Risk of Acute Ischemic Stroke in Patients With Monocular Vision Loss of Vascular Etiology

To evaluate the risk of concurrent acute ischemic stroke and monocular vision loss (MVL) of vascular etiology. Retrospective, cross-sectional study. Patients aged 18 or older diagnosed with MVL of suspected or confirmed vascular etiology who had no other neurologic deficits and who received brain MRI within 7 days of onset of visual symptoms were included. A medical record review was performed from 2013 to 2016 at Yale New Haven Hospital. Patients were included if vision loss was unilateral and due to transient monocular vision loss (TMVL), central retinal artery occlusion (CRAO), or branch retinal artery occlusion (BRAO). Any patients with neurologic deficits other than vision loss were excluded. Other exclusion criteria were positive visual phenomena, nonvascular intraocular pathology, and intracranial pathology other than ischemic stroke. The presence or absence of acute stroke on diffusion-weighted imaging (DWI) on brain MRI. A total of 641 records were reviewed, with 293 patients found to have MVL. After excluding those with focal neurologic deficits, there were 41 patients who met the inclusion criteria and received a brain MRI. Eight of the 41 subjects (19.5%) were found to have findings on brain MRI positive for acute cortical strokes. The proportion of lesion positive MRI was 1/23 (4.3%) in TMVL subjects, 4/12 (33.3%) in CRAO subjects, and 2/5 (40%) in BRAO subjects. Brain computed tomography (CT) scans were not able to identify the majority of acute stroke lesions in this study. Patients with MVL of vascular etiology such as TMVL, CRAO, or BRAO may have up to 19.5% risk of concurrent ischemic stroke, even when there are no other neurologic deficits. These strokes were detected acutely with brain MRI using DWI but were missed on CT.

Original Contribution Risk of Acute Ischemic Stroke in Patients With Monocular Vision Loss of Vascular Etiology Lucy Y. Zhang, MD, MEng, Jason Zhang, MD, Richard K. Kim, MD, Jared L. Matthews, MD, Danielle S. Rudich, MD, David M. Greer, MD, Robert L. Lesser, MD, Hardik Amin, MD Background: To evaluate the risk of concurrent acute ischemic stroke and monocular vision loss (MVL) of vascular etiology. Design: Retrospective, cross-sectional study. Subjects: Patients aged 18 or older diagnosed with MVL of suspected or confirmed vascular etiology who had no other neurologic deficits and who received brain MRI within 7 days of onset of visual symptoms were included. Methods: A medical record review was performed from 2013 to 2016 at Yale New Haven Hospital. Patients were included if vision loss was unilateral and due to transient monocular vision loss (TMVL), central retinal artery occlusion (CRAO), or branch retinal artery occlusion (BRAO). Any patients with neurologic deficits other than vision loss were excluded. Other exclusion criteria were positive visual phenomena, nonvascular intraocular pathology, and intracranial pathology other than ischemic stroke. Main Outcome Measures: The presence or absence of acute stroke on diffusion-weighted imaging (DWI) on brain MRI. Results: A total of 641 records were reviewed, with 293 patients found to have MVL. After excluding those with focal neurologic deficits, there were 41 patients who met the inclusion criteria and received a brain MRI. Eight of the 41 subjects (19.5%) were found to have findings on brain MRI positive for acute cortical strokes. The proportion of lesion positive MRI was 1/23 (4.3%) in TMVL subjects, 4/12 (33.3%) in CRAO subjects, and 2/5 (40%) in BRAO subjects. Department of Ophthalmology and Visual Sciences (LYZ, JZ, JLM, DSR, RLL), Yale University School of Medicine, New Haven, Connecticut; Yale University School of Medicine (RKK), New Haven, Connecticut; The Eye Care Group (DSR, RLL), New Haven, Connecticut; and Department of Neurology (DMG, HA), Yale University School of Medicine, New Haven, Connecticut. Presented at the American Academy of Ophthalmology Annual Meeting, November 14-17, 2015, Las Vegas, NV. The authors report no conflicts of interest. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the full text and PDF versions of this article on the journal's Web site (www. jneuro-ophthalmology.com). Address correspondence to Jason Zhang, MD, Department of Ophthalmology and Visual Sciences, Yale University School of Medicine, 40 Temple Street, Suite 3D, New Haven, CT 06510; E-mail: [e-mail] 328 Brain computed tomography (CT) scans were not able to identify the majority of acute stroke lesions in this study. Conclusions: Patients with MVL of vascular etiology such as TMVL, CRAO, or BRAO may have up to 19.5% risk of concurrent ischemic stroke, even when there are no other neurologic deficits. These strokes were detected acutely with brain MRI using DWI but were missed on CT. Journal of Neuro-Ophthalmology 2018;38:328-333 doi: 10.1097/WNO.0000000000000613 © 2018 by North American Neuro-Ophthalmology Society T he pathogenesis of monocular vision loss (MVL) of ischemic origin, categorized as transient monocular vision loss (TMVL), central retinal artery occlusion (CRAO), or branch retinal artery occlusion (BRAO), is considered to be analogous to that of a transient ischemic attack (TIA) or ischemic cerebral stroke (1). The 2009 revised definition of a TIA by the American Heart Association and the American Stroke Association (AHA/ASA) is "a transient episode of neurological dysfunction caused by focal brain, spinal cord, or retinal ischemia, without acute infarction" (2). Similarly, the updated 2013 definition of stroke by AHA/ASA is "brain, spinal cord, or retinal cell death attributable to ischemia, based on neuropathological, neuroimaging, and/or clinical evidence of permanent injury" (3). The ophthalmic artery is the first major branch off of the internal carotid artery. Therefore, it is reasonable to expect that emboli from a proximal source such as the heart, aorta, or carotid artery that affects the retinal vasculature could also cause brain ischemia by occluding the more distal anterior and middle cerebral arteries (4). The evidence for stroke after ischemic retinal events has been steadily increasing. A European prospective study of 77 CRAO patients enrolled in the European Assessment Group for Lysis in the Eye (EAGLE) study found that 5 patients (6%) had a newly diagnosed stroke within 1 month, of which only 1 was silent (5). Interestingly, 2 of Zhang et al: J Neuro-Ophthalmol 2018; 38: 328-333 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution the stroke patients in this study experienced their strokes immediately after local intra-arterial fibrinolysis. A Taiwanese population-based study showed that 19.6% of retinal artery occlusion patients had a stroke within a 3-year followup period, compared with 10.1% of matched controls. The highest incidence of stroke was within the first month after the retinal artery occlusion. The overall adjusted hazard ratio for having a stroke in these patients was 2.07 times higher than that of controls and 3.34 times higher in the #60-year-old subgroup (6). A Korean study of CRAO patients showed that the incidence rate ratio of ischemic stroke is significantly increased in the period just before and just after a CRAO, with the highest risk in the first 7 days after a CRAO (7). Two recent retrospective studies have shown that patients with MVL of ischemic origin are also more likely to have concurrent acute brain infarcts with a frequency of approximately 1 in 4 patients (8,9). Helenius et al (8) analyzed 129 patients with MVL of presumed ischemic origin and found that 31 (24.0%) of these patients had concurrent infarcts demonstrated on MRI imaging. Helenius et al did do a subgroup analysis of patients with isolated MVL (i.e., without other focal neurological signs at the time of presentation) and found that approximately 20% of these patients had a concurrent acute cerebral infarct. Lee et al (9) studied 33 patients with funduscopic evidence of acute retinal artery occlusion and found that 8 (24.2%) had concurrent acute brain infarctions of which only 3 (9.1%) had isolated MVL. The studies by Helenius et al and Lee et al had a disproportionate number of patients with additional focal neurological deficits (29% and 62.5%, respectively). Although patients with focal neurological symptoms are very likely to undergo brain imaging, those with isolated MVL may not. It is, therefore, important to characterize the true risk of an otherwise "clinically silent" stroke in patients with isolated MVL as the presenting symptom. Lauda et al (10) studied a cohort of patients with TMVL, CRAO, and BRAO seen at a single ophthalmic emergency department. The authors suggested that there is likely a high incidence of concurrent acute cerebral infarction in patients with isolated MVL but did not exclude patients with other focal neurological deficits from their study and subgroup analyses. The purpose of our study was to evaluate the risk of concurrent stroke as identified by MRI with diffusionweighted imaging (DWI) within 1 week of the onset of MVL (either transient of permanent) due to a vascular cause. We wanted to determine the true risk of a "silent stroke" in which the only presenting symptom was the MVL. METHODS The study protocol was approved by the Human Investigations Committee of the Yale University School of Zhang et al: J Neuro-Ophthalmol 2018; 38: 328-333 Medicine. A retrospective cross-sectional study was conducted through a chart review of all patients presenting to Yale New Haven Hospital with either transient or permanent MVL of vascular etiology (TMVL, CRAO, BRAO, and ophthalmic artery occlusion) between February 2013 and June 2016. Charts were selected through a review of ICD-9 codes. The inclusion criteria were age greater than 18 years; MVL with presumed or confirmed vascular etiology; and acquisition of a brain MRI within 7 days of onset of visual symptoms that included DWI. The exclusion criteria were bilateral vision loss, the presence of concurrent neurological symptoms not involving the visual pathways detected within 48 hours of presentation, the presence of concurrent higher order visual phenomenon including photopsias and aura, and the presence of intracranial pathology on MRI other than stroke. The diagnosis of vascular etiologies of MVL was made based on a combination of patient history, examination and findings, fundus photography, and fluorescein angiography. All patients included in the study were evaluated by both an ophthalmologist and a neurologist at Yale New Haven Hospital, and all patients with a cerebral infarct were managed accordingly. MRI scans were reviewed in all cases by an experienced neuroradiologist at Yale New Haven Hospital, and the images were re-reviewed to confirm the radiologist report for the purposes of this study. A total of 641 charts that included the previously mentioned ICD-9 codes were reviewed; of which 41 patients met the inclusion criteria for the study. These charts were analyzed with respect to various patient characteristics including age, sex, ethnicity, vascular risk factors (i.e., hypertension, diabetes, hyperlipidemia, atrial fibrillation, coronary artery disease), smoking status, history stroke/TIA, and cancer. One-way analysis of variance (ANOVA) was used to compare baseline demographics and risk factors and Fisher exact tests were used to assess associations of etiologies between patients with and without infarcts. Statistical analyses were performed using SAS 9.3 (SAS Institute, Inc, Glastonbury, CT). The primary outcome of this study was to assess the rate of co-occurrence of neurologically silent acute ischemic stroke and MVL of vascular etiology (TMVL, CRAO, BRAO ophthalmic artery occlusion) as diagnosed by MRI with DWI protocol. A secondary outcome was to evaluate the association between neurologically silent acute ischemic stroke in this setting and patient characteristics and comorbid medical conditions. RESULTS A total of 641 records were reviewed with 327 patients found to have MVL between February 2013 and June 2016. After excluding those with focal neurologic deficits (155), those without MRI imaging within 7 days of presentation (104), and those with intracranial pathology other than stroke (27), the inclusion criteria were met by 41 329 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. Flowchart of selection of patients with transient or permanent visual loss due to a vascular cause. MVL, monocular vision loss. patients and 41 eyes with either transient or permanent MVL of vascular etiology (Fig. 1). Patient demographics and characteristics are listed in Table 1. The average patient age was 64.8 years (SD, 13.5 years; range, 43-98 years), and the majority were men (68.2%). Most of the patients were Caucasian (70.7%) Nearly, all patients had comorbid risk factors at the time of presentation. The characteristics of the patients with available visual data (38 eyes) are listed in Table 2. Most patients presented with a visual acuity of at least 20/40 or better (58.5%), and 11 patients (30.6%) presented with a visual acuity of count fingers or worse. Among the 41 patients who met the inclusion criteria, 8 (19.5%) were found to have a MRI positive for acute cortical stroke (Fig. 2). Of these, 4 patients had CRAO, 2 had BRAO, 1 had TMVL (14.3%), and 1 had an ophthalmic artery occlusion. Brain computed tomography (CT) was able to identify acute infarction in only 2 patients. Of the 8 patients, 2 were found to have carotid stenosis of at least 70%. The proportion of patients with positive MRI findings was 1/23 for TMVL, 3/12 for CRAO, 2/5 for BRAO, and 1/1 for ophthalmic artery occlusion. A 1-way ANOVA analysis was conducted for each comorbid risk factor among our patient cohort patients with TMVL, CRAO, and BRAO to see if there was a statistically significant association between risk factor and MVL etiology (See Supplemental Digital Content, Table E1, http://links.lww.com/WNO/A289). Coronary artery disease, a history of stroke or TIA, and hypertension were 330 found in a statistically significant higher proportion of patients with CRAO than in patients with TMVL and BRAO with P values , 0.05. Likewise, atrial fibrillation was found in a statistically significant higher proportion of patients with BRAO than in patients with TMVL and CRAO with a P value , 0.05. No other statistically significant association was found. A Fisher exact test was also conducted for the same comorbid risk factors used in the ANOVA analysis TABLE 1. Patients with transient or permanent visual loss of vascular etiology Demographics Male Female Average age, yr Caucasian Hypertension Diabetes Mellitus Prior stroke or transient ischemic attack Coronary artery disease Atrial fibrillation Hyperlipidemia Tobacco use Hypercoagulable risk factors Eyes (N = 41) 28 (68.2%) 13 (21.8%) 64.5 (SD 13.5; range 43-98) 29 (70.7%) 31 (75.6%) 6 (14.6%) 7 (17.1%) 13 (31.7%) 8 (19.5%) 21 (51.2%) 14 (34.1%) 5 (12.2%) Zhang et al: J Neuro-Ophthalmol 2018; 38: 328-333 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 2. Visual function parameters of patients with transient or permanent visual loss due to a vascular cause Characteristics Eyes (N = 38)* Right sided visual symptoms Visual acuity better than or equal to 20/40 at presentation Visual acuity worse than or equal to count fingers at presentation Permanent visual deficits (.24 h) 23 (56.0%) 23 (62.1%) 12 (32.4%) 18 (43.9%) *Visual data were not available for 3 eyes. between patients with positive MRI findings and those with normal MRI findings (See Supplemental Digital Content, Table E2, http://links.lww.com/WNO/A290). A statistically higher proportion of patients with positive MRI findings also had concurrent hypercoagulability risk factors. No other statistically significant risk factor was identified. DISCUSSION The management of transient and permanent MVL without other neurologic symptoms or signs typically is for giant cell arteritis and embolic causes. This includes hematologic studies for acute phase reactants and carotid ultrasound and echocardiography. Most patients are not urgently evaluated nor do they frequently receive a full stroke work-up. A population-based study in the United Kingdom found that average time to referral and time to carotid ultrasound for patients with TMVL were 16 and 46 days, respectively (11). The North American Symptomatic Carotid Endarterectomy Trial (NASCET) found that patients with transient ischemic events of the retina had a longer average time of delay to medical treatment compared with patients with hemispheric TIAs, 48.5 vs 15.2 days, respectively (12). The American Heart Association/American Stroke Association recommends that patients with TIA be evaluated as soon as possible and undergo MRI with DWI within 24 hours of the symptom onset (2). In our study, we found that the rate of concurrent silent brain infarcts detected on MRI with DWI sequence was 19.5%. This finding is in contrast to the rate of incidental acute infarcts identified on DWI imaging in patients without clinical symptoms, which was reported to be 0.37% in a study of 16,206 individuals at a university hospital in Japan (13). An interesting finding of our study was that the strokes identified varied from singular to multifocal, and varied in size. Many of these infarcts were only seen on DWI sequence and not identified on CT. Multifocal infarcts suggest an embolic cause. Although the NASCET study found that the risk of subsequent ipsilateral stroke was lower after TMVL compared with hemispheric TIA in patients with carotid stenosis, there are Zhang et al: J Neuro-Ophthalmol 2018; 38: 328-333 certain features that may identify higher risk patients for whom carotid revascularization should be considered (advanced age, male gender, lack of collateral flow, peripheral vascular disease, and carotid stenosis .80%) (14,15). Carotid revascularization in patients with 2 or 3 of these risk factors led to a 3-year stroke absolute risk reduction of 4.9% and 14.3%, respectively. Silent brain infarcts are associated with adverse neurological and cognitive consequences, including impaired mobility, physical decline, depression, cognitive dysfunction, dementia, and clinical stroke (16). The risk of a subsequent stroke after a TIA or a minor stroke (defined as having no symptoms or no disability) has been reported to be 1.5%-3.9% within 2 days, increasing to 3.7%- 14.6% within 90 days (17,18). The Rotterdam Scan Study found that patients with silent brain infarcts experienced a 5 times higher incidence of follow-up stroke over an average 4.2 years than those without (19). When adjusted for other stroke risk factors, the adjusted hazard ratio for stroke was still 3.9 in patients with silent brain infarcts seen on MRI. Given this evidence, patients with MVL due to a vascular cause need to be evaluated urgently for stroke and given appropriate medical or surgical treatment. Unfortunately, this is not the practice pattern of most ophthalmologists. A survey of providers in the United States showed that only 35% of ophthalmologists would refer a patient with CRAO to the emergency department for immediate evaluation, whereas more neurologists (73%) and neuro-ophthalmologists (86%) would send patients with CRAO to the emergency department (20). A study in the United Kingdom demonstrated that even 3 years after introducing a daily TIA clinic at Leicester Royal Infirmary offering single-visit imaging (MRI and carotid ultrasound) and implementation of best medical therapy, almost none of the providers in the ophthalmology department reported referring a patient with TMVL to this clinic (21). Instead, 95% of the survey respondents reported a preference for sending patients for outpatient carotid ultrasound with a follow-up referral for carotid endarterectomy as needed. Interestingly, 90% of the respondents were aware of the TIA clinic and the services it provided. This study underscores the importance of increasing generalized awareness that MVL is a risk factor for concurrent and subsequent stroke. Limitations of our study included a small patient sample size. The requirement of TMVL, CRAO, or BRAO with a brain MRI done within 7 days, and excluding all patients with other neurologic deficits left a limited number of qualifying subjects for analysis. However, our strict inclusion and exclusion criteria provided a realistic assessment of the risk of concurrent acute stroke in patients with isolated MVL without other neurologic symptoms that would otherwise prompt brain imaging. Longer patient follow-up would also help determine the rate of subsequent TIA or stroke in these patients. Another limitation was the 331 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution inclusion of some patients based on subjective negative visual phenomena without a dilated funduscopic examination by an ophthalmologist. The retrospective nature of the study lends itself to possible bias in terms of why certain providers decided to obtain a brain MRI on some patients and not others. This bias would be eliminated with FIG. 2. Acute ischemic stroke in patients with monocular vision loss of vascular etiology. 332 Zhang et al: J Neuro-Ophthalmol 2018; 38: 328-333 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution a prospective study in which all patients with MVL due to a vascular case underwent brain MRI. REFERENCES 1. 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