby; 2005. Used with permission from Elsevier Ltd.

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reported substantial agreement (k = .70-.90) between the clinical examination of passive intervertebral movements related to the CCJ ligaments and soft tissues and MRI assessment of these tissues when us-ing a dichotomous grading scale of nor-mal versus abnormal findings.

Another diagnostic procedure to de-tect alar ligament laxity is the use of ante-rior-to-posterior open-mouth (AP-OM) radiographs, with the head in neutral and in right and left lateral flexion positions. This is typically performed to rule out se-rious instability secondary to pathology or anomalies of the C1 and C2 vertebrae, such as os odontoideum or fracture of the dens/body of C2.54 However, it is also possible to visualize the movements of C1 on C2. It is proposed that 2 findings will be visualized if alar ligament laxity is present: an ipsilateral “offset” at the lateral margins of C1 on C2, along with the inset of the contralateral side and a lack of C2 spinous rotation contralater-ally (FIGURES 3 and 4).21

Standard cervical MRI scans do not adequately visualize the small ligaments of the CCJ region. These ligaments and other soft tissues of the CCJ region can

be directly visualized using special high-resolution MRI techniques with thinner slices in the frontal and sagittal planes.

DIAGNOSIS

Case Presentation

In 2009 a 32-year-old female pre-sented to the clinic with chief com-plaints of chronic neck pain, severe

occipital headache that radiated behind her eyes, and dizziness. She also com-plained of intermittent paresthesia in the upper extremities bilaterally. At the time of initial examination, she was tak-ing Oxycontin (20 mg twice daily) and Topamax (75 mg twice daily). She stated that these medications had become rela-tively ineffective at reducing her symp-toms. Her baseline pain and function were assessed with the numeric pain rating scale (NPRS), the Neck Disabil-ity Index (NDI), and the Headache Dis-ability Index (HDI). The 3 NPRS scores indicated a current pain level of 3/10 (0, no pain;10, maximal pain), best pain level in past 24 hours of 2/10, and worst pain in past 24 hours of 6/10.65 The NDI was 48/100 and the HDI was recorded as

82/100 (both scales: 0, no impairment; 100, maximum impairment). These in-struments measure self-perceived im-pairment of activities of daily living due to neck pain and headaches, respectively.25,58

The patient related a history of previ-ous cervical spine and head injury from a physical assault 16 years prior to this examination, when she suffered multiple blows to her head and neck that resulted in a loss of consciousness for 2 days. She stated that after this episode she started to have episodes of neck pain and head-aches, which eventually became chronic and progressively more recurrent. She reported difficulty with such activities as shampooing her hair and standing at the kitchen sink turning her head to retrieve a plate to wash. She also stated that she had tried various types of chiro-practic and physical therapy treatment with little relief. Her primary care physi-cian had prescribed the previously noted medications, but due to lack of relief she presented for a neurosurgical evaluation in late 2008.

The neurosurgeon did not find any abnormal neurological signs but ordered an MRI of the cervical spine that revealed mild generalized degenerative disc dis-ease and mild/moderate left C3-4 neural foraminal narrowing. The patient re-called that the surgeon suggested surgery to fuse the cervical spine from C2 to C7. She did not want to undergo such exten-sive surgery and therefore sought out the current clinical evaluation as a nonsurgi-cal option for her chronic pain.

Review of past medical history, includ-ing a review of systems, was performed and revealed no high blood pressure or other cardiac conditions. The patient had fusion surgery of the lumbar spine at L3-4 in early 2008. The patient did not have any significant past or current medi-cal problems but was noted to be some-what anxious during the examination.

Tests and MeasuresSeated blood pressure was taken follow-ing the interview and was 110/72 mm-HG. Physical examination began with

FIGURE 3. Normal. The CCJ is coupled with rotation. In neutral (the center figure), during neutral the C2 spinous process (E) is in midline and the spaces between the dens and the lateral masses (A and B) are symmetrical. During lateral flexion, counterrotation of the C2 spinous process occurs due to the posterior insertion of the alar ligaments on the odontoid and occiput and the symmetry of the lateral masses (C and D) over the body of C2 is maintained. Compare to actual radiographic images in FIGURES 5 and 7.

FIGURE 4. Abnormal lateral flexion mechanics of the CCJ. The normal biomechanics are disrupted. In this example, during right lateral flexion, there is no counterrotation of the C2 spinous process, and note the right translation of the right lateral mass over the body of C2, due to the failure of the left alar ligament. Compare to radiographic image in FIGURE 6.

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[ resident’s case problem ]

visual analysis of posture, followed by active range-of-motion (ROM) testing of the cervical spine. Although assess-ment was nonpainful and within normal values, the patient reported feeling dizzy when she rotated her neck to the right, as well as with right lateral flexion. Addi-tional provocative testing was performed with patient seated, asking to hold her head in full right rotation, left rotation, and then extension for 15 seconds each. In each position the patient experienced immediate dizziness and nausea, while maintaining the position for 15 seconds. The symptoms resolved immediately upon returning to neutral. A brief cra-nial nerve assessment was performed. There was no nystagmus, facial asymme-try, deviation of the tongue, or slurring of words. Although the patient had pro-vocative symptoms with cervical rotation and extension, the absence of nystagmus and other abnormal cranial nerve find-ings suggested that additional physical examination procedures were reasonable to pursue.

After the cranial nerve screening, a more comprehensive set of neurological tests was performed. Upper extremity re-flexes were found to be bilaterally present and symmetrical. No sensory deficit was

noted upon soft touch testing in the der-matomes of the upper extremities. Motor strength of the upper extremity muscles, assessed with manual muscle testing, revealed no gross motor deficits. Hoff-man’s reflex52 was negative bilaterally, and ankle clonus was not present. Stand-ing with her feet together and eyes open/closed (Rhomberg’s test) did not reveal any loss of balance. Hautant’s test35 was performed in a seated position. This test involves the patient closing the eyes with the arms outstretched and forearms su-pinated. The examiner then observes for loss of arm position. If either arm moves in this position, the cause is considered nonvascular. If there is no arm move-ment, then the patient is asked to rotate or extend and rotate the neck while keep-ing the eyes closed. If wavering of the arms occurs, the dysfunction is consid-ered to be from a vascular impairment. This patient demonstrated a positive test during left cervical rotation, with an up-ward “drift” of the left arm. Because of the lack of any other central nervous sys-tem signs (ie, dizziness, facial asymmetry, dizziness, or nystagmus associated with Hautant’s test with this patient), it was felt that her signs were more suggestive of cervical spine dysfunction.

The examination continued with the

assessment of the craniocervical liga-mentous structures. The Sharp-Purser test (ONLINE VIDEO) was performed with the patient seated and the head brought into flexion. No discernable movement or reduction was noted with overpres-sure applied through the forehead. A modified version of the lateral shear test was performed in the supine position (ONLINE VIDEO). A noticeable shift, or later-al translation, was palpated when press-ing on the left C1 transverse process in an attempt to move the C1 segment from left to right. No such translatory motion was palpable when attempting to move C1 from right to left. The examiner pal-pated the spinous process of C2 and pas-sively brought the CCJ in lateral flexion to feel for conjunct rotation of the C2 spi-nous process. During right lateral flexion, the examiner was not able to feel the C2 spinous process rotating to the left. This finding was consistent with the results of the modified version of the Lateral Shear test. A decision to conclude the physi-cal examination was made at this time. Radiographic imaging was deemed nec-essary prior to initiating any additional examination or treatment procedures.

Diagnostic ImagingAfter completing the physical examina-

FIGURE 5. Open-mouth cervical radiograph taken in neutral, showing normal symmetrical spacing between the odontoid process and lateral masses of atlas, and the absence of lateral shift of the lateral masses.

FIGURE 6. Open-mouth cervical radiograph taken in right lateral flexion. Arrow points to the 3-mm offset of right lateral mass of atlas on the body of axis, which is suggestive of left alar ligament laxity.

FIGURE 7. Open-mouth cervical radiograph in left lateral flexion. Arrow points to the left lateral mass of atlas, which does not extend beyond the margin of the body of axis.

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tion, there were several key factors in this patient’s presentation that suggested occult CCJ hypermobility in the frontal plane that might warrant confirmation with diagnostic imaging: (1) past history of cervical trauma, (2) positive lateral shear test, (3) symptom provocation and arm drift with cervical rotation/exten-sion, and (4) asymmetrical movement of the C2 spinous process with lateral flexion.

To confirm hypermobility of C1-2, the patient was sent by the examiner to obtain radiographs of the upper cervical spine in lateral flexion through open-mouth projections. Lateral views radio-graphs in flexion and extension were also

performed. The open-mouth projections revealed that, on right lateral flexion, there was 3 mm of lateral translation of the right lateral mass of C1 with respect to C2, and normal alignment (0 mm of translation) of the left lateral mass of C1 on C2 during left lateral flexion (FIGURES

5-7). The findings were consistent with the results of the physical exam and ap-peared to confirm the clinical suspicion of hypermobility at C1-2.

Impression and Initial Plan of CareFIGURES 8 and 9 provide an overview of the decision-making process in this case and an algorithm of the “at risk” physical examination process that was used. The

TABLE provides a list of the key differential diagnostic considerations that were con-sidered. The results of this assessment process, coupled with the radiographic results, suggested that this patient pre-sented with features most consistent with a diagnosis of cervicogenic pain/headache syndrome, with signs of hypermobility in the region of the CCJ (category 5 in the TABLE). As the patient did not exhibit any abnormal neurological signs, more seri-ous diagnoses were ruled out (categories 1, 2, 3, and 4 in the TABLE).

Given the presence of hypermobility of the CCJ, the initial treatment plan was conservative and consisted of cervical stabilization exercises using the Stabi-lizer Pressure Biofeedback unit (Chat-tanooga Group, Inc, Hixson, TN), as described by Jull and colleagues,26 and performing head lifts with chin tucked in to facilitate reactivation of the deep cervical flexors.41 Eye/head coordination exercises32 in standing were used for pro-prioceptive training. Postural exercises, focusing on cervicoscapular stabilizers/scapular mechanics, featuring latissimus dorsi pull-downs, upright rows, prone strengthening of the middle and lower trapezius musculature,41 and upper body ergometry with postural control instruc-tions, were also performed. Specific strengthening exercises of the left leva-tor scapula, along with mobilization of the upper thoracic spine, were also in-corporated into the plan of care. A home exercise program of trunk stabilization exercises, consisting of bridging, prone planks, and side planks, was provided to the patient.

Initial OutcomeAfter 4 weeks of treatment 3 times per week, the patient demonstrated no sig-nificant change in her pain level or NDI score. The HDI demonstrated a 20-point reduction from baseline; however, this failed to meet the minimal clinically im-portant difference of 29 points.25

Due to the patient’s minimal response to this conservative course of physical therapy and growing concerns about the

• Patient reports of head and neck pain• Fractures/dislocation and acute disc rupture have been

ruled out• No apparent concerns/indication for medical

disease/pathology

Is patient presenting with any of the following clinical concerns?

• History of trauma to head/neck region• History of motor vehicle accidents or multiple motor

vehicle accidents• Frequent, persistent headaches of increasing severity• Sensation of dysequilibrium• Suboccipital pain• Facial symptoms• Hemibody symptoms• Difficulty with speech/swallowing• Visual disturbances• Gait disturbances• Radiating pain/paraesthesia in any or multiple

extremities

Yes No

“At risk” assessment required

Proceed to standard upper quarter screening exam

FIGURE 8. Overview of decision-making rationale.

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[ resident’s case problem ]radiographic findings suggestive of occult CCJ hypermobility, the patient felt that another consultation with a neurosur-geon to discuss these concerns was war-ranted. The managing clinician in this case supported her desire to seek an addi-tional opinion and facilitated a follow-up consultation with the same neurosurgeon she had previously seen. During the con-sultation, the neurosurgeon told her that the lateral translation of C1-2, visible on the radiographs, did not require surgi-cal stabilization and was due to “normal degenerative changes.” When asked what was causing her persistent neck pain, headaches, and dizziness, it was suggest-ed by the neurosurgeon that her symp-toms were related to “stress.”

ReexaminationThe patient was not satisfied with the neurosurgical consultation and returned for a follow-up clinical evaluation after a 4-week lapse in treatment. She re-ported that her symptoms had worsened over the past month but denied any new trauma or injury. Headache frequency was described as daily and frequently ac-companied by nausea. The examination was performed, which included collect-ing data on pain and disability. The pa-tient’s NPRS scores indicated a current pain of 6/10, and best and worst pain levels in past 24 hours of 4/10 and 8/10, respectively. The patient’s NDI score was 77/100, and her HDI score was 88/100. The patient was anxious and frustrated with the lack of progress and was un-sure of her clinical status. When it was explained to her that her condition, ac-cording to the neurosurgeon, did not warrant surgery, it appeared to improve her perceived health status and her un-derstanding of the need to be an active participant in her treatment plan. Fur-thermore, her anxiety level appeared dramatically reduced.

A differential diagnosis of benign par-oxysmal positional vertigo (BPPV) was considered during the second course of treatment. The Dizziness Handicap In-ventory was administered, but the sub-

scale score, which has been suggested by Whitney et al62 to indicate when the Dix-Hallpike maneuver should be performed, did not reach the level found in most pa-tients with BPPV. In addition, when care-fully questioned about her symptoms, the patient only reported feelings of dizziness but no true vertigo. This made the diag-nosis of BPPV very unlikely.

Follow-up examination of the neck

and upper quarter continued to reveal that there were no signs suggestive of neurological deficit. The patient’s re-flexes remained bilaterally active and symmetrical, and there continued to be no sensory or motor deficits in the up-per extremities. Full cervical rotation and lateral flexion motions again pro-voked her symptom of dizziness, but her overall cervical ranges of motion were

Any relevant contraindications for active physical exam?

If yes, referral is indicated

No

Suggested active physical exam procedures (performed in weight-bearing positions):

• Blood pressure, heart rate measures• Rhomberg, unilateral stance sequence• Hautant’s test• Reflex testing, including Hoffman’s test, ankle clonus• Seated, single movement tests of cervical spine• Seated, sustained movement tests of cervical spine• Sharp-Purser test• Cranial nerve exam

Any substantial clinical findings suggesting medical referral?

If yes, referral is indicated

No

Proceed to non–weight-bearing passive, tissue stress exam

Suggested passive, tissue stress procedures:• Positional testing for upper cervical segments• Upper cervical ligament stress tests• Progressive minimized DeKleyn’s test• Upper cervical segmental mobility testing• Midcervical segmental mobility testing

Differential diagnostic considerations (see TABLE)

FIGURE 9. “At risk” assessment, suggested physical examination.

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within expected limits. The modified lateral shear test was performed again, and the same noticeable shift of C1 lat-eral translation was palpated from left to right. All of these findings remained consistent with her previous examina-tion findings. However, it appeared that the severity and irritability of her symp-toms had increased.

During this second examination, ad-ditional attention was given to the status of the musculature of the CCJ region. Palpation of the cervical spine revealed local tenderness over the right C0-1 and C1-2 joints, with associated hypertonic-ity in the right suboccipital muscles.56 To assess the levator scapula for increased tone, the patient’s head and neck were brought in lateral flexion opposite the side to be tested, and the clinician placed one hand against the lateral side of the head, while the patient actively abducted the contralateral extremity into full eleva-tion, attempting to touch the humerus to the ear. In the starting position of this test, both the upper trapezius and leva-tor scapula are placed on stretch. How-ever, when the upper extremity becomes elevated, the upper trapezius shortens as the levator scapula elongates, due to the medial angle of the scapula moving in-feriorly and laterally on the thorax. Nor-mally, a slight decrease of lateral flexion of the head is allowed at the end of the movement; however, with increased tone in the muscle, as noted in this patient, the head immediately presses against the cli-nician’s fingers in an attempt to lessen the amount of neck lateral flexion and reduce tension on the overactive levator scapula musculature.14

Modified Plan of CareThe treatment protocol was modified to include the following 4 components: (1) occipital glide mobilization,17 (2) traction manipulation of the occiput,17 (3) specific scapular stabilization exercises,15 and (4) upper thoracic mobilization. The primary rationale for these components, as sug-gested by Erhard,14 was to inhibit some of the increased activity in the right suboc-

cipital and levator scapulae muscles and to relieve some stiffness from the upper thoracic region (FIGURES 10 and 11).

The specific scapular stabilization exercises prescribed for this patient in-cluded prone scapular depression and prone shoulder elevation, as described by Erhard.14 During the scapular depres-sion exercise, the clinician places the web space of the hand on the inferior angle of the scapula and passively elevates the pa-tient’s scapula. Then the patient actively depresses the scapula against the stimu-lus of the clinician’s hand. The prone shoulder elevation exercise requires that the patient, with the hand down at the side, start by moving the hand to the floor, then, in the latter phase, move the arm against gravity into full elevation. The clinician looks for abnormal scapu-lar mechanics, either the scapula ceasing to move inferiorly during the range or beginning to move superiorly. In either case of abnormal movement, the patient must stop and work on small incremen-tal elevation as long as biomechanics are normal.14 These exercises were used to reestablish normal scapulothoracic rhythm by making sure that the scapula did not elevate prematurely during arm elevation or abduction. Thoracic mobi-lization was applied with the intent of restoring motion to the upper thoracic segments and upper ribs, to help further facilitate normal scapulothoracic move-ment and to assist with reducing postural stiffness.

Patient Response to Modified Plan of CareAfter 3 treatment sessions over a 9-day period, the patient reported good relief of all of her symptoms. At the fourth treat-ment session, the patient’s current pain intensity and worst and least pain inten-sity over the previous 24 hours were re-ported as 2/10. The patient also indicated that her headache frequency was sub-stantially reduced. She was discharged from treatment and contacted by phone 6 months later, at which time she reported that she had not experienced any signifi-cant change in status since discharge and

was much improved.

DISCUSSION

This case is presented as an ex-ample of the clinical presentation and decision making that led us to

suspect occult hypermobility of the CCJ spine in a patient with chronic symptoms of neck pain, headache, and dizziness. Al-though this report represents just 1 pa-tient, we have seen numerous cases over the years that appear to follow the same clinical pattern: chronic symptoms, visits to multiple healthcare providers, a his-tory of cervical spine trauma, symptoms provoked by cervical extension and/or rotation, and a lateral shift of C1 noted on physical examination. These patients typically have negative MRI and routine radiographic results but demonstrate lat-eral displacement of C1 on C2 with sub-sequent open-mouth lateral flexion stress cervical radiographs.

From our clinical experience, we be-lieve that occult hypermobility of the CCJ complex may be more common in the clinical setting than currently suspected and may frequently go unrecognized. The true prevalence and incidence of this con-dition in the population of patients with chronic neck pain is presently unknown. This is confounded by the lack of any current gold standard diagnostic test or physical examination procedure to detect CCJ hypermobility. There is also a lack of any current clinical guideline outlin-ing the best treatment approach for this type of patient.

Although our patient reported a suc-cessful clinical outcome, the treatment methods used with this case are not gen-eralizable to all patients with chronic neck pain, headache, and dizziness. Cli-nicians should have experience in the management of complex cervical spine disorders before utilizing manual therapy in the CCJ region. The utilization of ma-nipulation to the cervical spine should be performed judiciously, after a systematic differential diagnostic process has been performed. The real value of this case is

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[ resident’s case problem ]

TABLE “At Risk” Differential Diagnostic Considerations

Abbreviations: AROM, active range of motion; BP, blood pressure; BPPV, benign paroxysmal positional vertigo; DHI, dizziness handicap inventory; DTR, deep tendon reflex; HR, heart rate; LE, lower extremities; UE, upper extremities.*5 Ds: dizziness, diplopia, dysphagia, dysarthria, drop attacks; 3 Ns: nystagmus, numbness (unilateral), nausea.

Diagnostic Categories Probable Signs and Symptoms

(1) Cervical artery disease • Suboccipital headache (severe)

• Facial symptoms: 5 Ds, 3 Ns*

• Positive medical history for cardiac factors

• Increased heart rate, increased blood pressure

• Positive Hautant’s test, positive DeKleyn’s test, with positive cranial nerve exam

(2) Cervical myelopathy • Bilateral lower extremity or bilateral upper extremity paraesthesia

• Quadrilateral paraesthesia

• Bilateral lower extremity or bilateral upper extremity weakness

• Gait/balance disturbances

• Positive Hoffman’s sign, DTR hyperflexia, ankle clonus, positive Babinski sign

• Full flexion with radiation (Lhermitte’s sign)

• Positive Rhomberg’s test and/or Hautant’s test

(3) Cervical radiculopathy • Unilateral upper extremity pain/paraesthesia

• Radiating symptoms with certain movement/position of head

• Bakote sign (relief with elevated arm)

• Positive myotome, dermatome, and/or reflex changes

• Worsens with neck compression, improves with neck distraction

(4) Benign paroxysmal positional vertigo (BPPV) • Dizziness/vertigo in response to positional change

• DHI positive for BPPV subscale

• Positive Hautant’s test, positive DeKleyn’s test (dysequilibrium), with negative cranial nerve exam

• Positive Dix-Hallpike test

(5) Cervicogenic pain/headache syndrome with signs of

hypermobility/instability

• Positive history cervical trauma and/or multiple incidents

• Suboccipital pain

• No facial symptoms, no radiating symptoms

• Positive Hautant’s test, limited AROM neck movement

• Negative DeKleyn’s test, negative cranial nerve exam

• Positive ligament stress test(s), abnormal end feel

• Indications for stress film work-up

(6) Cervicogenic pain/headache syndrome without signs

of hypermobility/instability

• Positive history cervical trauma and/or multiple incidents

• Suboccipital pain

• No facial symptoms, no radiating symptoms

• Positive Hautant’s test, limited cervical AROM

• Negative DeKleyn’s test, negative cranial nerve exam

• Positive indications for myofascial pain syndrome

(7) Psychological distress component • Elevated self-reports/questionnaire scores

• Exhibits kinesiophobic traits/catastrophizing tendencies

• Apprehension about being examined, difficulty completing physical exam, and/or inconsistent physical exam findings

(8) Postconcussion syndrome • Positive history of cervical trauma/multiple trauma

• Headache, dysequilibrium, fatigue, activity intolerance

• Memory/concentration/mental exertion difficulties

• Positive neurologic/cognitive findings

• Positive or negative cervical exam findings

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not in the particular treatment methods used with this patient but in the clinical decision making and reasoning used to determine why this patient had ongoing symptoms, despite apparently negative diagnostic tests and examinations and numerous other treatment approaches.

There are 3 important issues sur-rounding this case that require further discussion: (1) diagnostic imaging of the CCJ, (2) physical examination procedures of the CCJ, and (3) psychological stress in chronic pain syndromes.

Diagnostic ImagingThe use of lateral view stress radiographs to measure the atlantodental interspace in the neutral and full-flexion positions is considered a gold standard diagnostic test for determining CCJ instability in the sagittal plane, with normative data sug-gesting that any atlantodental interspace greater than 3 mm in an adult patient is concern for potential instability. Howev-er, there are no standardized normative values for measurements of the lateral displacements of C1 in the frontal plane when measured from open-mouth ra-diographs obtained at end range lateral flexion.

Taniguchi et al53 used dynamic AP-OM lateral flexion radiographs and re-ported an atlantodental lateral shift as the indicator of lateral instability of the C1-2 joint in patients with rheumatoid arthritis compared with healthy con-trols.53 They reported that dynamic lat-eral instability of the C1-2 joint noted on lateral flexion radiographs was just as prevalent as anterior C1-2 instabil-ity noted on flexion radiographs. It was concluded that stress radiographs show-ing dynamic instability in either the sag-ittal plane (lateral, flexed cervical spine view) or frontal plane (lateral flexion of the cervical spine, open-mouth view) were useful for making the diagnosis of early atlantoaxial disease in patients with rheumatoid arthritis.

Reich and Dvorak47 performed open-mouth lateral flexion radiographs on 26 patients with rheumatoid arthritis with

confirmed sagittal plane C1-2 instabil-ity and 31 control subjects. They found that individual in both groups had some amount of lateral C1 motion, with sig-nificantly more motion occurring in the patients with rheumatoid arthritis. The average lateral displacement for the con-trol group was just under 1 mm (range, 0.1-2.2 mm), compared to an average of just under 2 mm (range, 0.6-3.8 mm) for those with rheumatoid arthritis.

Howe21 presented a case report of a pa-tient with cervical trauma and a control patient, both of whom had open-mouth lateral flexion radiographs performed. According to that author, during normal lateral flexion, up to 2 mm of lateral ex-cursion of C1 on C2 to the same side of the lateral flexion normally occurs and should be symmetrical bilaterally. His patient with cervical trauma exhibited ra-diographic findings similar to those of the present case, with a unilateral offset of the lateral mass of C1 on C2 that was not seen on the radiographs of the control patient.

Increased ligament signal intensity on high-resolution proton density-weighted magnetic resonance scans can also be used as an indication of damage to the

transverse and alar ligaments in some pa-tients with chronic whiplash-associated disorders.30 However, increased MRI sig-nal changes have also been found in the alar ligaments of asymptomatic patients, which brings into question the utility of the grading schema for making a diagno-sis of structural ligamentous disruption.39 The data on interexaminer reliability of MRI evaluation of alar ligament signal intensity changes are mixed, with Roy et al48 finding poor to fair interobserver agreement and Krakenes et al31 report-ing moderate to good agreement between radiologists trained to evaluate MRI im-ages using a specific grading system.

Krakenes et al31 reported that the alar ligaments are particularly vulnerable to trauma when the head is rotated on the neck at the moment of impact. Kaale et al28 performed MRI scans on 92 patients with whiplash-associated disorders re-sulting from accidents that occurred 2 to 9 years prior to examination and found increased signal intensity on MRI, sug-gestive of chronic lesions of the alar liga-ments, in 66% of these patients. Vetti et al59 performed cervical MRI of 1266 in-dividuals with neck trauma. They found abnormally increased signals over the alar ligaments in approximately 35% of the cases and abnormal signals over the

FIGURE 10. Supine traction manipulation of occiput. This technique is intended to mobilize the C0-1 joint with an axial traction force. The head is slightly tilted away from the side of the joint. Care is taken to avoid any rotational forces at the C1-2 joint. See Grieve17 for a more detailed description of this technique (ONLINE VIDEO).

FIGURE 11. Supine occipital glide technique. The patient’s head is stabilized by the therapist’s shoulder, while the hands are placed on the occiput. Gentle retraction and flexion movements are induced with the intent of providing a mild stretch of the suboccipital muscles. See Grieve17 for a more detailed description of this technique.

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[ resident’s case problem ]transverse ligaments in approximately 25% of the cases, and concluded that it was unlikely these changes represented age-dependent degeneration.59 How-ever, others have reported findings of increased MRI signals over the alar liga-ments, questioned the diagnostic utility of visualizing “abnormal” signals over the alar ligaments, and found it hard to dif-ferentiate from normal variants.5

There is currently disagreement about whether increased MRI signal intensities over the CCJ ligaments represent signifi-cant abnormality or normal anatomical variation. Standard cervical MRI cannot assess whether the ligaments have been overstretched and become lax, because standard MRI evaluation shows only static anatomy and not dynamic function.

Dynamic MRI evaluation of the CCJ is a promising new technology for as-sessing the integrity of this region. Lind-gren et al,33 comparing 25 patients with whiplash-associated disorders to 25 age-matched and sex-matched controls, found that the patients with whiplash-associated disorders demonstrated sig-nificantly more abnormal alar ligament MRI signals and more abnormal motion at C0-1-2 than the controls. The biggest limitation in the use of dynamic MRI as a routine screening test is the high cost of the procedure, whereas the use of dy-namic open-mouth radiographs is quite cost effective and involves a relatively low radiation dosage.

Physical Examination ProceduresAnother clinical issue that arises from this case report relates to the clinical utility of common physical exam pro-cedures used to assess the structures of the upper cervical spine. Many clini-cians routinely screen for vertebral ar-tery disease using a variety of sustained cervical rotation/extension procedures, such as DeKleyn’s test.35,55 These tests are not specific to the cervical arteries, as they apply stress to the articulations of the cervical spine. Hautant’s test has been suggested to be useful to differenti-ate dizziness caused by vascular versus

articular problems.35 However, no reli-ability or validity data exist to establish the diagnostic accuracy of this test. The sustained end range position of cervical rotation and extension employed in both Dekleyn’s and Hautant’s tests may pro-voke symptoms of dizziness and nausea by other nonvascular mechanisms aris-ing from the cervical spine.

This patient did not have any central nervous system abnormalities sugges-tive of vascular dysfunction, such as nys-tagmus, facial numbness, facial muscle weakness, etc. In our opinion, the mere provocation of dizziness with these ma-neuvers is not as clinically relevant as the negative findings from the cranial nerve examination. Kerry et al29 published a re-port of 2 cases that highlighted the limi-tations of using provocative tests alone as incomplete clinical reasoning. The validity of these tests in the detection of vertebral or carotid artery dissection is questionable, due to their poor sensitiv-ity and specificity that has led some au-thors to suggest abandoning their routine use as screening tests.6,19,20,55 The Sharp-Purser test has been shown to have good reliability and validity for the detection of sagittal plane instability (integrity of transverse ligament) of C1-2, when compared to the gold standard of lateral-view cervical flexion stress radiographs, in individuals with rheumatoid arthritis. However, there is only minimal evidence on the reliability or validity of other physical examination procedures that are used to detect CCJ hypermobility in other planes of motion, such as the lateral shear test and palpation of C2 spinous process rotation with neck lateral flexion. The re-sults of these physical exam procedures would need to be compared to those from an established reference standard test.

Kaale et al27 compared the results of passive mobility testing of the CCJ liga-ments and soft tissues with the reference standard of high-intensity signals over these tissues found on MRI. There was substantial agreement between the clini-cal and MRI assessments (k = .70-.90), when using a dichotomous grading scale

of normal versus abnormal findings.27 They described their clinical assessment of the alar ligaments in the following manner: both hands are placed on the same side of the person’s cervico-occip-ital junction; the lower hand stabilizes C2 by pressing fingers 2 and 3 against the lateral aspect of C2 and pulling this part backward. The test of the ligament is performed by an upward pull into rota-tion with 2 fingers of the left hand, with 1 finger placed (finger 3) under the lateral mass of the atlas and finger 2 placed un-der the mastoid process. The test is per-formed with different angles of cervical rotation to locate the exact test position that gives the maximal movement be-tween C1-2.

Though this study by Kaale et al27 used static MRI of the alar ligaments as the reference standard, there is contro-versy as to whether static MRI versus dynamic MRI is the more appropriate reference standard for detecting liga-mentous instability. We used a modified version of the lateral shear test and pal-pation of the C2 spinous process rotation as the physical examination procedures to detect frontal plane CCJ hypermobil-ity in our patient. Just as the validity of the Sharp-Purser test was tested using cervical flexion stress radiographs as the reference standard, we propose that the validity of these exam procedures could be tested using open-mouth lateral flex-ion stress radiographs as the reference standard. Alternatively, dynamic cervical MRI could serve as a reference standard for validity testing when this technology becomes more readily accessible.

Psychological Stress in Chronic Pain SyndromesPatients with chronic pain syndromes often display varying amounts of psycho-logical stress that impact clinical man-agement and outcomes. Some patients may show overt signs of fear-avoidance behavior, such as reluctance to perform certain simple exercises, disproportion-ate expressions of pain during minimal activities, or exaggerated responses to

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nonprovocative physical examination procedures.40 In others, these behavioral signs may not be obvious, but the report-ed levels of pain may not be congruent with the levels of self-reported disability/impairment.

At her initial visit, this patient re-ported a current pain level of 3/10, but her NDI score was 48/100 and her HDI score was 82/100. Upon reexamination, she reported a pain level of 6/10, with an NDI score of 77/100 and an HDI score of 88/100. These disproportionate scores were probably the first indication that the patient might have underlying anxi-ety and fear-avoidance beliefs associated with her chronic pain syndrome.

During the initial treatment period, the patient’s coping mechanism could be described as passive. Grossi et al18 define passive coping as involving withdrawal or giving up and relinquishing control of the pain to something or someone else. The examiner tried to have the patient take an active coping approach to her condi-tion, which involves conscious attempts to relieve or control pain, or to function in spite of the pain.

In this case, there was an unforeseen psychosocial consequence of informing the patient of the results of the examina-tion and stress radiographs which indi-cated that she had CCJ hypermobility. When she failed to achieve good results after the first round of treatment, she became alarmed and anxious. The well intentioned idea of educating her in how to be careful with her neck positions and movements to self-manage her condition was not successful. Instead of feeling re-lieved and self-empowered, she might have catastrophized her condition when progress was less than expected. This was further exacerbated by discussions with her social support system, who felt that she must have a significant pathol-ogy and insisted on getting a surgical consultation.

When the neurosurgeon downplayed the significance of her symptoms and told her that her symptoms were due to “stress,” she might have realized that

passive coping alone was insufficient. She was able to comprehend the seri-ous nature of any surgical stabilization procedure and began to comply with the previously stated recommendations. She eventually became more careful with head and neck positions during her nor-mal activities. She began to understand that this was a chronic problem that she could manage herself with appropriate modifications in her lifestyle and pos-ture. The importance of this psychosocial aspect (ie, coping style) of her case man-agement cannot be underestimated, and it may help to explain a large part of the positive outcomes.

This case demonstrates the impor-tance of screening patients with chronic pain syndromes for underlying anxiety, fear-avoidance behaviors, and posttrau-matic stress disorders. It is important to recognize these psychosocial issues early and to use this information in the development of appropriate treatment and management strategies.13,51 For an excellent review of the subject of post-traumatic stress disorders, please refer to Defrin et al.8 It is possible that emotional stress was a significant component of this patient’s symptoms of headache and diz-ziness, and that relief of these symptoms was somehow related to the reduction in her anxiety levels during the course of her treatment. The manner in which a pa-tient is informed about the diagnosis and prognosis may have a profound influence on the patient’s subsequent response to treatment. The value of these psychoso-cial components to clinical management cannot be underestimated.

CONCLUSION

This report reviews the clinical decision-making process that led to a diagnosis of CCJ hypermobil-

ity in a patient with chronic neck pain, occipital headache, and dizziness. It also highlights the need for more research into a number of issues surrounding the prevalence, diagnosis, and treatment of CCJ hypermobility. t

ACKNOWLEDGEMENTS: We would like to ac-knowledge the late Richard Erhard, DC, PT for his role as a mentor, friend, and colleague. He often said that “challenges stimulate solu-tions” and was the person who first brought to our attention the need for clinical assessment of hypermobility in the craniocervical junc-tion in patients with chronic neck pain. We also acknowledge his wife Natalie Erhard, who was very supportive of Dr Erhard’s time with us during the twilight year of his life. Lastly, we would like to thank Kevin P. Mathers, RT(R), CT for his technical support and Edward Gates, MD for his radiological interpretation.

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