Frequency and Etiologies of Visual Disturbance After Cataract Surgery Identified in Neuro-Ophthalmology Clinics

Background: To identify the frequency and etiologies of visual disturbances after cataract surgery in patients referred to Neuro-ophthalmology. Methods: This study is a retrospective chart review. Records of patients 18 years and older referred to neuro-ophthalmology clinics for new-onset visual disturbances within 6 months of cataract surgery were reviewed. Those with pre-existing neuro-ophthalmic disorders, combined intraocular procedures with cataract surgery, or inadequate follow-up were excluded. The main outcome measures were frequency and etiologies of visual disturbances after cataract surgery. Secondary analyses of a cohort of patients who had cataract surgery at our institution were performed to determine the frequency and etiology of visual disturbances after uneventful cataract surgery. Results: One hundred seventy-three patients met the inclusion criteria (internal referral: 36/173, from outside surgeons: 137/173). Sixty-one percent (106/173) were newly diagnosed with neuro-ophthalmic etiologies, including 21% (36/173) with afferent and 40% (70/173) with efferent disorders. Thirty-six percent (62/173) of patients had non neuro-ophthalmic causes and 3% (5/173) had systemic conditions responsible for visual disturbances postoperatively. Decompensated strabismus causing diplopia was the most common neuro-ophthalmic diagnosis after cataract surgery (50%, 53/106). Of the 13,715 patients who had cataract surgery performed at our institution over a 9-year period, 20 of 36 patients referred for visual disturbances were identified with neuro-ophthalmic etiologies of which 85% (17/20) had postoperative diplopia. Conclusions: In our study, decompensated strabismus causing diplopia was the most common neuro-ophthalmic visual disturbance after cataract surgery. Detailed history and ocular alignment should be assessed before cataract surgery to identify patients with the risk.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Frequency and Etiologies of Visual Disturbance After Cataract Surgery Identified in Neuro-Ophthalmology Clinics Shuai-Chun Lin, MD, Angie Giang, BS, Grant T. Liu, MD, Robert A. Avery, DO, Kenneth S. Shindler, MD, Ali G. Hamedani, MD, MHS, Ahmara G. Ross, MD, PhD, Madhura A. Tamhankar, MD Background: To identify the frequency and etiologies of visual disturbances after cataract surgery in patients referred to Neuro-ophthalmology. Methods: This study is a retrospective chart review. Records of patients 18 years and older referred to neuroophthalmology clinics for new-onset visual disturbances within 6 months of cataract surgery were reviewed. Those with pre-existing neuro-ophthalmic disorders, combined intraocular procedures with cataract surgery, or inadequate follow-up were excluded. The main outcome measures were frequency and etiologies of visual disturbances after cataract surgery. Secondary analyses of a cohort of patients who had cataract surgery at our institution were performed to determine the frequency and etiology of visual disturbances after uneventful cataract surgery. Results: One hundred seventy-three patients met the inclusion criteria (internal referral: 36/173, from outside surgeons: 137/173). Sixty-one percent (106/173) were newly diagnosed with neuro-ophthalmic etiologies, including 21% (36/173) with afferent and 40% (70/173) with efferent disorders. Thirty-six percent (62/173) of patients had non neuro-ophthalmic causes and 3% (5/ 173) had systemic conditions responsible for visual disturbances postoperatively. Decompensated strabismus causing diplopia was the most common neuro-ophthalmic diagnosis after cataract surgery (50%, 53/106). Of the 13,715 patients who had cataract surgery performed at Departments of Ophthalmology (S-CL, AG, GTL, RAA, KSS, AGH, AGR, MAT) and Neurology (S-CL, GTL, RAA, KSS, AGH, MAT), University of Pennsylvania, Philadelphia, Pennsylvania. Portions of this study were previously presented in the American Academy of Ophthalmology Annual Meeting, 2020. (11/13-15, 2022, virtual meeting). The authors report no conflicts of interest. Address correspondence to Madhura A. Tamhankar, MD, Department of Ophthalmology and Neurology, Scheie Eye Institute, 51N, 39th Street, Philadelphia, PA 19104; E-mail: madhura.tamhankar@ pennmedicine.upenn.edu Lin et al: J Neuro-Ophthalmol 2023; 43: 359-363 our institution over a 9-year period, 20 of 36 patients referred for visual disturbances were identified with neuro-ophthalmic etiologies of which 85% (17/20) had postoperative diplopia. Conclusions: In our study, decompensated strabismus causing diplopia was the most common neuro-ophthalmic visual disturbance after cataract surgery. Detailed history and ocular alignment should be assessed before cataract surgery to identify patients with the risk. Journal of Neuro-Ophthalmology 2023;43:359–363 doi: 10.1097/WNO.0000000000001792 © 2023 by North American Neuro-Ophthalmology Society C ataract surgery is the most common elective surgical procedure worldwide (1). Previous studies have shown that improvement in visual outcomes after cataract surgery strongly correlate with improved quality of life and patientreported health outcomes (2). Although expectations of visual recovery after cataract surgery are high, patients may experience visual disturbances after cataract surgery due to ocular and rarely neuro-ophthalmic causes (3). Neuro-ophthalmic conditions such as those causing diplopia (4–6) and optic neuropathies (7,8) after cataract surgery are uncommon but visually debilitating and may be undiagnosed before cataract surgery because of media opacity and failure to recognize occult neuro-ophthalmic disorders leading to potentially missing a serious underlying systemic or central nervous system (CNS) pathology (9). We investigated the etiologies contributing to postcataract surgery visual disturbances among patients who were referred to our neuro-ophthalmology clinics, including referrals from both inside and outside our institution. We also assessed the prevalence of neuro-ophthalmic disorders identified among patients who underwent cataract surgery at our institution over a 9-year period. 359 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution METHODS Study Population The study was approved by the Institutional Review Board of the University of Pennsylvania. We performed a retrospective chart review of adult patients seen by 6 neuro-ophthalmologists at the University of Pennsylvania between January 2010 and October 2019. Patients were identified by their electronic medical records (EMRs) using PennSeek. PeenSeek (http://www.med. upenn.edu/dac/pennseek.html) is a natural language search tool developed by the Penn Medicine Data Analytics Center to search EMRs with targeted keywords. The patient list was generated after querying outpatient encounters in the neuro-ophthalmology division with free-text search throughout the patient encounter (including reason for referral, chief complaint, ophthalmic examination, impression, and plan) for any of the targeted keywords: “history of cataract surgery,” “cataract surgery,” “new patient visit,” “pseudophakia,” or “posterior chamber intraocular lens,” followed by a manual chart review to identify patients referred to neuro-ophthalmology clinics for changes of vision that were reported within 6 months after cataract surgery. The changes of vision referred to all visual complaints that the patients had for which the referring doctors requested a neuro-ophthalmology consult. Patients with known previous neuro-ophthalmic disorders, those who had undergone combined intraocular procedures along with cataract surgery, and patients lost to follow-up were excluded. Patient demographics, medical history including ocular comorbidities, neuro-ophthalmic examination, and diagnostic test results were collected. Secondary analyses of all patients who underwent cataract surgery at the Scheie Eye Institute was performed to determine the prevalence of neuro-ophthalmic disorders contributing to visual disturbances after uneventful cataract surgery in this cohort. Outcome Measures The main outcome measure was the identification of a neuro-ophthalmic etiology as the cause for visual disturbance occurring after cataract surgery. The secondary outcome measure was the prevalence of a neuroophthalmic disorder causing a visual disturbance within 6 months after cataract surgery in those who underwent cataract surgery at the Scheie Eye Institute during the study period. Neuro-ophthalmic etiologies were defined as disorders involving an afferent or efferent visual pathway, including optic neuropathies, CNS lesions with visual pathway involvement, higher-order cortical visual impairment, eye movement abnormalities, strabismus, pupillary abnormalities, and systemic disorders with ocular involvement. Patients were diagnosed with decompensated strabismus if they had comitant heterophorias with full extraocular motility and no other identifiable neuromuscular cause. 360 Congenital fourth nerve palsy was diagnosed based on history, observation of head tilt, and presence of .2 prism diopters (PD) of vertical fusional amplitude. Optic neuropathy was identified when patients had decreased visual acuity, dyschromatopsia, positive afferent pupillary defect (APD), or optic disc edema or pallor. The diagnosis of nonarteritic ischemic optic neuropathy (NAION) was made based on patients’ history of sudden visual loss, disc edema followed by disc pallor in 4–6 weeks, and crowded optic disc in the fellow eye, with presence of vasculopathic risk factors and/or sleep apnea. Some of the patients underwent laboratory testing looking for inflammatory, infectious, nutritional/toxic etiologies, or brain imaging studies if structural abnormalities were suspected. Statistical Analyses All statistical tests were 2-sided with 95% confidence interval (CI), using SPSS statistical software (version 24.0; IBM Corp, Armonk, NY). Frequencies and medians of demographic variables were calculated. Data were compared across participants. Basic descriptive statistics including mean (range), SDs, and percentages were calculated for patient demographics, neuro-ophthalmic examination data, etiologies, and prevalence of visual disturbance. RESULTS Of the 1,460 patients identified with visual disturbances after cataract surgery, 220 were included after manual chart review screening for “new-onset visual disturbance” and “within 6 months after having the surgery.” Of the 1,240 patients who were excluded, most were excluded because the onset of visual disturbances occurred outside the 6month window. Forty-seven subjects were further excluded based on the exclusion criteria, leading to the final 173 eligible patients. Patients who had cataract surgery outside the institution constituted 79% (137/173) of the cohort while the rest 21% (36/173) of the patients had cataract surgery within the institution. The mean age at the time of cataract surgery was 69 (range: 20–96) years, with 60% female (104/173). Blurry vision was the most common symptom in neuroophthalmology clinic, followed by binocular double vision, light sensitivity, and scotoma in the visual field (Fig. 1). Of the 173 patients, 61% (106/173) were diagnosed with neuro-ophthalmic disorders: 21% (36/173) of the afferent visual pathway, 40% (70/173) with efferent disorders, 36% (62/173) with ocular causes, and 3% (5/ 173) with systemic conditions (Tables 1 and 2). The causes of afferent visual pathway disorders are listed in Table 1. These include optic neuropathies from NAION, nutritional/toxic, compressive, and idiopathic causes. The onset of NAION in 13 patients occurred between 10 days and 5 months postoperatively. Disc edema was found in 7 patients while the other 6 patients presented Lin et al: J Neuro-Ophthalmol 2023; 43: 359-363 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. Reasons for referral to neuro-ophthalmology clinic after cataract surgery (number of patients). Total 235 patients (some patients carry more than one diagnosis). with disc pallor with previous disc edema documented by the referring doctors. Nine of 13 patients had crowded disc in both eyes, and 11 of 13 patients had 1 or more systemic comorbidities including hypertension, diabetes, hyperlipidemia, and sleep apnea. Among 7 patients with compressive optic neuropathy, 6 had failure of visual improvement after cataract surgery and 3 had visual field defects (1 with monocular temporal defect, 1 with bitemporal, and 1 with homonymous visual defect). Three patients were diagnosed with a pituitary neoplasm, 3 with meningioma, and 1 with a left temporooccipital glioblastoma. TABLE 1. Neuro-ophthalmic etiologies among 106 patients after cataract surgery Etiologies Afferent Optic neuropathy NAION Unclear etiology* Nutritional/toxic Compressive optic neuropathy Posterior cortical atrophy Efferent Decompensated strabismus Vasculopathic cranial nerve palsy† Myotoxicity from retrobulbar anesthesia Thyroid eye disease Myasthenia gravis Head tremor–related oscillopsia Nystagmus Blepharospasm Skew deviation Number (%) 36 (34) 13 (12) 7 (7) 6 (6) 7 (7) 3 (3) 70 (66) 53 (50) 4 (4) 2 (2) 4 (4) 1 (1) 1 (1) 1 (1) 1 (1) 3 (3) *Negative MRI/blood work. † One with oculomotor nerve palsy, 2 with trochlear nerve palsy and 1 with abducens nerve palsy. NAION, nonarteritic ischemic optic neuropathy. Lin et al: J Neuro-Ophthalmol 2023; 43: 359-363 Three patients were diagnosed with posterior cortical atrophy (PCA) with the presentation of optic ataxia, simultanagnosia, ocular motor apraxia, progressive cognitive problems, and PCA on MRI. Decompensated strabismus causing diplopia was the most common neuro-ophthalmic etiology diagnosed after cataract surgery (76%, 53/70, Table 1). Overall, 58% had no history of diplopia before cataract surgery while 12 of 53 (17%) in the decompensated category had a history of transient double vision before the surgery. The causes were congenital fourth nerve palsies in 38% (20/53), esotropia in 17% (9/53), exotropia in 11% (6/53), hypertropia in 13% (7/53), and combined vertical and horizontal strabismus in 21% (11/53). Forty-six percent (32/70) were treated with prisms, 9% (6/70) had strabismus surgery, and 1 patient’s diplopia resolved after having cataract surgery in the fellow eye. Twenty percent (14/70) were able to fuse through their deviation and did not require prisms or surgery. Ocular causes of postoperative visual disturbances were numerous and heterogenous, as shown in Table 2. During the 9-year study period, there were 13,715 patients who underwent cataract surgery at our institution. Thirty-six of them were referred for neuro-ophthalmic evaluation for visual disturbance after cataract surgery (referral rate was 0.26% [36/13,715]), of which 20 patients had neuro-ophthalmic etiologies as a cause for their visual symptoms. The prevalence of neuro-ophthalmic disorders identified in this cohort was 0.15% (20/13,715). Seventeen of 20 patients developed double vision after cataract surgery, for an estimated prevalence of postoperative diplopia of 0.12% (17/13,715). DISCUSSION Cataracts account for a major proportion of visual disability around the world, and cataract surgery is the most commonly performed eye procedure worldwide (10). Expectations from cataract surgery are high, and patients expect significant visual improvement and uneventful recovery. Failure of visual improvement after cataract surgery can be quite distressing to the patient and the surgeon and may cast doubt on the surgeon’s expertise and motives. Overall, in our study we found a very low prevalence of neuroophthalmic disorders after uneventful cataract surgery (0.15%), although some serious pathologies were discovered, including compressive brain lesions. Diplopia from decompensated strabismus was the most common neuroophthalmic disorder in this cohort, followed by NAION. Diplopia can be a distressing adverse outcome after cataract surgery. It is important to note that over half of these patients did not have a history of double vision before cataract surgery. Although the incidence of strabismus in the general population is approximately 2.5%–4% (11), new-onset diplopia after cataract extraction is relatively 361 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution uncommon (0.17% and 0.75%) (4,12). In our cohort, the incidence of diplopia after cataract surgery was 0.12% (17/ 13,715). A retrospective case series by Nayak evaluating the etiologies of diplopia occurring after cataract surgery found that 34% were from decompensated strabismus, 25% from extraocular muscle restriction/paresis, with an overall estimated prevalence of 0.17% (150/87,500 cataract surgeries in the 70-month period of patient recruitment) (4). Other etiologies reported in other studies include postsurgical anisometropia, monovision, and concurrent onset of systemic disease (thyroid eye disease or vasculopathic cranial nerve palsy) (4,12). In myopic patients with pre-existing convergence insufficiency, the base-in prismatic effect of their glasses may have helped preoperatively when converging, masking an underlying convergence insufficiency (4). Pre-existing anisometropia, amblyopia, or strabismus can cause a change in ocular dominance or modification of the ocular deviation after surgery (4). This leads to modification of sensory adaptation, giving rise to symptoms that can range from asthenopia to diplopia (4). Keeping the anisometropia to small levels such as 1.25–1.50 diopters may lessen the chance of producing strabismus after monovision (13). Diplopia due to retrobulbar anesthesia may occur but is rare now due to topical cataract surgery (5). Eliciting a history of previous strabismus and examination TABLE 2. Other etiologies among 67 of 173 patients after cataract surgery Etiologies Number (%) Ocular 62 (93) Residual refractive error 6 (9) Anterior segment Dry eye/iritis 23 (34) IOL related Positive/negative dysphotopsia 9 (13) Tilted IOL 2 (3) Posterior capsular opacity 1 (1) Glaucoma 5 (7) Retinal disorders 13 (19) CRAO 1 Floaters/asteroid hyalosis 2 Macular edema (Irvine–Gass) 3 BRAO 1 Epiretinal membrane 3 Autoimmune retinopathy 1 PHPV 1 Foveal hypoplasia 1 Ptosis 3 (4) Others 5 (7) Inner ear disorders (vertigo and blurry vision) 1 (1) Orthostatic hypotension (transient visual loss) 1 (1) Functional visual loss 3 (4) BRAO, branch retinal artery occlusion; CRAO, central retinal artery occlusion; IOL, intraocular lens; PHPV, persistent hyperplastic primary vitreous. 362 to detect ocular misalignment preoperatively is recommended to ascertain the risk of developing postoperative diplopia. Notably, 12% (20/173) in our cohort were found to have likely pre-existing afferent pathway disorders that were diagnosed after cataract surgery, including compressive optic neuropathy and homonymous visual field defects from brain tumors, nutritional/toxic optic neuropathy, shock-induced optic neuropathy, and optic atrophy from other causes. Although patients with pre-existing neuro-ophthalmic disorders are likely to report persistent blurry vision after cataract surgery, it is often difficult to differentiate whether preoperative decrease in vision is from occult neuro-ophthalmic disease, cataract, or both. The presence of dyschromatopsia, APD, visual field defects, and vision loss out of proportion to the extent of the cataract may offer clues to the presence of an afferent neuro-ophthalmic disorder. Gerges et al (9) investigated the frequency of cataract surgery in patients with pituitary macroadenoma with chiasmal compression and found that the prevalence of cataracts was roughly the same as in those with macroadenoma compared with the age-adjusted general population (18% vs 17.2%). However, the prevalence of having cataract surgery was 2.5 times higher in patients with macroadenoma with chiasmal compression compared with the national average (12.5% vs 5.1%), suggesting that visual dysfunction from chiasmal compression may have been misinterpreted as being due to cataracts and treated with cataract surgery. Although 32% of these patients had no improvement in their vision after cataract surgery and 76% had visual improvement after transsphenoidal surgery, those patients with cataract were also less likely to recover their vision after transsphenoidal surgery alone. Addressing both pathologies is therefore important for optimizing the final visual outcome. In the 13 patients in our study with perioperative NAION, the event occurred 10 days to 5 months after cataract surgery, thereby making perioperative causes such as raised intraocular pressure (IOP) less likely in this cohort. Cataract surgery as a potential risk factor for development of NAION has been proposed by many authors (14,15) and a study also suggested that there was a 53% risk of a similar event if they underwent cataract surgery in the fellow eye (16). In a study evaluating incidence of ischemic optic neuropathy in 5,787 patients who underwent cataract surgery, 3 patients experienced ischemic optic neuropathy within 1 year of the cataract surgery with an estimated 6-month incidence of 51.8 in 100,000 cases (CI, 10.7–151). These rates are significantly higher than the previously reported incidence of NAION estimated to be 2.3–10.2 per 100,000 in the general population of people 50 years and older (17). The above studies include data from surgeries performed between 1986 and 2001 and include intracapsular, extracapsular, and phacoemulsification techniques with most patients receiving retrobulbar or peribulbar anesthesia. A recent study that Lin et al: J Neuro-Ophthalmol 2023; 43: 359-363 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution looked at prevalence and incidence of optic neuropathy after cataract surgery did not find a higher risk of NAION in their cohort of patients as compared to the general population (7). This has been reported by other studies that found a similar prevalence of NAION after cataract surgery compared with the general population, ranging from 2.8 to 10.9 cases per 100,000 procedures (7). It is possible that with evolving surgical techniques and the progression from larger scleral to smaller corneal incisions, the decrease in post-operative inflammation and surgical trauma potentially may decrease the risk of developing NAION after surgery although the precise mechanism continues to be debated (15). Our study has some limitations including the retrospective study design. Although the overall prevalence of neuro-ophthalmic disorders after cataract surgery is low, it is important to realize that the expectations of visual outcomes after surgery are high. Because postoperative diplopia from decompensated strabismus was the most commonly identified neuro-ophthalmic etiology, a history of strabismus, diplopia, or prism wear should be assessed before cataract surgery. Examination of ocular motility and alignment, which is an essential aspect of ophthalmic examination, could help identify patients with asymptomatic strabismus who are at risk for diplopia after cataract surgery. Informing these patients of pre-existing ocular misalignment before cataract surgery may help to mitigate anxiety if double vision does occur after surgery. Visual acuity loss out of proportion to the level of cataracts should prompt further testing including color vision testing, visual fields, and optical coherence tomography to identify a potential visual pathway disorder. STATEMENT OF AUTHORSHIP Conception and design: S.-C. Lin, A. Giang, G. T. Liu, R. A. Avery, K. S. Shindler, A. G. Hamedani, A. G. Ross, M. A. Tamhankar; Acquisition of data: S.-C. Lin, A. Giang, G. T. Liu, R. A. Avery, K. S. Shindler, A. G. Hamedani, A. G. Ross, M. A. Tamhankar; Analysis and interpretation of data: S.-C. Lin, A. Giang, G. T. Liu, R. A. Avery, K. S. Shindler, A. G. Hamedani, A. G. Ross, M. A. Tamhankar. Drafting the manuscript: S.-C. Lin, M. A. Tamhankar; Revising the manuscript for intellectual content: S.-C. Lin, G. T. Liu, R. A. Avery, K. S. Shindler, A. G. Hamedani, A. G. Ross, M. A. Tamhankar. Final approval of the completed manuscript: S.-C. Lin, A. Giang, G. T. Liu, R. A. Avery, K. S. Shindler, A. G. Hamedani, A. G. Ross, M. A. Tamhankar. Lin et al: J Neuro-Ophthalmol 2023; 43: 359-363 REFERENCES 1. Behndig A, Montan P, Stenevi U, Kugelberg M, Lundstrom M. One million cataract surgeries: Swedish national cataract register 1992-2009. J Cataract Refractive Surg. 2011;37:1539–1545. 2. Pellegrini M, Bernabei F, Schiavi C, Giannaccare G. Impact of cataract surgery on depression and cognitive function: systematic review and meta-analysis. Clin Exp Ophthalmol. 2020;48:593–601. 3. Samadi B, Lundstrom M, Kugelberg M. Improving patientassessed outcomes after cataract surgery. Eur J Ophthalmol. 2017;27:454–459. 4. 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