Long-Term Disability Outcomes for Patients With Ischemic Stroke Presenting With Visual Deficits

Ischemic strokes in both the anterior and posterior circulation can lead to visual deficits, which can affect functional ability. Thrombolytic therapies are often withheld to patients with visual deficits because of either being missed on initial evaluation or because of the misconception that their deficits are not as severe or as disabling. Alternatively, delays in patient arrival for emergent evaluation lead to missed opportunities for acute stroke treatment. This retrospective study aims to explore the differences in perceived long-term disability for patients with stroke who present with visual deficits vs those who do not as a manifestation of their acute stroke syndrome. In addition, we explore the differences in treatment effect with thrombolytics and further analyze if the region of ischemia causing the deficit leads to differences in disability outcomes.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Long-Term Disability Outcomes for Patients With Ischemic Stroke Presenting With Visual Deficits Natalie Johnson, Tariq Nisar, MPH, Amber Criswell, BA, CCRC, David McCane, BA, CCRC, Jason Lee, RN, BNS, SCRN, David Chiu, MD, Rajan Gadhia, MD Background: Ischemic strokes in both the anterior and posterior circulation can lead to visual deficits, which can affect functional ability. Thrombolytic therapies are often withheld to patients with visual deficits because of either being missed on initial evaluation or because of the misconception that their deficits are not as severe or as disabling. Alternatively, delays in patient arrival for emergent evaluation lead to missed opportunities for acute stroke treatment. This retrospective study aims to explore the differences in perceived long-term disability for patients with stroke who present with visual deficits vs those who do not as a manifestation of their acute stroke syndrome. In addition, we explore the differences in treatment effect with thrombolytics and further analyze if the region of ischemia causing the deficit leads to differences in disability outcomes. Methods: We conducted a retrospective analysis of patients with visual deficits as evidenced by an abnormal score on NIHSS categories related to vision (gaze palsy, visual fields, or extinction/inattention). Patients with Acute Ischemic Stroke were reviewed from the Houston Methodist Hospital Outcomes-based Prospective Endpoints in Stroke (HOPES) Registry from 2016–2021 for visual deficits. In total, 155 patient charts with visual deficits and 155 patient charts without a documented visual deficit were reviewed for ischemic stroke location (anterior vs posterior circulation), NIHSS scores, and thrombolytic therapies. The outcome variable was categorized using mRS, as mRS between 0 and 3 while mRS 4 to 6 was considered as poor functional outcome at 90 days. The independent variable was the vision group. A multivariable logistic regression model was constructed adjusting for demographics and comorbidities on the binary outcome. Results: Multivariable logistic model after adjusting for demographics and comorbidities showed that patients with acute ischemic stroke with vision defects were 4 times Houston Methodist Neurological Institute (AC, DM, JL, DC, RG), Houston, Texas; Houston Methodist Research Institute (NJ), Houston, Texas; and Center for Outcomes Research (TN), Houston, Texas. The authors report no conflicts of interest. Address correspondence to Natalie Johnson, Houston Methodist Research Institute, 315 Regent Circle, San Antonio, TX 78231; E-mail: [e-mail] 518 more likely to have poor functional outcomes at 90 days, with most of these patients (14% vs 6%; P , 0.05) suffering from severe disability compared with patients in the control group (i.e., patients with acute ischemic stroke without vision defects) (OR = 4.05; 95% CI [2.28–7.19]; P , 0.001). The application of thrombolytics and the location of ischemia (ACS vs PCS) did not result in a significant change in disability outcomes in patients with visual defects in this limited sample size. Conclusions: The results of this study indicated that a large population of patients with ischemic stroke experience visual deficits and are, therefore, at an increased likelihood of worse functional outcome. This reveals the necessity for rehabilitation techniques that specifically target visual deficits to speed up the recovery process of these patients. Further studies with larger sample size are needed to assess whether the location of ischemic event and the application of thrombolytic treatments plays a role in the disability outcomes of these patients. Journal of Neuro-Ophthalmology 2022;42:518–523 doi: 10.1097/WNO.0000000000001624 © 2022 by North American Neuro-Ophthalmology Society S troke is the number one cause of long-term disability and the fifth leading cause of death in the United States (1). Ischemic strokes account for approximately 87% of all strokes in the United States and are due to a blockage of a cerebral artery, leading to hypoxia that can cause significant damage to brain tissue (1). Depending on the location of the cerebral infarction, deficits in vision can occur. In one study that aimed to characterize patients with self-reported vision problems after an ischemic event, 25.4% of patients reported some type of visual deficit (2). Visual deficits can present as visual field defects (VFDs), monocular vision loss, gaze palsies, or inattention with neglect (2). The VFDs can be homonymous or nonhomonymous hemianopia or quadrantanopia, depending on the severity and location of ischemia present (3). The type of visual deficit is dependent on which vascular region is affected by the ischemic event. Johnson et al: J Neuro-Ophthalmol 2022; 42: 518-523 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Anterior circulation strokes (ACSs) are typically infarcts within the territory of the internal carotid artery branches and the ophthalmic artery, which can result in ipsilateral visual changes such as monocular vision loss or VFDs (3). Posterior circulation strokes (PCSs) due to infarcts in the posterior cerebral artery (PCA) or vertebrobasilar vascular regions can damage the visual pathway in the occipital lobe and result in binocular visual field defects (3). Furthermore, PCSs can also include brainstem strokes that can lead to ocular motor symptoms, such as gaze palsies; however, there is certainly overlap with anterior circulation infarcts (3). Acute ischemic strokes in the PCA territory, typically in the occipital lobe, are often missed during an acute evaluation because of inconsistent visual field testing often being inadequately performed or overlooked in an acute stroke evaluation. Oftentimes, strokes within this region present with isolated field cuts without the common stroke symptoms of unilateral weakness, aphasia, or ataxia. Computed tomography (CT) scans of patients with PCS have only limited sensitivity early on in the ischemia, which further increases the difficulty in detecting these infarctions during the hyperacute evaluation (4). The delays and often missed diagnoses can result in delayed treatment, which can exclude thrombolysis treatment in some cases because of exceeding the recommended 3–4.5 hour time window for treatment (4). PCSs are also underrepresented in the National Institute of Health Stroke Scale (NIHSS), which is weighted toward ACS, leading to further challenges in treating these patients in communication of quantitative severity of deficits (5). Patients who present primarily with visual deficits after an ischemic stroke may receive a low NIHSS score, depending on the affected region. In these patients, physicians acutely determine and weigh the benefits of live-saving thrombolytics, such as intravenous recombinant tissue-type plasminogen activator (r-tPA), with the risk of symptomatic intracranial hemorrhage (sICH) that can potentially occur with treatment (6,7). Typically, when making this decision, physicians weigh the types of neurological deficits that are present and determine whether the disability from those symptoms outweigh the risk of sICH. If the symptoms are perceived as less likely to be disabling or if they seem to rapidly improve to a point of nondisabling as per the patient and the provider, thrombolytic treatment may be withheld (6). However, many patients with mild or rapidly improving stroke symptoms experience poor disability outcomes without this treatment, as evidenced in the MaRISS trial that a large proportion of patients with low NIHSS scores have disabled outcomes (7–9). For patients with visual deficits, they may experience a greater risk of falling, difficulty reading, and depression that can make rehabilitation poststroke even more difficult (2,10,11). Those with VFD may also have difficulty recognizing their symptoms, which could lead to further safety Johnson et al: J Neuro-Ophthalmol 2022; 42: 518-523 issues, such as challenges while driving, in addition to difficulties with rehabilitation (12,13). In this retrospective review, we aim to determine the difference in 90-day disability outcome, as measured by the modified Rankin Scale (mRS) score, for patients with stroke presenting primarily with visual defects compared with those who do not manifest these deficits. Furthermore, we aim to analyze the difference in 90-day disability outcome for patients with visual deficits if they received thrombolytic interventions and to determine if the location of the infarction, whether ACS or PCS, changes the disability outcome. METHODS We conducted a retrospective analysis of patients with visual deficits due to an ischemic stroke from the Houston Methodist Hospital System. Relevant medical history, 90day mRS score, and thrombolytic decisions were collected from the Houston Methodist Hospital Outcomes-based Prospective Endpoints in Stroke (HOPES) Registry from 2016–2021 (14). The HOPES Registry contains information on patient age, sex, race, cardiovascular risk factors (including hypertension, diabetes, hyperlipidemia, atrial fibrillation, and smoking history), and discharge disposition. Of 4,726 patients who were collected in this registry, 3,275 patients (69%) were documented with Acute Ischemic Stroke (AIS). Patients with AIS with an abnormal NIHSS score on gaze palsy, visual fields, or extinction/inattention were included in this analysis (1,074 total: 32.8% of patients with AIS). Of these patients with documented visual deficits, 155 patient charts from 2020–2021 were reviewed to determine the location of stroke (hemisphere and ACS vs PCS). Another 155 AIS patient charts from 2020–2021 who presented with no visual defects (normal scores on visual categories of NIHSS) were similarly reviewed as a control. ACS was defined as an infarct in the anterior cerebral artery (ACA), middle cerebral artery (MCA), or fetal posterior cerebral artery (PCA) vascular territories while PCS was defined as an infarct in the vertebral artery, basilar artery, or PCA vascular territories (15,16). In the patient chart review, admission NIHSS score and discharge NIHSS score were recorded, in addition to the visual deficit subscores, to observe the overall symptom severity for patients presenting with visual deficits. In patients who received tPA treatment, the post-tPA NIHSS score was also recorded to track the efficacy of the treatment. Furthermore, in patients who received tPA treatment, the time from last known well until the start of treatment was reviewed to see if the patients with visual defects had delayed treatment decisions. Mechanical thrombectomy patients were also included, and their Thrombolysis in Cerebral Infarction (TICI) scores were recorded to assess the rate of reperfusion post-treatment (Table 1). 519 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Measures of central tendency are summarized, and descriptive characteristics are reported medians with interquartile ranges (IQR) for continuous variables and proportions for categorical variables. Median differences between continuous variables were identified with the Wilcoxon rank test. Differences between categorical variables were identified with chi-squared (x2) test. The outcome variable was categorized using mRS, as mRS between 0 and 3 while mRS 4 to 6 was considered as poor functional outcome at 90 days. The independent variable was the vision group. A multivariable logistic regression model was constructed adjusting for demographics and comorbidities on the binary outcome. The odds ratios (OR) and 95% confidence intervals (CI) were reported, providing likelihood estimates of a shift to higher mRS for a given comparison between control group (reference category) and vision group (Table 2). Statistical significance was defined as two-tailed P , 0.05 for all tests. All analyses were performed using R statistical software (version 3.6.3). RESULTS There was an even distribution of both sexes across the 2 groups (P . 0.05); however, patients in the vision group were significantly older compared with patients in the control group (median = 72 years (IQR [63.00–80.00]). vs median = 69 years (IQR [59.00–77.00]); P = 0.05). Furthermore, comorbidities were similar between the 2 groups, except for atrial fibrillation which had a higher proportion in patients with vision defects (56% vs 31%). The median admits NIHSS and discharge NIHSS was higher in patients with vision defects (15 vs 3; P , 0.001; and 7 vs 1; P , 0.001). The median post-tPA NIHSS was also found to be higher in patients with vision defects (8.5 vs 3.0; P = 0.006). In addition, 39% patients with vision defects received mechanical thrombectomy (MT) and 36% resulted in hemorrhagic transformation (HT), as compared with 10% MT and 6% HT in the control group (P , 0.05). Multivariable logistic model after adjusting for demographics and comorbidities showed that patients with acute ischemic stroke with vision defects were 4 times more likely to have poor functional outcomes at 90 days, with most of these patients (14% vs 6%; P , 0.05) suffering from severe disability compared with patients in the control group (i.e., patients with acute ischemic stroke without vision defects) (OR = 4.05; 95% CI [2.28–7.19]; P , 0.001). The application of thrombolytics and the location of ischemia (ACS vs PCS) did not result in a significant change in disability outcomes in patients with visual defects in this limited sample size. CONCLUSIONS In our retrospective study of patients presenting with a visual field deficit, as evidenced by questions on the NIHSS, 520 this cohort was 4 times more likely to have poorer outcomes when compared with patients without visual deficits because of their ischemic event. The HOPES Registry contained 1,074 patients with some form of visual deficit, which accounts for 33% of patients with AIS in the registry (3,275 patients). This indicates that a large population of patients with ischemic stroke face these deficits and are, therefore, at an increased likelihood of worse functional outcome. The NIHSS score for patients with visual deficits were also higher at all 3 documented time stamps (admission, post-tPA, and discharge). Patients with visual deficits were also older (median 72 vs 69 years; P = 0.05) and experienced a higher rate of atrial fibrillation (56% vs 31%; P , 0.001) when compared with the control population. This could indicate that visual deficits accompany more severe strokes as opposed to milder strokes and potentially a higher incidence of cardioembolism than other etiologies. This finding of worse outcomes for patients with stroke presenting with visual deficits has also been documented in other studies (17). The presence of visual deficits are associated with lower overall quality of life, increased risk of falling, and higher levels of institutionalization (10,12). In our review, vision patients experienced a significantly higher rate of discharge to skilled nursing facilities (16% vs 6%; P , 0.011) and hospice (22% vs 3%, P , 0.001) than patients without recorded visual deficits. Patients without deficits were significantly more likely to be discharged home than vision patients (65% vs 33%, P , 0.001), which can further indicate that their disabilities were not as severe. Quality of life and ability to perform activities of daily life (ADL) have been documented to be significantly affected by visual deficits (12). In one study, quality-of-life data were gathered for 63 patients and specifically assessed vision-related ADLs, such as impact on mobility, reading and writing, and visual recognition (12). The results of this found that visual recognition, mobility, and near vision tasks were all reduced in patients with visual deficits, which inhibited overall quality of life and functional outcomes of the patients (12). Because of this negative impact on functional outcome from visual deficits, rehabilitation techniques specifically targeting these defects are necessary. The visual deficits from strokes can resolve over time, but visual rehabilitation techniques can help speed up the recovery process for these patients (12). Visual search training, which consists of exercises that increase head movements and fast eye movements to scan the impaired side of a VFD, is associated with the greatest improvement in functional ability (11,12). The application of techniques such as visual search training could potentially improve functional outcomes in patients with visual deficits poststroke. Stroke localization can produce varied disabilities based on the visual deficit present. A pure PCA stroke may produce a dense homonymous hemianopia, which can Johnson et al: J Neuro-Ophthalmol 2022; 42: 518-523 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Baseline characteristics Sample Characteristics By Group From HOPES Registry Control No. 155 Age (median, IQR) Sex (N, %) Female Male Race (N, %) White Black Asian Decline/Others Comorbidities (N, %) Hypertension Diabetes mellitus Hyperlipidemia Atrial fibrillation Smoking Admit NIHSS (median, IQR) Post-tPA NIHSS (median, IQR) Discharge NIHSS (median, IQR) Discharge disposition (N, %) Home Rehabilitation Skilled nursing facility Long-term acute care Hospice Died IV-tPA (N, %) Time until tPA (median, IQR) Mechanical thrombectomy (N, %) Hemorrhagic transformation (N, %) TICI scores (N, %) TICI-2a TICI-2b TICI-2c TICI-3 Stroke affected (N, %) Left-affected stroke hemisphere Right-affected stroke hemisphere Both-affected stroke hemisphere Anterior circulation (N, %) MCA-anterior circulation ACA-anterior circulation Fetal PCA-anterior circulation Posterior circulation (N, %) Vertebral artery-posterior circulation Basilar artery-posterior circulation PCA-posterior circulation mRs binary comparison (N, %) mRs # 3 mRs 4–6 mRS (median, IQR) mRS ordinal scale (N, %) mRs-0 mRs-1 mRs-2 mRs-3 Vision No. 155 P 69.00 (59.00–77.00) 72.00 (63.00–80.00) 0.05 64 (41.29) 91 (58.71) 72 (46.45) 83 (53.55) 0.42 0.42 93 (62.00) 43 (28.67) 11 (7.33) 3 (2.00) 93 (62.84) 46 (31.08) 9 (6.08) 0 (0.00) 0.91 0.70 0.82 0.25 148 (95.48) 83 (53.55) 139 (89.68) 47 (30.52) 53 (35.33) 3.00 (1.00–6.00) 3.00 (1.50–7.00) 1.00 (0.00–4.00) 150 (96.77) 82 (52.90) 135 (87.66) 82 (56.16) 49 (37.69) 15.00 (7.00–21.00) 8.50 (4.00–13.75) 7.00 (2.00–17.75) 0.77 1.0 0.60 ,0.001 0.71 ,0.001 0.006 ,0.001 100 (64.52) 38 (24.52) 10 (6.45) 2 (1.29) 5 (3.23) 0 (0.00) 39 (25.16) 115.00 (88.00–157.25) 16 (10.32) 2 (5.56) 51 (32.90) 34 (21.94) 25 (16.13) 8 (5.16) 34 (21.94) 3 (1.94) 45 (29.03) 111.00 (85.00–155.00) 60 (38.71) 4 (36.36) ,0.001 0.69 0.011 0.10 ,0.001 0.25 0.52 0.82 ,0.001 0.021 1 3 2 8 (6.67) (20.00) (13.33) (53.33) 3 (5.26) 6 (10.53) 15 (26.32) 31 (54.39) 1.0 0.38 0.50 1.0 85 (54.84) 68 (43.87) 2 (1.29) 76 (49.03) 71 (45.81) 8 (5.16) 0.36 0.82 0.10 98 (85.22) 12 (10.43) 3 (2.61) 101 (86.32) 4 (3.42) 1 (0.85) 0.85 0.040 0.37 11 (27.50) 2 (5.00) 25 (62.50) 8 (21.05) 8 (21.05) 19 (50.00) 0.60 0.045 0.36 120 (77.42) 35 (22.58) 2.00 (1.00–3.00) 67 (43.23) 88 (56.77) 4.00 (2.00–6.00) ,0.001 ,0.001 ,0.001 38 36 25 21 7 (4.52) 16 (10.32) 22 (14.19) 22 (14.19) ,0.001 0.004 0.75 1.0 Johnson et al: J Neuro-Ophthalmol 2022; 42: 518-523 (24.52) (23.23) (16.13) (13.55) 521 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution (Continued ) Sample Characteristics By Group From HOPES Registry Control No. 155 mRs-4 mRs-5 mRs-6 12 (7.74) 10 (6.45) 13 (8.39) result in difficulties while driving. Although driving is not delineated on the mRS, it is certainly considered when evaluated during patient interviews. Patients presenting with pure PCA strokes are often scored lower on the NIHSS because of its preference for anterior ischemic strokes (5). More effective scoring tools should be implemented to evaluate posterior circulation presentations of stroke to prevent misdiagnoses or delayed diagnoses of these events. Larger cerebral hemispheric strokes may result in neglect or gaze palsy; however, evaluating these deficits presents with several limitations. Neglect, when visual, is often associated with higher mRS and higher NIHSS because of larger areas of ischemia and is categorized as a disabling feature of the stroke. This visual neglect can lead to more difficulties in rehabilitation by introducing another hurdle for patients to overcome in their recovery efforts. Furthermore, gaze palsy may be seen after a larger cerebral stroke, but it may be only a transient symptom. Gaze palsy resulting from posterior infarcts, such as from ischemic events in the brainstem, are unlikely to present with neglect. Localization of the ischemic event in the case of gaze palsy and neglect can help differentiate these 2 groups and yield results about the disability outcomes. However, because of the limited number of patients in this retrospective review, no meaningful conclusions can be drawn relating to infarct localization. Vision No. 155 21 (13.55) 22 (14.19) 45 (29.03) P 0.14 0.039 ,0.001 Although we attempted to extrapolate based on the NIHSS subscores and imaging findings as to the type of visual complaint, whether monocular vision loss, VFD, blurry vision, diplopia, etc., it was not specific to the clinical deficit. We also did not exclude patients who had prior vision problems. A future study could exclude prior visual complaints, such as glaucoma, cataracts, macular degeneration, or prior field defects, to isolate patients with visual deficits only from the cerebral infarction. Furthermore, investigation of the specific visual complaint could also help determine what symptoms result in worse functional outcomes overall. Stroke etiology also could have played a role in the poor disability outcomes experienced in visual deficit patients so future research into this is also necessary. One major limitation to this study was the limited sample size studied. The limited sample size of only 155 visual deficit patients reviewed did not allow any meaningful conclusions about functional disability outcomes to be drawn from the application of thrombolytic treatments (such as tPA or mechanical thrombectomy) to visual deficit patients or from the infarct location (ACS vs PCS). The limited sample size in this study also prevented any meaningful subgroup analysis of the visual deficit patients who presented with hemorrhagic transformations because of only 6 patients in the data set. Further research, therefore, is warranted with larger sample sizes to assess whether the TABLE 2. Statistical model Outcome Variable (mRs4-6 = 1 vs mRs # 3 = 0) Variable Group control Group vision Age Sex (male, female = reference) Race White Black Asian Others Hypertension (yes, no = reference) Hyperlipidemia (yes, no = reference) Diabetes (yes, no = reference) Atrial fibrillation (yes, no = reference) Smoking (yes, no = reference) 522 Odds Ratio (95% CI) Reference P Reference 4.05 (2.28–7.19) 1.04 (1.02–1.07) 0.86 (0.49–1.54) ,0.001 ,0.001 0.62 0.96 (0.49–1.87) 1.03 (0.33–3.24) 1.26 (0.09–17.22) 1.28 (0.24–6.99) 0.44 (0.18–1.03) 1.17 (0.66–2.11) 1.42 (0.79–2.55) 1.67 (0.91–3.04) 0.9 0.95 0.86 0.77 0.06 0.59 0.24 0.1 Johnson et al: J Neuro-Ophthalmol 2022; 42: 518-523 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution location of ischemic event and application of thrombolytic treatments plays a role in long-term disability outcomes for patients with visual defects. In our study, AIS with visual deficits is associated with an increased chance of poor functional outcomes than AIS without visual deficits after adjusting for comorbidities and demographics. Earlier recognition of patients with visual deficits could help reduce these functional disability outcomes by more aggressive hyperacute stroke treatment measures and earlier application of visual rehabilitation techniques. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: N. Johnson, A. Criswell, and R. Gadhia; b. Acquisition of data: N. Johnson, A. Criswell, D. McCane, J. Lee, D. Chiu, and R. Gadhia; c. Analysis and interpretation of data: N. Johnson, T. Nisar, and R. Gadhia. Category 2: a. Drafting the manuscript: N. Johnson and T. Nisar; b. Revising the manuscript for intellectual content: N. Johnson, T. Nisar, A. Criswell, and R. Gadhia. Category 3: a. Final approval of the completed manuscript: N. Johnson, T. Nisar, A. Criswell, and R. Gadhia. REFERENCES 1. Barthels D, Das H. 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