The Impact of COVID-19 on Neuro-Ophthalmology Office Visits and Adoption of Telemedicine Services

Background: The COVID-19 public health emergency (PHE) has significantly changed medical practice in the United States, including an increase in the utilization of telemedicine. Here, we characterize change in neuro-ophthalmic care delivery during the early COVID-19 PHE, including a comparison of care delivered via telemedicine and in office. Methods: Neuro-ophthalmology outpatient encounters from 3 practices in the United States (4 providers) were studied during the early COVID-19 PHE (March 15, 2020-June 15, 2020) and during the same dates 1 year prior. For unique patient visits, patient demographics, visit types, visit format, and diagnosis were compared between years and between synchronous telehealth and in-office formats for 2020. Results: There were 1,276 encounters for 1,167 patients. There were 30% fewer unique patient visits in 2020 vs 2019 (477 vs 670) and 55% fewer in-office visits (299 vs 670). Compared with 2019, encounters in 2020 were more likely to be established, to occur via telemedicine and to relate to an efferent diagnosis. In 2020, synchronous telehealth visits were more likely to be established compared with in-office encounters. Conclusions: In the practices studied, a lower volume of neuro-ophthalmic care was delivered during the early COVID-19 public health emergency than in the same period in 2019. The type of care shifted toward established patients with efferent diagnoses and the modality of care shifted toward telemedicine.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD The Impact of COVID-19 on Neuro-Ophthalmology Office Visits and Adoption of Telemedicine Services Heather E. Moss, MD, PhD, Melissa W. Ko, MD, Devin D. Mackay, MD, Divya Chauhan, MD, Karen G. Gutierrez, BS, Natacha C. Villegas, MD, Kevin E. Lai, MD Background: The COVID-19 public health emergency (PHE) has significantly changed medical practice in the United States, including an increase in the utilization of telemedicine. Here, we characterize change in neuroophthalmic care delivery during the early COVID-19 PHE, including a comparison of care delivered via telemedicine and in office. Methods: Neuro-ophthalmology outpatient encounters from 3 practices in the United States (4 providers) were studied during the early COVID-19 PHE (March 15, 2020–June 15, 2020) and during the same dates 1 year prior. For unique patient visits, patient demographics, visit types, visit format, and diagnosis were compared between years and between synchronous telehealth and in-office formats for 2020. Results: There were 1,276 encounters for 1,167 patients. There were 30% fewer unique patient visits in 2020 vs 2019 (477 vs 670) and 55% fewer in-office visits (299 vs 670). Compared with 2019, encounters in 2020 were more likely to be established, to occur via telemedicine and to relate to an efferent diagnosis. In 2020, synchronous telehealth visits were more likely to be established compared with in-office encounters. Conclusions: In the practices studied, a lower volume of neuro-ophthalmic care was delivered during the early COVIDDepartments of Ophthalmology (HEM, KGG, NCV) and Neurology & Neurological Sciences (HEM), Stanford University, Palo Alto, California; Departments of Neurology (MWK, DDM, DC), Neurosurgery (MWK, DDM), and Ophthalmology (MWK, DDM, KEL), Indiana University School of Medicine, Indianapolis, Indiana; Ophthalmology Service (KEL), Richard L. Roudebush Veterans Administration Medical Center, Indianapolis, Indiana; and NeuroOphthalmology Section (KEL), Midwest Eye Institute, Carmel, Indiana. Research to Prevent Blindness unrestricted grant to the Stanford Department of Ophthalmology, and NIH P30 086277. 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). H. E. Moss and M. W. Ko authors contributed equally to this article. Address correspondence to Kevin E. Lai, MD, Midwest Eye Institute, 10300 N. Illinois Street, Suite 1000, Carmel, IN 46290; E-mail: kevin.e. [e-mail] 362 19 public health emergency than in the same period in 2019. The type of care shifted toward established patients with efferent diagnoses and the modality of care shifted toward telemedicine. Journal of Neuro-Ophthalmology 2021;41:362–367 doi: 10.1097/WNO.0000000000001356 © 2021 by North American Neuro-Ophthalmology Society T he COVID-19 pandemic indelibly altered medical practice worldwide. In order to maintain access to care for high-risk patients and decrease the risk of exposure to the severe acute respiratory syndrome coronavirus 2 virus, telemedicine, previously reserved for limited populations, was broadly adopted to meet these demands (1–3). Neuro-ophthalmologists, like many specialties, had to rapidly develop new protocols, consider what conditions may be appropriate for telemedicine, and determine which cases warranted an in-person visit with associated increased risks in order to continue delivery of care (4,5). In a survey of neuro-ophthalmologists in active independent practice, the COVID-19 public health emergency (PHE) was associated with a significant global increase in the adoption of video and other telemedicine services for neuro-ophthalmic care despite barriers of data quality and infrastructure. A majority of users indicated that video visits were most helpful for efferent problems and afferent problems with prior ancillary testing (6). Other reviews have noted an important role of synchronous telemedicine for patient triage (7). However, data on patient volumes in neuro-ophthalmology has not been reported in these and other studies, so the impact on patient care has not been assessed. The primary purpose of this study was to evaluate the impact of COVID-19 on outpatient neuro-ophthalmic care by comparing clinical visits in 3 practices (4 practitioners) during the early PHE with a control period from the same time in 2019. A secondary purpose was to compare telemedicine and in-person visits during the PHE. Moss et al: J Neuro-Ophthalmol 2021; 41: 362-367 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution METHODS A multicenter, retrospective, chart review was performed on all neuro-ophthalmology outpatient encounters by 4 providers at 3 institutions, 1 private practice (Circle City NeuroOphthalmology at Midwest Eye Institute) and 2 academic centers (Indiana University and Stanford University), between March 15, 2020, and June 15, 2020. This date range was selected to capture the first 3 months of the COVID-19 PHE in the United States. Outpatient encounters for 3 of the providers between March 15, 2019, and June 15, 2019, were used as a comparison. Inclusion criteria for encounters were completed visits with a participating neuro-ophthalmologist for a neuro-ophthalmic appointment during 1 of the 2 periods. Exclusion criteria were general ophthalmology, general neurology, or surgical (preoperative or postoperative) visits. The study was deemed exempt by the Indiana University Institutional Review Board and was approved with waiver of informed consent by the Stanford research compliance office. Data were extracted at the encounter level. Encounter variables included site, year (2019, 2020), visit type (new, return, research study), visit format (in-office, synchronous video and audio, synchronous audio only, interprofessional consult), visit number for a given patient in a given year, and primary diagnosis International Classification of Diseases Tenth Edition code that was classified as afferent, efferent, or other. Patient variables either extracted from or calculated based on the medical record included age at time of visit (difference between encounter date and birth date), gender, type of insurance (Medicare, Medicaid/Other Government, Commercial, Self-Pay), and distance from the patient’s address to the examining provider’s clinic address calculated using the shortest driving distance on Google maps. Each site collected data separately. Deidentified data was merged for analysis. Statistical Analysis Data analysis considered first encounters for each patient during each period studied. Subsequent encounters were excluded from analysis. The primary comparison was between 2019 and 2020 encounters. Encounter and patient variables were compared using a chi-squared test for categorical variables, t test for independent samples for continuous normally distributed variables and Mann–Whitney U test for continuous variables with skewed distributions. The secondary comparison was between 2020 synchronous telemedicine encounters (video + audio, audio only) and in-office visits. Similar to the primary analysis, only first visits for each patient were included. Statistical comparisons were performed as for the primary comparison. Statistical analysis was performed using SPSS V26 (IBM Inc). RESULTS One thousand two hundred seventy-six encounters for 1,167 patients were extracted. They were approximately Moss et al: J Neuro-Ophthalmol 2021; 41: 362-367 evenly divided between Indiana-private practice, Indianaacademic, and California-academic (n = 357, 457, 462 respectively). Among first visits during the study periods, 741 were new patient encounters, 422 were established patient encounters, and 4 were study visits. Nine hundred sixty nine (83%) of visits were in-office, 179 (15.3%) were synchronous video + audio, 15 (1.3%) were synchronous audio only, and 4 (0.3%) were asynchronous interprofessional consults. Visit diagnoses were afferent for 722 (62%) of first encounters, efferent for 267 (22.9%), and other for 176 (15.1%). The most common diagnoses seen were papilledema/pseudotumor cerebri (174, 13.6%), diplopia (122, 9.56%), and visual field defect (121, 9.48%). Diagnosis was missing for 2 encounters. Unique patients ranged in age from 2 to 95 years old, were 64.5% female, and lived 1 to 2,968 miles from the outpatient clinic. The majority of patients had commercial insurance (50.9%), whereas 28.2% had Medicare, 18.6% had other government insurance (Medicaid or Veterans’ Affairs), and 2.2% were self-pay. Residential address could not be obtained for 53 patients. Insurance status was missing for 5 patients. 2019 vs 2020 Six hundred eighty-two encounters occurred for 670 patients between March 15, 2019, and June 15, 2019, and 594 encounters occurred for 497 patients between March 15, 2020, and June 15, 2020. The proportion of unique patient visits did not differ across sites, with all sites seeing fewer visits in 2020 vs 2019 (P = 0.12, chi-square). Although 2020 saw a shift in encounter distributions, the majority of visits remained in office and for afferent diagnoses. Compared with those in 2019, unique patient encounters in 2020 were more likely to be established, to occur via telemedicine, and to relate to an efferent diagnosis (Table 1). A 2019 to 2020 comparison stratified by site is provided in the supplemental data (See Supplemental Digital Content, Tables E1–E3, http://links.lww.com/WNO/A490). In 2019, the most common diagnoses seen in new patients were visual field defects, other, diplopia, papilledema, optic atrophy, and subjective visual disturbances; in 2020, the most common diagnoses seen in new patients were diplopia, visual field defects, subjective visual disturbances, papilledema, and sudden vision loss (Fig. 1). In both 2019 and 2020, papilledema/ pseudotumor cerebri was the most commonly seen diagnosis (Table 2). 2020 Office vs 2020 Telehealth Between March 15, 2020, and June 15, 2020 (early COVID-19 PHE), unique patients had 299 in-office visits and 194 synchronous telehealth visits in the practices studied. Synchronous telehealth visits were less likely to be new patient encounters (Table 3). A 2020 in-office vs 363 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Comparison between unique patient encounters between 2019 and 2020 (March 15–June 15) Age in years (mean ± SD) Female gender (n (%)) Distance in miles (median, range) Insurance Medicare Commercial Other government Self-pay Visit type New Established Study Visit format In office Video + audio Audio only Interprofessional Diagnosis Afferent Efferent Other 2019 (n=670) 2020 (n=467) 51.3 ± 18.9 443 (66.1%) 35 (1.2–2,968) 50.2 ± 18.9 310 (62.4%) 28.5 (1–461) 193 (29.0%) 330 (49.6%) 130 (18.5%) 12 (1.8%) 135 (27.2%) 262 (52.7%) 86 (17.3%) 14 (2.8%) 445 (60.1%) 221 (33.0%) 4 (0.6%) 201 (47.6%) 296 (59.6%) 0 (0%) 670 (100%) 0 0 0 299 (60.2%) 179 (36.0%) 15 (3.0%) 4 (0.8%) 417 (62.3%) 137 (20.5%) 115 (17.2%) 305 (61.5%) 130 (26.2%) 61 (12.3%) P 0.32 0.19 0.06 0.40 (t test) (CS) (MW) (CS) 0.009 (CS) ,0.0005 (CS) 0.01 (CS) CS, Chi-squared test; MW, Mann–Whitney U test. telehealth comparison stratified by site is provided in supplemental data (See Supplemental Digital Content, Tables E4–E6, http://links.lww.com/WNO/A490). CONCLUSIONS This study builds on a survey of telemedicine adoption by neuro-ophthalmologists during the COVID-19 PHE (6) and multiple expert commentaries of application of telemedicine to deliver neuro-ophthalmic care (4,5,7–10) by quantifying the amount and type of care provided by a convenience sample of neuro-ophthalmologists during this unprecedented time. This study also contributes to the broader literature on medical care during the COVID-19 PHE. Strengths of the study are the inclusion of all patients seen by the included providers, inclusion of academic and nonacademic practices in multiple states, and comparison with a control period 1 year prior. Approximately 30% fewer unique patients were seen in the early COVID period studied in 2020 than in 2019 with 55% fewer in-office visits. This is despite 1 of the providers only contributing patients to the 2020 sample and less work and personal travel by all the providers in 2020 compared with 2019. This aligns with what has been reported in the United States across medical specialties with drop-off in all visits and in-person visits during the early COVID-19 PHE (11). Many factors may have contributed to this decrease, including changes to supply factors (offices closed, decreased staff, social distancing, policy limiting scheduling to urgent visits, efforts to preserve personal protective equipment, increased home commitments of providers) and demand FIG. 1. Number of patients with common neuro-ophthalmic diagnoses seen pre-COVID (March 15, 2019–June 15, 2019) and early-COVID (March 15, 2020–June 15, 2020) according to visit type (new, established). 364 Moss et al: J Neuro-Ophthalmol 2021; 41: 362-367 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 2. Most common diagnoses in pre-COVID (March 15–June 15, 2019) and early-COVID (March 15–June 15, 2020) periods according to visit type 2019 2020 New Established Visual field defect Other Diplopia Papilledema/pseudotumor cerebri Optic atrophy Diplopia Visual field defect Subjective visual disturbances Papilledema/pseudotumor cerebri Sudden vision loss Papilledema/pseudotumor cerebri Optic atrophy Optic neuropathy not otherwise specified factors (decreased referrals, patient voluntary deferral, office-recommended deferral). Differences in early COVID 2020 patient visits when compared with 2019 included an increase in the proportion of established patient visits, increase in the proportion of efferent diagnoses, and decrease in the proportion of other (nonafferent and nonefferent) diagnoses. The most commonly seen diagnoses also changed for new consults between 2019 and 2020, suggesting a shift away from less urgent conditions (visual field defect, other, optic atrophy) toward more urgently perceived conditions (diplopia, papilledema, sudden vision loss) during the PHE. The increase in utilization of telehealth modalities was particularly striking as telemedicine modalities were not utilized by any of the 3 sites in 2019. This adoption was enabled by a combination of institutional technological support at the 2 academic institutions, changes in regulation and reimbursement, and increased interest by providers and patients to accommodate lockdown measures during the COVID-19 PHE. Similar changes in the modality and volume of care Papilledema/pseudotumor cerebri Optic neuritis/papillitis Optic atrophy Diplopia were observed in primary care. A comparison from the second calendar quarters of 2018 and 2019 to the second calendar quarter of 2020 in primary care showed a 21.4% decrease in the total number of primary care health care encounters. Office-based visits decreased by 50.2% in quarter 2 of 2020 compared with the same quarter in 2018 and 2019. 1.1% of visits were based on telemedicine in 2018 and 2019, compared with 35.3% in the second quarter of 2020 (12). Prepandemic, telemedicine adoption within neurology was well established for some neurological subspecialties, including stroke (13), but in ophthalmology, it was limited to remote review of images (14). The COVID-19 pandemic led to rapid, near-universal adoption in many medical disciplines with neurology being a leader and ophthalmology having low uptake (15). Neuro-ophthalmology straddles the 2 fields, sharing telemedicine benefits with neurology, including thorough history, external examination, and record review, but also suffering the drawbacks of the inability to perform an ophthalmoscopic examination that has TABLE 3. Comparison between unique patient encounters from March 15, 2020 to June 15, 2020 according to visit format Age in years (mean ± SD) Gender (female) Insurance Medicare Commercial Other government Self-pay Distance in miles, median (range) Visit type (new) Diagnosis Afferent Efferent Other In-Office Visit (n = 299) Synchronous Telehealth Visit (n = 194) 49.7 ± 18.9 189 (63.2%) 51.0±18.3 119 (61.3%) 78 (26.1%) 164 (54.8%) 50 (16.7%) 7 (2.3%) 29.6 (1.1–234) 197 (65.9%) 56 (28.9%) 95 (49.0%) 36 (18.6%) 7 (3.6%) 26.2 (1.0–461) 95 (49.0%) 191 (64.1%) 71 (23.8%) 36 (12.1%) 110 (56.7%) 59 (30.4%) 25 (12.9%) P 0.46 (t test) 0.68 (CS) 0.57 (CS) 0.84 (MW) ,0.0005 (CS) 0.219 (CS) CS, Chi-squared test; MW, Mann–Whitney U test. Moss et al: J Neuro-Ophthalmol 2021; 41: 362-367 365 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution limited uptake of telemedicine in ophthalmology beyond neuro-ophthalmology, oculoplastics, and pediatric ophthalmology (16). Although the majority of unique patient encounters were delivered via in-office care during early COVID-19 PHE in 2020, almost 40% were delivered via telemedicine. Consistent with opinion surveys of the suitability of telehealth visits for neuro-ophthalmic disorders, patients with efferent conditions were more likely to be seen via telemedicine, whereas patients with afferent conditions were less likely to be seen via telemedicine, although this difference did not reach statistical significance. However, the majority of telemedicine patient encounters were for afferent diagnoses, reinforcing the role of telemedicine for check-in and triage during the pandemic (7). New visit encounters, which formed the majority of neuro-ophthalmic encounters in 2019 and 2020, were less likely to occur via telemedicine. This may reflect new referrals during the PHE being for urgent matters and triaged to in-person and both patient and provider discomfort with telemedicine as a format for the initial encounter. Anecdotally, the authors feel that telemedicine formats enabled them to increase access to care beyond what would have been possible in 2020 due to governmental and institutional restrictions. The benefit of increasing patient access to care offered by the telemedicine format suggests a potential role for addressing the demand–supply mismatch for neuro-ophthalmology outside of a pandemic (17–21). This is particularly relevant as the negative outcomes to delayed neuro-ophthalmic care are becoming quantified (22). There are some limitations to this study. Although the sample size of visits is large, the number of practices studied (4 practitioners in 3 settings) is small with only 2 geographic regions considered. The use of primary diagnosis as the reason for visit does not capture subtleties of each patient’s presentation and the type of care provided. One provider did not see patients at any of the study sites in 2019 and therefore only contributed patients in 2020. In conclusion, medical care is just one of many services that changed dramatically during the COVID-19 PHE. In this study, we demonstrate the overall reduction in neuroophthalmic care delivered during the early COVID-19 PHE, with a shift from new consults to established visits compared with the same period 1 year prior. Adoption of telemedicine modalities shifted some care away from inoffice settings in 2019, although the majority of neuroophthalmology care was still provided in office. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: K. E. Lai, H. E. Moss, and M. W. Ko; b. Acquisition of data: K. E. Lai, D. Chauhan, K. G. Gutierrez, and N. C. Villegas; c. Analysis and interpretation of data: H. E. Moss and K. E. Lai. Category 2: a. Drafting the manuscript: K. E. Lai, H. E. Moss, M. W. Ko, and D. D. Mackay; b. Revising it for intellectual content: H. E. Moss, M. W. Ko, D. D. Mackay, and K. E. Lai. Category 366 3: a. Final approval of the completed manuscript: H. E. Moss, M. W. Ko, D. D. Mackay, and K. E. Lai. REFERENCES 1. Mann DM, Chen J, Chunara R, Testa PA, Nov O. COVID-19 transforms health care through telemedicine: evidence from the field. J Am Med Inform Assoc. 2020;27:1132–1135. 2. Wosik J, Fudim M, Cameron B, Gellad ZF, Cho A, Phinney D, Curtis S, Roman M, Poon EG, Ferranti J, Katz JN, Tcheng J. Telehealth transformation: COVID-19 and the rise of virtual care. J Am Med Inform Assoc. 2020;27:957–962. 3. Kanamori H, Weber DJ, Rutala WA. 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