Bilateral Abducens Nerve Palsies After Middle Meningeal Artery Embolization for Chronic Subdural Hematoma

Clinical Correspondence Section Editors: Robert Avery, DO Karl C. Golnik, MD Caroline Froment, MD, PhD An-Guor Wang, MD Bilateral Abducens Nerve Palsies After Middle Meningeal Artery Embolization for Chronic Subdural Hematoma Subahari Raviskanthan, MBBS, Peter William Mortensen, MD, Yi Jonathan Zhang, MD, Andrew Go Lee, MD S ubdural hematoma (SDH) is a relatively common and potentially deadly condition. The historical management of SDH is surgical with burr hole drainage or craniotomy with evacuation. Recently, middle meningeal artery embolization (MMAE) has been proposed as a treatment for SDH. MMAE aims to decrease the vascular supply to abnormal membranes produced in response to the inflammatory response within the dural space and may be the underlying cause of SDH. Randomized controlled trials on MMAE are ongoing. We report a case of bilateral abducens nerve palsies after bilateral MMAE. To the best of our knowledge, this is the first such reported case in the English language ophthalmic literature. CASE A 37-year-old man presented to the emergency department with increasing falls, headaches, and generalized weakness. He had a previous motorbike accident with residual left homonymous hemianopsia and limb weakness. His medical history was significant for Type 1 diabetes mellitus and asthma. His medications included insulin, albuterol, lisinopril, trazodone, pantoprazole, and budesonide-eformoterol. He had no significant family history. He did not smoke and had alcohol consumption equivalent to 40 standard drinks weekly. On initial neurological examination, his pupils were isocoric and reactive, with no motility defects. He had a left homonymous hemianopsia, left pronator drift, and 4+/5 power in his left upper extremity and proximal left lower extremity. Left ankle plantar and dorsiflexion were 3/5. Department of Ophthalmology (SR, PWM), Blanton Eye Institute, Houston Methodist Hospital, Houston, Texas; Department of Neurosurgery (YJZ, AGL), Houston Methodist Hospital and Weill Cornell Medicine, New York, New York; Department of Ophthalmology (AGL), University of Texas Medical Branch, Galveston, Texas; University of Texas MD Anderson Cancer Center (AGL), Houston, Texas of Ophthalmology; Texas A and M College of Medicine (AGL), Bryan, Texas; and Department of Ophthalmology (AGL), The University of Iowa Hospitals and Clinics, Iowa City, Iowa. The authors report no conflicts of interest. Address correspondence to Andrew G. Lee, MD, Department of Ophthalmology, Blanton Eye Institute, Houston Methodist Hospital, 6560 Fannin St. Ste 450, Houston, TX 77030; E-mail: aglee@ houstonmethodist.org Raviskanthan et al: J Neuro-Ophthalmol 2022; 42: e505-e507 These findings were all consistent with his previous traumatic brain injury. His initial laboratory studies revealed elevated blood glucose (240 mg/dL [normal range 65–99 mg/dL]) and ketones (beta hydroxybutyrate level 4.46 mmol/L [normal 0.02–0.27 mmol/L]) consistent with diabetic ketoacidosis. Computed tomography (CT) of the brain was significant for SDH overlying the left cerebral convexity with extension to the falx cerebri and bilateral tentorium (Fig. 1A). A chronic right posterior cerebral artery/middle cerebral artery border zone territory infarct and right subdural hygroma were noted. MRI of the brain revealed bilateral frontal/ temporal/parietal SDHs approximately 1 cm at their largest in the left posterior temporal convexity and right frontal convexity. There was minimal midline shift to the right of 2–3 mm. Chronic ischemic changes from the previous stroke were noted in the right posterior cerebral artery/ middle cerebral artery border zone. He was admitted and subsequently underwent bilateral MMAE with 300–500-mm Embosphere particles (Fig. 1B). The anatomy of both intracranial and extracranial circulations was identified before the embolization, and no abnormal anastomoses were identified. Preoperatively, there was no sixth nerve palsy, and he did not report diplopia. Postoperatively, however, he complained of new binocular FIG. 1. A. Computed tomography (CT) of the brain demonstrating bilateral subdural hematoma (arrows) with a small amount of midline shift to the right. B. Cerebral angiogram depicting dye injection through the right external carotid artery after Embosphere embolization, showing complete occlusion of the middle meningeal artery (arrow) and lack of flow to the dura. e505 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Correspondence FIG. 2. Horizontal gaze images of patient postoperatively (A–C) and at follow-up review (D–F). A. Right gaze, with .50 PD ET noted. B. Primary gaze showing 30 PD ET noted. C. Left gaze with 10 PD ET noted. D. Right gaze, with significant improvement noted. E. Primary gaze with improvement noted. F. Left gaze, with significant improvement noted. horizontal diplopia, and the neuro-ophthalmology service at Houston Methodist Hospital was consulted. Neuro-ophthalmic examination showed a bilateral abduction deficit with a 30-prism diopter (PD) esotropia (ET) in primary gaze, increasing to .50 PD ET in the right gaze and 10 PD ET in the left gaze, consistent with bilateral abducens nerve palsies (Fig. 2A–C). The remainder of the eye examination was normal except for the previously documented left homonymous hemianopsia. He had no other cranial nerve deficits. There was no papilledema. Repeat brain CT and subsequent MRI revealed stable SDH with new punctate foci of diffusion restriction bilaterally—most notably in the right parietal lobe, right basal ganglia, right temporal lobe, right caudate head, left insula, genu of the corpus callosum, right cerebellum, and scattered throughout the bilateral periventricular white matter around the corona radiata and centrum semiovale. There were no brainstem infarctions, and there was no midline shift. These infarcts did not account for his bilateral abducens nerve palsy. The timing of the abducens palsies being present immediately after bilateral MMAE is suspicious for a procedure-related complication, although other etiologies should also be considered. The patient had multiple cardiovascular risk factors, including long-term poorly controlled diabetes, excessive alcohol intake, and previous stroke, so abducens nerve microangiopathy remains possible. There were no features of intracranial hypertension on MRI or dilated fundus examination. There was also no suggestion of intracranial hypotension on MRI, making these etiologies less likely. No brainstem pathology or lesions along the course of the abducens nerve bilaterally were noted. There were no other clinical features to suggest malnutrition or an acute Wernicke encephalopathy, and his symptoms resolved without treatment for Wernicke encephalopathy. Neuro-ophthalmic review 2 months after his procedure showed significant improvement in his bilateral abducens nerve palsies, with improved ET in primary gaze from 30 PD to 20 PD (Fig. 2D–F). DISCUSSION MMAE was first reported in 1994 as a potential treatment for SDH, with some studies suggesting it has lower rates of SDH recurrence compared with conventional surgical drainage options (1). Increasing research into the pathophysiology of SDH suggests that trauma may trigger the proliferation of dural border cells, initiation of an inflammatory cascade, and formation of multiple abnormal membranes, which then bleed and cause recurrent SDH (2). MMAE is believed to decrease vascular supply and induce ischemia to the abnormal membranes, thus causing regression of the SDH (2). The vascular supply to the abducens nerve is rich, with multiple external carotid artery branches, including the middle meningeal artery, accessory meningeal artery, and TABLE 1. Details of 4 patients reported in the literature with abducens palsy in the setting of endovascular procedures Journal Details Long et al. (5) Cavernous dural arteriovenous fistula Kurata et al. (3) 3 patients undergoing lidocaine testing before endovascular surgery e506 Artery Embolized Bilateral meningohypophseal trunks, right middle meningeal artery, and internal maxillary artery Middle meningeal artery Complication Symptom Course Abducens nerve palsy Recovered within 2 weeks Transient abducens nerve palsy related to lidocaine testing Resolved within 5 minutes Raviskanthan et al: J Neuro-Ophthalmol 2022; 42: e505-e507 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Correspondence ascending pharyngeal artery, as well as the inferolateral trunk and meningohypophyseal trunk of the internal carotid artery (3,4). Typically, cranial neuropathies occurring after embolization procedures result from occlusion of the vasa nervorum—the small size of these vessels typically means that this complication is more common with smaller particles/liquid embolization. When occlusion of the vasa nervorum is considered a risk, larger particles, such as the 300–500-mm particles used for our patient, are often used, and some particle types, including the Embosphere particles our patient had, are believed to theoretically increase distal penetration and therefore decrease risk, making this patient’s bilateral abducens palsies unexpected (4). A search of published English language literature was performed using PubMed, Ovid MEDLINE, EMBASE, and the Cochrane Database of Systematic Reviews from dates of commencement until December 2020. Medical Subject Headings “Subdural hematoma,” “Chronic subdural hematoma,” “Therapeutic embolization,” “Artificial embolization” and keywords “middle meningeal artery embolization” were combined to identify all published complications of MMAE in patients with SDH. Two cases of transient diplopia in a series of 89 patients were reported, but it is unclear if these were abducens nerve palsies (1). Although there have not been any reports of embolization of MMAE for chronic SDH causing cranial neuropathy, Kurata found that 3 of 67 patients who had provocative lidocaine testing into the middle meningeal artery for other endovascular procedures developed transient abducens nerve palsy, with further 3 developing facial nerve palsies and 1 patient with an oculomotor nerve palsy (3). All the patients who subsequently underwent endovascular surgery suffered cranial nerve palsies as predicted by the initial provocative testing (3). Table 1 demonstrates the other cases of abducens nerve palsy after MMA procedures. There are many potential mechanisms for abducens nerve palsy in the setting of SDH, including traumatic, ischemic, and nonlocalizing, increased or decreased intra- Raviskanthan et al: J Neuro-Ophthalmol 2022; 42: e505-e507 cranial pressure. There was no imaging evidence for direct mass effect, tractional irritation on the abducens nerves, or typical imaging features of altered intracranial pressure or large vessel or brainstem stroke. No systemic hypotension occurred. The possible role of indirect ischemia after embolization of the middle meningeal artery cannot be completely excluded. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: S. Raviskanthan, P. W. Mortensen, Y. J. Zhang, and A. G. Lee; b. Acquisition of data: S. Raviskanthan, P. W. Mortensen, Y. J. Zhang, and A. G. Lee; c. Analysis and interpretation of data: S. Raviskanthan, P. W. Mortensen, Y. J. Zhang, and A. G. Lee. Category 2: a. Drafting the manuscript: S. Raviskanthan, P. W. Mortensen, Y. J. Zhang, and A. G. Lee; b. Revising it for intellectual content: S. Raviskanthan, P. W. Mortensen, Y. J. Zhang, and A. G. Lee. Category 3: a. Final approval of the completed manuscript: S. Raviskanthan, P. W. Mortensen, Y. J. Zhang, and A. G. Lee. 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