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Isolated Third, Fourth, and Sixth Cranial Nerve Palsies from Presumed Microvascular Versus Other Causes a Prospective Study

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Isolated Third, Fourth, and Sixth Cranial Nerve Palsies from Presumed Microvascular Versus Other Causes a Prospective Study Isolated Third, Fourth, and Sixth Cranial Nerve Palsies from Presumed Microvascular versus Other Causes A Prospective Study Madhura A. Tamhankar, MD,1 Valerie Biousse, MD,2 Gui-Shuang Ying, MD, PhD,1 Sashank Prasad, MD, PhD,3 Prem S. Subramanian, MD, PhD,4 Michael S. Lee, MD,5 Eric Eggenberger, DO,6 Heather E. Moss, MD, PhD,7 Stacy Pineles, MD,8 Jeffrey Bennett, MD, PhD,9 Benjamin Osborne, MD,10 Nicholas J. Volpe, MD,11 Grant T. Liu, MD,1 Beau B. Bruce, MD, MS,2 Nancy J. Newman, MD,2 Steven L. Galetta, MD,1 Laura J. Balcer, MD, MSCE1 Purpose: To estimate the proportion of patients presenting with isolated third, fourth, or sixth cranial nerve palsy of presumed microvascular origin versus other causes. Design: Prospective, multicenter, observational case series. Participants: A total of 109 patients aged 50 years or older with acute isolated ocular motor nerve palsy. Testing: Magnetic resonance imaging (MRI) of the brain. Main Outcome Measures: Causes of acute isolated ocular motor nerve palsy (presumed microvascular or other) as determined with early MRI and clinical assessment. Results: Among 109 patients enrolled in the study, 22 had cranial nerve III palsy, 25 had cranial nerve IV palsy, and 62 had cranial nerve VI palsy. A cause other than presumed microvascular ischemia was identified in 18 patients (16.5%; 95% confidence interval, 10.7e24.6). The presence of 1 or more vasculopathic risk factors (diabetes, hypertension, hypercholesterolemia, coronary artery disease, myocardial infarction, stroke, and smoking) was significantly associated with a presumed microvascular cause (P ¼ 0.003, Fisher exact test). Vasculopathic risk factors were also present in 61% of patients (11/18) with other causes. In the group of patients who had vasculopathic risk factors only, with no other significant medical condition, 10% of patients (8/80) were found to have other causes, including midbrain infarction, neoplasms, inflammation, pituitary apoplexy, and giant cell arteritis (GCA). By excluding patients with third cranial nerve palsies and those with GCA, the incidence of other causes for isolated fourth and sixth cranial nerve palsies was 4.7% (3/64). Conclusions: In our series of patients with acute isolated ocular motor nerve palsies, a substantial proportion of patients had other causes, including neoplasm, GCA, and brain stem infarction. Brain MRI and laboratory workup have a role in the initial evaluation of older patients with isolated acute ocular motor nerve palsies regardless of whether vascular risk factors are present. Financial Disclosure(s): The author(s) have no proprietary or commercial interest in any materials discussed in this article. Ophthalmology 2013;120:2264-2269 ª 2013 by the American Academy of Ophthalmology. Isolated third, fourth, and sixth cranial nerve palsies in adults whereas other studies have advocated observation without frequently occur from presumed microvascular ischemia to the neuroimaging unless spontaneous resolution has not occurred nerve in the setting of atherosclerotic risk factors, such as older by 3 to 6 months.29,31e35 We thus conducted a multicenter age, diabetes mellitus, hypertension, and hyperlipidemia.1e3 prospective study to assess whether early neuroimaging is Since the development of magnetic resonance imaging warranted in the evaluation of acute isolated ocular motor (MRI), less benign and potentially treatable causes for acute nerve palsy. ocular motor mononeuropathies have been documented, including intracranial neoplasm, aneurysm, inflammation, 3e30 infection, and brain stem infarction. In prior prospective Methods studies, the percentage of patients with identifiable non- microvascular causes of acute ocular motor mononeuropathy 3,27e29 Patients aged 50 years or older presenting with neurologically hasrangedfrom1%to15%. On the basis of these isolated third, fourth, or sixth cranial nerve palsies within 30 days findings, some authors recommend that early neuroimaging of onset were prospectively evaluated by neuro-ophthalmologists with MRI be performed during the initial evaluation of adults at 10 centers from June 2010 to December 2011. Patients with presenting with acute ocular motor mononeuropathies,3,27,28,30 a history of strabismus, orbital disease, head trauma, neurosurgical 2264 Ó 2013 by the American Academy of Ophthalmology ISSN 0161-6420/13/$ - see front matter Published by Elsevier Inc. http://dx.doi.org/10.1016/j.ophtha.2013.04.009 Tamhankar et al MRI in Patients with 3-4-6 Nerve Palsy intervention, or lumbar puncture, or those for whom an MRI could Table 1. Distribution of the 109 Enrolled Patients across Centers not be obtained were excluded from the study. Neurologically isolated palsy was defined as the absence of other Center No. signs and symptoms, with the exception of headache or periorbital University of Pennsylvania 31 pain, within 1 month of the onset of diplopia and during follow-up Brigham and Women’s Hospital 20 until enrollment. A standardized protocol was used to document the Emory University 19 time course of diplopia symptoms, the presence of headache or pain, Wilmer Eye Institute 13 and a history of vasculopathic risk factors other than older age (i.e., Michigan State University 6 diabetes mellitus, hypertension, hypercholesterolemia, stroke, University of Minnesota 6 myocardial infarction, coronary artery disease, and tobacco use). University of Illinois 4 The presence or absence of a history of neurologic disease, ocular University of California at Los Angeles 4 motor palsy, or cancer or any other pertinent history was assessed by University of Colorado 3 the examining neuro-ophthalmologist. Magnetic resonance imaging University of Maryland 3 of the brain with and without gadolinium was obtained for all patients who presented with no prior neuroimaging or computed tomography (CT) scan only, performed for this acute event. All patients were followed until the resolution of diplopia or until 1e30 days). Sixty percent of the cohort (n¼65) experienced pain adefinitive diagnosis was established for their ocular motor palsy. or headache in association with double vision, and the presence or Results of diagnostic testing (e.g., erythrocyte sedimentation rate, C- absence of pain was not predictive of the cause of the palsy. reactive protein, acetylcholine receptor antibody test, temporal There were 22 patients with a cranial nerve III palsy (18 were artery biopsy, and lumbar puncture) were recorded when obtained. partial and 4 were complete with pupillary sparing), 25 patients At the end of follow-up, the patients were determined to have had an with a cranial nerve IV palsy, and 62 patients with a cranial nerve ocular motor palsy due to presumed microvascular ischemia versus VI palsy. Seventy-one patients presented with neuroimaging another cause. A presumed microvascular cause was assigned in (CT or MRI scan) before presentation, while a prospective MRI those patients for whom the MRI scan and clinical testing did not was obtained in 39 patients (36%). A total of 103 patients (95%) reveal an alternative cause, other neurologic signs remained absent, were reexamined during follow-up at 8 to 12 weeks, whereas in and the ophthalmoparesis resolved spontaneously.36 6 patients, follow-up was obtained via telephone contact. A panel of neuro-ophthalmologists (S.L.G., G.T.L., and Of the 109 subjects, neuroimaging and other studies identified M.A.T.) reviewed all the patient data and classified the patients into a nonmicrovascular cause in 18 patients (16.5%; 95% CI, 2 groups on the basis of the presence of relevant medical history. 10.7e24.6), while 91 patients (83.5%; 95% CI, 75.4e89.3) were Group I included patients for whom the history and clinical diagnosed with a presumed microvascular palsy. The comparisons examination suggested a different cause for the third, fourth, or of patient characteristics between the presumed microvascular sixth cranial nerve palsy (e.g., history of neurologic symptoms, ischemia group and the other causes are shown in Table 2. worsening eye pain or headache, progression of diplopia, history of Distribution of age and sex was similar between the 2 groups. The cancer, history of immunosuppression). Group 2 included patients percentage of patients with 1 or more vasculopathic risk factors who presented with isolated third, fourth, or sixth cranial nerve (diabetes, hypertension, hypercholesterolemia, coronary artery palsy with vasculopathic risk factors alone. These groups were disease, myocardial infarction, stroke, and smoking) was further divided into subgroups: patients with no prior neuroimaging significantly higher in patients with presumed microvascular versus patients who presented to the study examiner with a prior ischemia than in those with other causes (91.2% vs. 61.1%; P ¼ CT or MRI of the brain that had been performed for the inclusion 0.003, Fisher exact test). In univariate analysis, the association event. Study data were collected using a Microsoft Access database of diabetes with presumed microvascular palsy was most frequent, (Microsoft Corp, Redmond, WA) and transferred into SAS version although this did not reach significance (P ¼ 0.06). Vasculopathic 9.2 (SAS Inc., Cary, NC) for statistical analysis. Mean, standard risk factors also were present in 11 of the 18 patients (61%) with deviation (SD), median, and range were used to summarize the other causes. The sixth cranial nerve was the most commonly continuous variables; proportions and 95% confidence intervals involved and had the highest incidence of other causes. (CIs)
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