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Show Clival Epidural Hematoma in Traumatic Sixth Cranial Nerve Palsies Combined with Cervical Injuries Hugh J. Garton, MD, Stephen S. Gebarski, MD, Omar Ahmad, MD, Jonathan D. Trobe, MD Abstract: Eight patients sustained a combination of clival epidural hematoma, traumatic sixth cranial nerve palsy (6 NP), and occipitocervical injury. This combination of features has been sparsely described. Whether the hematoma, which represents tectorial membrane injury, is merely a marker for 6 NP and occipitocervical injury or is causative is unresolved, but this imaging finding should alert examiners who note traumatic 6 NP to the need for detailed cervical imaging, as surgical stabiliza-tion of this region may be critical to prevent future spinal cord dysfunction. Journal of Neuro-Ophthalmology 2010;30:18-25 doi: 10.1097/WNO.0b013e3181ce14ae 2010 by North American Neuro-Ophthalmology Society Sixth cranial nerve palsy (6 NP) is a common finding in closed head injury, but the mechanism of the palsy in this setting is unresolved (1-4). In a large post-mortem study of 10 cases of 6 NP in severe blunt head trauma, histopathologic analysis showed intraneural edema and perineural hemorrhage within the petroclival segment of the sixth cranial nerve (5). It has been proposed that the nerve is contused as the brain accelerates and decelerates while the petroclival portion of the nerve remains fixed (6,7). Among the 10 cases examined in the post-mortem study of traumatic 6 NP (5), 3 also had cervical spine fracture. The combination of traumatic 6 NP and cervical spine fracture has also been described elsewhere (8-12). However, the combination of occipitocervical spine injury and clival epidural hematoma (CEH) has been reported in only 11 cases (9,10,13-21). Among them, 4 cases also had traumatic 6 NP (9,10,20,21). We describe 8 additional cases of the combination of CEH, 6 NP, and occipitocervical spine injury, drawing attention to the need for careful cervical spine imaging when CEH is identified. We discuss several hypotheses to explain this constellation of findings. A list of 18 patients with a combination of 6 NP after head trauma and cervical spinal injury was produced through the clinical experience of the Inpatient Ophthal-mology Consultation Service and the outpatient Neuro-ophthalmology Service at the University of Michigan Health Center between 1986 and 2008. From among them, a neuroradiologist (S.S.G.) identified 8 cases with CEH, which form the basis of this report. CASE REPORTS Case 1 A 38-year-old woman was a restrained driver whose auto-mobile was struck in the rear by a van traveling at 60 mph. The airbag deployed. There was no loss of consciousness. The Glasgow Coma Scale (GCS) score was 15 on the day of transfer from an outside hospital to our emergency room. Ophthalmologic examination 6 days after admission disclosed 60% abduction of the right eye, 25% abduction of the left eye, marked esotropia, and an otherwise normal examination. There were no other neurologic abnormalities. Brain and cervical spine CT performed on the day of admission showed a displaced anterior occipital fracture and CEH (Fig. 1). There was separation of the occiput-C1 articulation on the left with condyle fracture on the left. At surgery, occipital-C1 instability was noted, as was hemorrhage within the posterior cervical ligaments. An instrumented occiput-to-C2 fusion was performed with a rod-and-wire construct. At the final neurosurgical follow-up visit 7 months after admission, the patient had complete resolution of the 6 NPs. Cervical spine radiographs showed good placement of instrumentation and no evidence of abnormal movement at the occipitocervical junction. Departments of Neurosurgery (HJG, JDT), Radiology (Neuroradi-ology) (SSG, OA), Ophthalmology (JDT), and Neurology (JDT), University of Michigan Medical Center, Ann Arbor, Michigan. Address correspondence to Jonathan D. Trobe, MD, Kellogg Eye Center, 1000 Wall Street, Ann Arbor, MI 48105; E-mail: jdtrobe@ umich.edu 18 Garton et al: J Neuro-Ophthalmol 2010; 30: 18-25 Original Contribution Case 2 A 44-year-old woman involved in a high-speed motor vehicle accident as an unrestrained passenger was found unconscious at the scene with a subsequent admission GCS score of 8. Ophthalmologic examination 1 day after admission disclosed a complete loss of abduction of the right eye with a large primary position esotropia. Results of the rest of the ophthalmologic examination were normal. She had a mild right hemiparesis. CT showed occipital condyle-C1 distraction and sub-luxation, rotary subluxation of C1-C2, a C5-C6 fracture subluxation, and a CEH (Fig. 2). Results of CT angio-graphy were negative for a vascular injury. She underwent occiput-to-C2 instrumented fusion with rod-and-wire instrumentation and lateral mass plating at C5-C6 without complications. Eight months after dis-charge, she underwent transposition of the right superior and inferior rectus muscles for nonimproving complete 6 NP with a large primary position esotropia. After the initial surgical correction, the patient had a small esotropia with double vision. A second extraocular muscle procedure later aligned her eyes in primary position. Case 3 A 4-year-old girl was a backseat restrained passenger in a head-on automobile accident. She did not lose conscious-ness and had a GCS scale of 15 at the scene. Ophthalmologic examination 2 days after admission disclosed 10% abduction bilaterally with marked esotropia. Results of the rest of the ophthalmologic examination were normal. She also had a mild right hemiparesis. CT showed an anteriorly displaced distracted dens frac-ture (Fig. 3A). MRI showed not only the fracture subluxa-tion at C1-C2 but also a subtle avulsion of the tectorial membrane at the posterior aspect of the clivus with a small CEH (Fig. 3B). After initial management in a halo brace, the patient's cervical alignment could not be maintained, with progressive distraction of C1 from C2. She underwent an instrumented fusion of C1 and C2. At surgery a transverse tear in the dura was noted just above the lamina of C2. Mechanical testing with intraoperative flexion and extension films demonstrated functional stability of the occipitocervical junction. Within 7 months of hospital discharge, ophthalmologic examination disclosed spontaneous resolution of the 6 NPs. Cervical spine radiographs 1 year after trauma showed a firm spinal fusion between C1 and C2 with good alignment. Case 4 A 13-year-old boy was a restrained back seat passenger in an automobile struck from behind by a snowplow. At the FIG. 1. Case 1. Precontrast cervical spine CT. A. Axial bone algorithm through the basiocciput shows a displaced comminuted right occipital condyle fracture (arrow). B. Axial soft tissue algorithm CT section through the basiocciput shows the displaced comminuted right occipital condyle fracture (white arrow), but a beam-hardening artifact partially obscures the occipital epidural hematoma (black arrow). C. Sagittal reformatted image centered on the basiocciput displayed with soft tissue windowing shows the epidural hemorrhage more conspicuously (black arrow). FIG. 2. Case 2. Precontrast head CT after spinal stabilization shows a large occipital epidural hematoma (black arrow) despite the scatter artifact from the metallic spinal stabilization hardware. Original Contribution Garton et al: J Neuro-Ophthalmol 2010; 30: 18-25 19 scene, he was conscious but intubated for agonal breathing. No GCS score was documented. Ophthalmologic examination 3 weeks after admission disclosed complete loss of abduction bilaterally with a large esotropia and alternating fixation. Results of the rest of the ophthalmologic examination were normal. The patient was quadriplegic and ventilator-dependent with some preserva-tion of sensation. MRI showed atlanto-occipital disarticulation with frank detachment of the tectorial membrane from the posterior aspect of the clivus with a large CEH. The tectorial membrane was completely peeled away from the clivus (Fig. 4). He underwent stabilization of the atlanto-occipital disarticulation via occiput-to-C3 instrumented posterior fusion. Esotropia was present at the time of discharge from the hospital 3 months after admission, but no further ophthalmologic follow-up information was available. CT at time of discharge 3 months after trauma revealed a firm occipitocervical spinal fusion. Case 5 A 4-year-old girl was playing in the driveway in front of her house when the family car was accidentally backed out over her. Tire marks were present on her chest. Upon admission, she had a GCS score of 15. Ophthalmologic and neurologic examinations 2 days after admission disclosed bilateral, nearly complete, abduc-tion deficits as the only clinical impairment. Imaging showed severe atlanto-occipital dislocation with ligamen-tous injuries and a CEH. She underwent occiput-to-C2 fusion and an occipital periosteal flap with autologous iliac harvest (22). The FIG. 3. Case 3. Precontrast cervical spine CT and MRI. A. Sagittal reformatted CT image centered on the basiocciput displayed with bone windowing shows a displaced and distracted dens fracture (arrow). B. Sagittal short tau inversion recovery MRI centered on the basiocciput shows the displaced and distracted dens fracture (white arrow) and a subtle occipital epidural hemorrhage just underneath the tectorial membrane (black arrow). The tectorial membrane has been partially torn away from the clivus. There are large regions of periligamentous hemorrhagic swelling (H). FIG. 4. Case 4. Precontrast head and cervical spine MRI. A. Precontrast T1 sagittal image shows a large occipital epidural hematoma under the tectorial membrane (black arrow). The tectorial membrane has been torn completely away from the clivus, allowing the large hematoma to dissect up to the level of the dorsum sellae. B. Sagittal short tau inversion recovery magnetic resonance image centered on the basiocciput shows that the tectorial membrane (black arrow) has been torn away from the clivus with a resultant large occipital epidural hematoma (H), spinal cord contusion (white arrow), and periligamentous hemorrhagic swelling (h). Original Contribution 20 Garton et al: J Neuro-Ophthalmol 2010; 30: 18-25 abduction deficits were improving at time of discharge and had fully resolved 13 years later. Case 6 A 20-year-old man was an unrestrained driver in a rollover accident. He had brief loss of consciousness after the incident. During evacuation from the car, he had a respira-tory arrest and hypotension. Upon arrival to our emergency room, he was intubated but conscious. The GCS score was not documented. Ophthalmologic examination 2 months after trauma disclosed bilateral incomplete abduction deficits, right greater than left. He had a 9-prism-diopter esotropia in primary position, increasing to 16 prism-diopters in right gaze. He had incomplete quadriplegia with a Brown- Sequard type pattern of asymmetric myelopathic weakness and sensory findings together with swallowing impairment. CT and MRI showed atlanto-occipital dislocation with ligamentous injuries and CEH. The patient underwent an occiput-to-C3 fusion. Ophthalmologic examination 5 months after the trauma revealed improvement in the 6 NPs with alignment measurements of 2 prism-diopters of esotropia in primary gaze increasing to 6 prism-diopters in right gaze. Five years after injury he had fully recovered. Case 7 A 67-year-old woman was a restrained driver in a head-on motor vehicle accident. The GCS score was not documented. Ophthalmologic examination 5 days after admission disclosed bilateral 6 NPs and a right third cranial nerve palsy. She had a central cord pattern of injury with relative preservation of lower extremity movement but bilateral arm weakness. CT and MRI showed subluxation of C1-C2 with ligamentous injuries, including rupture of the transverse ligament, and a CEH. She underwent fusion of C1 to C2 with C1-C2 transarticular screw fixation with a Brooks-type fusion. Case 8 An 8-year-old girl was a front seat restrained passenger in a head-on motor vehicle accident at an impact speed of 28 mph (23). Bedside ophthalmologic examination disclosed visual acuities of 20/20 at near and 80% abduction of the right eye. MRI showed a CEH elevating the tectorial membrane but without associated evidence of fracture or dislocation on plain X-rays. She was managed in a cervical collar without oper-ative intervention. At 1 month follow-up, the 6 NP had improved to normal alignment in primary gaze, but esotropia of 4 prism-diopters was present in right gaze. Her brothers, ages 3 and 6, also sustained CEHs in the accident, and each required occiput-to-C2 fusion. Neither had 6 NPs. DISCUSSION Our series of 8 patients represents the largest reported collection of the combination of CEH, 6 NP, and occipitocervical injury (Table 1). In all but 1 case (Case 8), there was imaging evidence of direct injury to the tectorial membrane (Cases 3, 4, 6, and 8) or disruption of the occipital condylar-C1 joint (Cases 1, 2, 5, and 7). MRI showed that the CEH separated the clivus from the tectorial membrane, a connective tissue band interwoven with the posterior longitudinal ligament and dura that extends from the petroclival junction to the C1-C2 cervical segment (24). This membrane is tightly bound to the underlying clivus and cervical bones by connective tissue insertions with rich vascular and neural structures (24). Avulsion of these high tensile strength connective tissues results in a CEH. Because the stability of the occipitocervical junction depends on preservation of the tectorial membrane and the apical ligaments (25), their injury leads to gross instability between head and neck and loss of protection of the underlying neural structures. The concurrence of CEH, 6 NP, and occipitocervical injury has been previously described in only 4 case reports (9,10,20,21) (Table 2). In 3 of 4 of these reports, patients had bilateral 6 NP. Similarly, 6 of our 8 patients had bilateral 6 NPs. The association of CEH with 6 NP and occipitocervical injury emphasizes the importance of identifying a CEH in patients presenting with traumatic 6 NP. If it is present, there is a need to obtain careful imaging evaluation of the cervical spine, particularly the occipitocervical region, even when cervical spine injury may not be clinically suspected, as in 5 of our 8 cases. Although imaging of the cervical spine is a routine part of trauma evaluation, occipitocervical injuries, particularly those involving the tectorial mem-brane, are often poorly seen on plain cervical spine films and may even be difficult to discern on CT without a reasonable index of suspicion. MRI studies provide the best opportunity to visualize the ligamentous structures of the occipitocervical region. Given the rarity of traumatic 6 NP and occipitocervical spinal injury, their combination is probably not a chance occurrence. Although the sixth cranial nerve is often said to be vulnerable to head trauma because of its intrinsic mechanical properties or its relatively long exposure in the intracranial space, direct cadaver assess-ments of force required to break this nerve show that it is relatively resistant and tougher, for example, than the fourth cranial nerve (26). The intracisternal course of the fourth cranial nerve is 3 times that of the sixth cranial nerve (27), yet the fourth cranial nerve is less often Original Contribution Garton et al: J Neuro-Ophthalmol 2010; 30: 18-25 21 clinically damaged than the sixth cranial nerve (27,28). Thus, the sixth cranial nerve's anatomic orientation and interactions with surrounding structures must predispose it to injury. The nerve exits the brainstem at the pontomedullary sulcus and travels for 15 mm in the basal cisterns before passing through a dural ring on the superior clival surface. It is surrounded within the dural canal by venous lakes in continuity with the cavernous sinus, basilar plexus, and superior and inferior petrosal sinuses. Ascending for several millimeters beneath the clival dura to enter the Dorello canal, it is bounded superiorly by the petrosphenoidal TABLE 1. Our cases of clival epidural hematoma, sixth cranial nerve palsy, and occipitocervical injury Case Age (years)/ Sex Mechanism Side of Sixth Cranial Nerve Palsy Occipitocervical Imaging Findings Brain Injury Spinal Cord Injury 1 38/F Rear impact Bilateral Left occipital condylar fracture O-C1 separation left > right Posterior cervical hemorrhage noted at surgery GCS score 15 None 2 44/F Unknown Right O-C1 distraction C1-C2 rotatory subluxation C5-C6 fracture Retrolisthesis of C5 on C6, with rupture of the anterior longitudinal ligament and disk space injury GCS score 8 None (right hemiparesis explained by left internal capsule injury) 3 4/F Head on Bilateral Type II dens fracture Anterior and posterior longitudinal ligament rupture Partial tectorial membrane tear on imaging but occipitocervical junction to be stable to manipulation at surgery GCS score 15 None 4 13/M Rear impact Bilateral Anterior displacement occiput on C1O-C1 separation Frank tectorial membrane avulsion no other cervical spine injury Agonal at scene, MRI shows injury to medulla Complete injury at C1 5 4/F Crush injury Bilateral Anterior displacement of occiput on C1 GCS score 15 None 6 20/M Rollover Bilateral Atlanto-occipital dissociation, tectorial membrane disruption GCS score not documented, patient conscious on arrival Brown-Sequard syndrome 7 67/F Head on Bilateral Transverse ligament rupture Not documented High cervical central cord syndrome 8 8/F Head on Right Tectorial membrane injury GCS score 15 None GCS, Glasgow Coma Scale; O, occipital condyle. TABLE 2. Previously reported cases of clival epidural hematoma, sixth cranial nerve palsy, and occipitocervical injury Author, Reference Age (years) Mechanism Side of Sixth Cranial Nerve Palsy Occipitocervical Imaging Findings Mizushima et al (9) 8 Hyperflexion Bilateral Odontoid fracture, type I managed in a collar Ratilal et al (10) 26 Hyperextension Bilateral Right C6 transverse process fracture, no atlanto-occipital instability by flexion and extension Fuentes et al (20) 47 Not available Left Bilateral occipital condyle fractures Papadopoulos et al (21) 10 Pedestrian versus truck Bilateral Atlanto-occipital dissociation Original Contribution 22 Garton et al: J Neuro-Ophthalmol 2010; 30: 18-25 (Gruber) ligament, inferiorly by the clivus, medially by the dorsum sellae, and laterally by the petrous bone (29). The nerve then passes anteriorly through the cavernous sinus to the superior orbital fissure and into the orbit (Fig. 5). In a 1971 report of 2 patients who had sustained 6 NP without a basilar skull fracture but with cervical spine injury, Schneider and Johnson (6) attributed the spine injury to hyperextension causing a type II dens fracture with posterior dislocation of C1 on C2 in 1 patient, and a C2 (‘‘hangman's'') fracture in the other. In that report (6), they referred to their animal cervical spine trauma model (30,31), in which they had replaced a portion of the calvaria with transparent Lexan plastic and induced cervical hyperextension. They observed that the cerebrum and brainstem moved upward and backward with respect to the skull as the hyperextension movement came to an abrupt end. They proposed that the sixth cranial nerve moves upward against the Gruber ligament at the superior aspect of the Dorello canal, encountering a sheer force perpen-dicular to the long axis of the nerve (6) (Fig. 6). In 1976, Takagi et al (7) reported a single case of traumatic 6 NP and argued that upward movement of the brain after hyperextension produced an injury at the petrous apex rather than at the Gruber ligament. They believed that the dural porus acted like a pulley, translating the upward movement of the cisternal portion of the nerve to a longitudinal stretch and forcing the nerve down into the petrous apex. This action would result in a sheering injury, the damage again occurring with a force perpen-dicular to the long axis of the nerve (Fig. 7). Arias (8) pointed out that injury would occur at the dural ring and petrous apex when the nerve was placed under tension. Describing a patient with bilateral 6 NP and an associated C5-C6 flexion distraction injury in 1996, Uzan et al (11) proposed a similar mechanism in flexion head injuries. Reporting on a patient with bilateral 6 NP and atlanto-occipital dislocation, Fruin and Pirotte (32) suggested that distraction (stretching) across the cervicomedullary junction was responsible for the lower cranial nerve palsies seen in this setting (Fig. 8). In a case very similar to those presented here, Calisaneller et al (33) proposed an entirely different mechanism, namely direct distortion of the sixth cranial nerve along its subarachnoid course or at the Dorello canal by the clival hematoma (Fig. 9). Whatever the mechanism of injury, the pathologic lesion in these cases appears to be restricted to a short segment of the sixth cranial nerve. In an autopsy study of the sixth cranial nerve in 10 patients who had suffered head injury, Sam et al (5) found hemorrhagic contusions at the dural ring, petrous apex, and point of apposition of the sixth cranial nerve to the vertical segment of the internal carotid artery (ICA), where sympathetic fibers join the sixth cranial nerve briefly en route to the first division of the fifth cranial (trigeminal) nerve (29). They noted that these 3 sites of nerve injury were associated with points of angulation or tethering along the course of the nerve. Evidently, such injury can result from either flexion or extension of the head. Our Cases 1, 2, 4, 5, and 6 had varying degrees of occiput-C1 separation. These injuries FIG. 5. Normal extra-axial path of the sixth cranial nerve in relation to the tectorial membrane, clivus, and petrous apex. C1, atlas; C2, axis; DP, dural porus; GL, Gruber ligament; ICA, internal carotid artery; PA, petrous apex; VI N, sixth cranial nerve. FIG. 6. The hypothesis of Schneider and Johnson (6). The sixth cranial nerve suffers shear stress against the Gruber ligament as the brainstem and cisternal segment of the nerve move upward and posteriorly during hyperextension injury. DP, dural porus; GL, Gruber ligament; ICA, internal carotid artery; PA, petrous apex; VI N, sixth cranial nerve. Original Contribution Garton et al: J Neuro-Ophthalmol 2010; 30: 18-25 23 have mostly been considered as occurring during severe cervical hyperextension and distraction, often with a frontal facial trauma (34-37). Cases 3 and 7 presented with fracture and ligamentous injuries at C2 also consistent with a degree of distraction in conjunction with extension and/or flexion (38,39). Case 8 is unique in having sustained a pure flexion-distraction injury. She and her 2 younger siblings were all improperly restrained in a head-on motor vehicle accident. All 3 children sustained CEHs and the 2 younger siblings had varying degrees of frank occipitocervical dissociation. By modeling this accident based on data retrieved from the vehicle's ‘‘black box'' and substituting industry standard anthropomorphic crash dummies, Sochor et al (23) noted that in Case 8 the maximum neck strain occurred in flexion-distraction, with no secondary contact of her head to the vehicle interior. In her case, an improperly applied shoulder harness restrained only the lower torso. The primary mechanism of force application in this accident was in the sagittal plane, with the body and lower neck mechanically coupled to a rapidly decelerating vehicle, whereas the head initially continued in forward progress at the initial vehicle speed. The unifying feature of our cases is distraction across the craniocervical junction with the tectorial membrane damaged by a straining force. Whether through upward or downward movement of the brainstem in neck flexion or extension, the sixth cranial nerve is probably placed under tension at points where the nerve is tethered (straining force) or angled (sheer stress). We consider it unlikely that the CEH could, by pure compression, have produced injury FIG. 8. The hypothesis of Fruin and Pirotte (32). The sixth cranial nerve experiences strain during occipitocervical dissociation. DP, dural porus; GL, Gruber ligament; ICA, internal carotid artery; PA, petrous apex; VI N, sixth cranial nerve. FIG. 9. The hypothesis of Calisaneller et al (33). Hematoma within and beneath the tectorial membrane directly distorts the sixth cranial nerve. DP, dural porus; GL, Gruber ligament; ICA, internal carotid artery; PA, petrous apex; VI N, sixth cranial nerve. FIG. 7. The hypothesis of Takagi et al (7). 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