Interprofessional Electronic Consultations for the Diagnosis and Management of Neuro-Ophthalmic Conditions

Interprofessional electronic consultation (eConsult) is a telemedicine modality in which consulting providers review outside records and provide recommendations without in-person consultation. The purpose of this study was to describe the utilization of eConsults in the management of neuro-ophthalmic conditions.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Interprofessional Electronic Consultations for the Diagnosis and Management of Neuro-Ophthalmic Conditions Timothy T. Xu, MD, Felix F. Kung, MD, Kevin E. Lai, MD, Melissa W. Ko, MD, Michael C. Brodsky, MD, M. Tariq Bhatti, MD, John J. Chen, MD, PhD Background: Interprofessional electronic consultation (eConsult) is a telemedicine modality in which consulting providers review outside records and provide recommendations without in-person consultation. The purpose of this study was to describe the utilization of eConsults in the management of neuro-ophthalmic conditions. Methods: Retrospective cohort study of all patients who received an eConsult for a neuro-ophthalmic condition at a single quaternary referral center from 2018 to 2020. Main outcome measures included proportion of eConsults in which sufficient data were provided to the neuroophthalmologist to generate a definitive management decision, proportion of patients for whom an in-person neuroophthalmology evaluation was recommended, and the eConsult’s impact on patient care. Results: Eighty eConsults were conducted on 78 patients during the 3-year study period. Forty-eight (60.0%) subjects were female, mean age was 54 years, and 65 (81.3%) were White. The median time from eConsult request to completion was 4 days (range: 0–34 days). The most frequent eConsult questions were vision/visual field disturbances in 28 (35.0%) cases, optic neuropathies in 22 (27.5%), and optic disc edema in 17 (21.3%). At the time of eConsult, sufficient prior information was provided in 35 (43.8%) cases for the neuro-ophthalmologist to provide a definitive Department of Ophthalmology (TTX, FFK, MCB, MTB, JJC), Mayo Clinic, Rochester, Minnesota; Department of Neurology (MCB, MTB, JJC), Mayo Clinic, Rochester, Minnesota; Circle City NeuroOphthalmology (KEL), Carmel, Indiana; Neuro-Ophthalmology Section (KEL), Midwest Eye Institute, Carmel, Indiana; Ophthalmology Service (KEL), Richard L. Roudebush Veterans Administration Medical Center, Indianapolis, Indiana; Department of Ophthalmology (KEL, MWK), Indiana University School of Medicine, Indianapolis, Indiana; and Department of Neurology and Neurosurgery (MWK), Indiana University School of Medicine, Indianapolis, Indiana. The authors report no conflicts of interest. The contents of this manuscript were presented in part as a poster presentation at the North American Neuro-Ophthalmology Society 2022 Annual Meeting in Austin, TX. Address correspondence to John J. Chen, MD, PhD, Mayo Clinic, Departments of Ophthalmology and Neurology, 200 First Street Southwest Rochester, MN 55905 ; E-mail: [e-mail] 34 management decision. In 45 (56.3%) eConsults, further diagnostic testing was recommended. In-person neuroophthalmology consultation was recommended in 24 (30.0%) cases. Sixty-one (76.3%) eConsults provided diagnostic and/or treatment direction, and 12 (15.0%) provided reassurance. Conclusion: eConsults increase access to timely neuroophthalmic care and provide diagnostic and treatment direction to non–neuro-ophthalmology providers when sufficient information is provided at the time of eConsult. Journal of Neuro-Ophthalmology 2023;43:34–39 doi: 10.1097/WNO.0000000000001643 © 2022 by North American Neuro-Ophthalmology Society N euro-ophthalmology faces a workforce shortage, resulting in estimated waiting times of 6 weeks with 25% of patients waiting .3 months (1). Limited access to neuro-ophthalmologists contributes to suboptimal care and patient harm because of the time-sensitive nature of neuro-ophthalmic conditions (2). Telemedicine represents a promising avenue to supplement in-person neuroophthalmic care by increasing access to timely care, diagnostic consultations, and follow-up care (3). Ophthalmologists have become increasingly comfortable with delivering telemedicine-based care over the past decade, particularly in the setting of the COVID-19 pandemic (4,5). Interprofessional electronic consultation (eConsult) is a telemedicine modality in which consulting providers review medical records and provide management recommendations without in-person evaluation, including whether inperson consultation is warranted. At the North American Neuro-Ophthalmology Society 2021 Annual Meeting, 18.7% of polled participants reported performing eConsults during the pandemic, compared with 4.4% before the pandemic (6,7). It remains unclear how amenable neuroophthalmic diagnoses are to management through eConsults. The purpose of this study was to describe the Xu et al: J Neuro-Ophthalmol 2023; 43: 34-39 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution utilization of eConsults in the diagnosis and management of neuro-ophthalmic conditions. METHODS A retrospective review was conducted of all patients who received an eConsult for any neuro-ophthalmic condition at Mayo Clinic in Rochester, Minnesota, from January 1, 2018, to December 31, 2020. Mayo Clinic Rochester serves as a referral center not only for domestic and international patients but also for patients within the Mayo Clinic Health System in the upper Midwest United States. An eConsult was defined as an encounter in which non–neuro-ophthalmology providers (e.g., optometry, comprehensive ophthalmology, neurology, and neurosurgery) performed an inperson evaluation and then referred the patient to neuroophthalmology for remote evaluation of the patient’s medical record, laboratory testing, and imaging studies without an in-person evaluation. The neuro-ophthalmologist was expected to provide recommendations regarding diagnosis and management within 24 hours from when the eConsult was placed on their clinical calendar, including whether inperson neuro-ophthalmology consultation was warranted. All eConsults were performed by Rochester-based fellowship-trained neuro-ophthalmologists (M.C.B., M.T.B., and J.J.-W.C.). All eConsults were identified through individual review of each neuro-ophthalmologist’s clinical calendar. Patients who were evaluated through synchronous telephone or video encounters were excluded. This study was approved by the Mayo Clinic Institutional Review Board, complied with the Health Insurance Portability and Accountability Act, and adhered to the tenets of the Declaration of Helsinki. Data collected included the purpose of eConsult (e.g., diagnosis, testing, and/or treatment recommendations), time between eConsult referral date and completion date, patient’s home zip code, referring provider’s speciality, referring provider’s diagnosis, and neuro-ophthalmology’s recommendations. Data regarding neuro-ophthalmology’s recommendations included whether the diagnosis was determined at the time of eConsult, further testing (e.g., visual fields, fundus photography, imaging, and optical coherence tomography [OCT]) was recommended, or an in-person evaluation was requested. The eConsult questions were categorized into 6 categories based on the clinical question: optic neuropathies, optic disc edema, vision and visual field disturbances, diplopia/nystagmus/afferent/efferent pathologies, headache/eye pain, and orbital/intracranial masses. Followup data were assessed through March 1, 2021. Main outcome measures included the percentage of eConsults in which enough information was provided at the time of eConsult for a definitive diagnosis and/or treatment decision to be made, percentage of patients who were recommended in-person evaluation, and eConsult’s impact on patient care. The eConsult’s impact on patient care was retrospectively ascertained into 6 classifications adopted Xu et al: J Neuro-Ophthalmol 2023; 43: 34-39 from a previous study (2): negative (e.g., associated with poor patient outcome), no impact, provided reassurance (e.g., neuro-ophthalmologist agreed with referring provider’s assessment and plan, which avoided unnecessary testing and/or in-person evaluation), avoided harmful treatment or provided urgent referral to appropriate provider, and directly saved vision and/or life. Categorical variables were reported as frequency and percentage. Continuous variables were summarized using mean and SD. Variables were presented for all eConsults performed overall. Statistical analysis was conducted using Microsoft Excel 2010 (Microsoft Corporation; Redmond, WA). RESULTS During the 3-year study period, there were 80 eConsults performed on 78 patients. Seventeen (21.3%) eConsults were performed in 2018, 27 (33.8%) in 2019, and 36 (45.0%) in 2020. The mean age at the time of eConsult was 54 years. Female accounted for 48 (60.0%) subjects and 65 (81.3%) were White. The median time between eConsult request to completion of eConsult was 4 days (range: 0–34 days). Seventy-four (92.5%) eConsults were performed on domestic patients with a median distance of 63 miles (range: 4 to 1,432 miles) from the patient’s home to Mayo Clinic Rochester. Six (7.5%) were performed on international patients from 4 countries. Fifty-nine (73.8%) eConsults were requested from within Mayo Clinic Health System while 21 (26.3%) were from external facilities. The most frequent specialties of referring providers were optometry in 29 (36.3%) cases, comprehensive ophthalmology in 20 (25.0%), and neurology in 11 (13.8%). The eConsult diagnosis categories were vision/visual field disturbances in 28 (35.0%) cases, optic neuropathies in 22 (27.5%), optic disc edema in 17 (21.3%), headache/ eye pain in 7 (8.8%), orbital/intracranial masses in 4 (5.0%), and diplopia, nystagmus, and afferent/efferent pathologies in 1 (1.3%) (Table 1). The eConsult’s purpose was recommendations regarding diagnosis in 66 cases (82.5%), testing in 57 (71.3%), and treatment in 37 (46.3%). Compared with suspected diagnoses before eConsult, the number of final diagnoses ascertained through eConsult and/or subsequent in-person evaluation increased for optic neuropathies by 10 (45.5%) cases, decreased for optic disc edema by 7 (41.2%), vision/visual field disturbances by 13 (46.4%), and headache/eye pain by 1 (14.3%) and was the same for orbital/intracranial masses and diplopia/nystagmus/afferent/efferent pathologies. No pathology was identified after eConsult and further workup in 12 (15.0%) subjects. At the time of eConsult, sufficient information was provided to neuro-ophthalmology to formulate a definitive diagnostic and/or treatment decision without further testing recommendations in 35 (43.8%) cases. In 45 (56.3%) eConsults, further diagnostic testing was recommended 35 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Neuro-Ophthalmic Diagnoses Before and After eConsult Diagnosis Category Diagnosis Queried by eConsult Final Diagnosis Change No pathology identified Optic neuropathies Anterior ischemic optic neuropathy Chorioretinal scarring Compressive optic neuropathy Epiretinal membrane Glaucoma Leber hereditary optic neuropathy Myelin oligodendrocyte glycoprotein-IgG optic neuritis Neuromyelitis optica optic neuritis Neuroretinitis Optic nerve atrophy Optic disc drusen Optic nerve hypoplasia Optic neuritis (etiology unknown) Optic neuropathy (etiology unknown) Peripapillary atrophy Relative afferent pupillary defect Vitreopapillary traction optic neuropathy Optic disc edema Diabetic papillitis Idiopathic intracranial hypertension Optic disc edema Papilledema (secondary to congenital hydrocephalus) Papilledema (unknown etiology) Pseudopapilledema Vision and visual field disturbances Amblyopia Associative synesthesia Blurred/decreased vision Charles Bonnet syndrome Dry eye syndrome Illusory palinopsia Light-induced amaurosis Light-induced visual aura Refractive error Visual field defect (congenital) Visual field defect (etiology unknown) Vision disturbance (etiology unknown) Diplopia, nystagmus, and afferent/Efferent pathologies Binocular diplopia (unknown etiology) Headache and eye pain Acephalgic migraine Eye pain (unknown etiology) Giant cell arteritis Migraine headache Orbital/intracranial masses Benign orbital mass Metastatic orbital melanoma Ocular metastasis screening for cancer clinical trial with no metastatic lesions detected Optic pathway glioma — 22 7 0 1 0 1 1 0 1 1 1 2 1 2 3 0 1 0 17 0 4 7 0 6 0 28 0 1 3 1 0 0 0 1 0 1 13 8 1 1 7 0 4 1 2 4 1 0 2 12 32 9 1 0 1 5 1 2 1 2 3 2 1 0 2 1 0 1 10 1 5 0 1 0 3 15 1 1 0 1 1 1 1 0 1 1 2 5 1 1 6 2 1 0 3 4 0 1 2 [ [ [ [ Y [ [ 4 [ 4 [ [ 4 4 Y Y [ Y [ Y [ [ Y [ Y [ Y [ 4 Y 4 [ [ [ Y [ 4 Y Y 4 4 Y [ Y Y [ 4 Y [ 4 1 1 4 Arrows indicate a change in the diagnosis queried with the e-consult and the final diagnosis. after eConsult, including imaging (e.g., MRI of brain/orbits and positron emission tomography of brain) in 27 (33.8%), formal visual field testing (e.g., perimetry) in 26 (32.5%), 36 OCT in 16 (20.0%), laboratory testing (e.g., vitamin A, vitamin B12, thyroid stimulating hormone, and erythrocyte sedimentation rate) in 15 (18.8%), fundus photography in Xu et al: J Neuro-Ophthalmol 2023; 43: 34-39 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution 5 (6.3%), fluorescein angiography in 5 (6.3%), genetic testing in 2 (2.5%), and lumbar puncture in 1 (1.3%). Inperson consultation with other subspecialties, specifically neurosurgery, neurology, endocrinology, and vitreoretinal surgery was recommended in 5 (6.3%) cases. Among 35 (43.8%) subjects with the in-person follow-up with any eye care provider (e.g., ophthalmology or optometry) after eConsult, the median follow-up time from eConsult to last follow-up was 3.5 months (range: 6 days to 2.0 years). In 24 (30.0%) cases, in-person neuro-ophthalmology consultation was recommended. Of these 24 subjects, the most common referring providers were comprehensive ophthalmology in 12 (50.0%) cases and optometry in 6 (25.0%). Twelve (50%) subjects underwent in-person evaluation at a median time from eConsult of 2.1 months (range: 7 days to 4.4 months). The eConsult diagnosis was congruent with the in-person diagnosis in 10 (83.3%) cases. Two diagnoses were changed after in-person consultation; both were initially diagnosed with papilledema through eConsult and subsequently diagnosed with pseudopapilledema during in-person neuro-ophthalmology evaluation. The impact of the eConsult on patient care was ascertained to provide diagnostic and/or treatment direction in 60 (75.0%) cases, reassurance (e.g., avoided further testing/visits) in 12 (15.0%), no impact in 5 (6.3%), avoid harmful treatment and urgent referral in 2 (2.6%), and negative impact in 1 (1.3%) (Fig. 1). The 2 eConsults that avoided harmful treatment and urgent referral involved 2 patients referred for papilledema and subsequently diagnosed with pseudopapilledema. In one case referred by neurosurgery, OCT was not obtained before eConsult, which demonstrated optic nerve drusen when evaluated in-person. In the other case, the diagnosis of papilledema in a pediatric patient was unclear based on fundus photographs and OCT; B-scan ultrasonography during in-person evaluation demonstrated optic nerve drusen. The sole eConsult deemed to have a negative impact involved a middle-aged male referred by neurosurgery for consideration of orbital biopsy for an incidentally identified medial orbital mass, which was believed to be a benign cavernous hemangioma. Observation with repeat imaging in 6 months was recommended without in-person evaluation or biopsy because the patient was asymptomatic and had a normal eye examination 5 months before eConsult. The patient was lost to follow-up until 1 year later, when at that time the lesion had grown and was subsequently found to be a malignant orbital melanoma that was managed through exenteration and systemic chemoradiation. CONCLUSIONS Telemedicine is an increasingly used modality of health care delivery in neuro-ophthalmology (8). In this retrospective cohort study of 80 neuro-ophthalmology eConsults, the most frequent eConsult questions were vision/visual field Xu et al: J Neuro-Ophthalmol 2023; 43: 34-39 FIG. 1. Impact of neuro-ophthalmology eConsult on patient care (classifications adapted from previous study) (7). disturbances, optic neuropathies, and optic disc edema. Most eConsults were completed within 1 week and positively affected patient care by providing diagnosis and/or treatment direction to referring providers. Nearly half of eConsults provided sufficient prior information for consulting neuro-ophthalmologists to provide definitive management decisions, and one-third of subjects were recommended to undergo in-person neuro-ophthalmology evaluation. These findings highlight the utility of eConsults for triaging patients requiring in-person evaluation, increasing timely access to neuro-ophthalmic care, and providing diagnostic and treatment direction to non–neuro-ophthalmology providers when sufficient information was provided at the time of eConsult. Few studies have assessed outcomes of neuro-ophthalmic diagnoses managed through telemedicine. In a survey of neuro-ophthalmologists who use synchronous video visits, conditions considered amenable to telemedicine management included migraine with aura, pituitary tumor with prior visual field testing, and analysis of MRI results, while ischemic optic neuropathy and optic atrophy were difficult to evaluate through telemedicine alone (7). In 133 patients referred for blurred optic discs, Jefferis et al compared the reliability of diagnoses in a simulated virtual clinic with inperson diagnoses and found that neuro-ophthalmologists accurately identified all potential papilledema cases that required in-person evaluation (9). In this study, eConsults were effective at assisting in the management of vision/ visual field disturbances, optic neuropathies, optic disc edema, and orbital/intracranial masses when appropriate testing was provided, such as formal visual field testing 37 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution and OCT. Few patients in this study were referred for diplopia, nystagmus, headaches, and eye pain, which may reflect that referring providers prefer these complaints to be evaluated in-person and/or require emergency evaluation. To maximize the value of eConsults, it is important to have the pertinent information available for review at the time of eConsult. If the clinical question involves vision/ visual field disturbances, optic neuropathies, and optic disc edema, we recommend fundus photography, OCT of the peripapillary retinal nerve fiber layer and macular ganglion cell layer, and formal visual field testing at a minimum before eConsult. For orbital/intracranial masses, neuroimaging is important, ideally MRI brain/orbit with and without contrast reviewed by neuroradiology, along with visual fields and OCT. For diplopia and nystagmus pathologies, motility examination and strabismus measurements should be included in pre-eConsult evaluation. For eye pain or headache etiologies, complete eye examination is required and neuroimaging is often necessary. We do not endorse the use of eConsults for acute etiologies of eye pain or headaches, such as giant cell arteritis, rather in-person or emergency evaluation should be pursued. Workup targeted toward suspected diagnoses is preferable (e.g., MRI brain, MR venography, and lumbar puncture if suspecting idiopathic intracranial hypertension); however, we acknowledge that the purpose of the eConsult is oftentimes for further testing recommendations. We also recognize that pre-Consult workup may vary based on referring providers’ familiarity with neuro-ophthalmic workup; for example, non-eye care providers might be less likely to order eye-specific testing such as OCT. Although most patients in this study (75%) were referred by comprehensive ophthalmology or optometry, we were unable to assess whether eConsults from certain referring specialties were associated with higher in-person consultation rates because of our limited sample size. An advantage of eConsults is rapid access to neuroophthalmology consultation, particularly for patients and providers residing in rural areas who may lack access to local neuro-ophthalmology providers. Although patients may be unable to see a neuro-ophthalmologist in-person for months, referring providers may obtain recommendations through eConsult within days. Recent investigations of standard neuro-ophthalmology referral patterns revealed wait times of approximately 7 months from symptom onset to neuro-ophthalmology consultation and .1 month from referral to neuro-ophthalmology consultation (2,10). By contrast, the median time from eConsult request to completion was 4 days in this study. Early input from neuroophthalmology providers is imperative because most patient harm in neuro-ophthalmology is due to misdiagnoses by referring providers which could have been prevented with earlier neuro-ophthalmic evaluation (2). Barriers of telemedicine in neuro-ophthalmology include reimbursement, data quality, and legal considerations (7). Before the COVID-19 pandemic, the United States 38 insurers did not reimburse several forms of telemedicine (11); eConsult-related reimbursement was not implemented by the Centers for Medicare and Medicaid Services until 2019 (12). Furthermore, conditions requiring visualization and monitoring of the optic disc may be difficult to manage remotely because examination and testing can typically only be performed reliably in-person (7). However, digital health technologies such as tablet-based measurement of visual fields are rapidly being developed and improving with respect to data quality (13,14). Finally, it is important to note that because eConsults do not involve face-to-face patient care, it remains unclear whether eConsults represent establishment of a patient-provider relationship and whether the referring and/or consulting provider bears legal responsibilities for eConsult recommendations (15,16). An important consideration is whether quality of care delivered through telemedicine is comparable with that of inperson care. In this study, most eConsults provided diagnostic and/or treatment guidance, and 2 eConsults were ascertained to help avoid unnecessary testing and/or treatment. The case with a negative outcome was a patient referred for consideration of orbital biopsy for an incidentally identified medial orbital mass on MRI, which was reviewed by neuroradiology and believed to represent a benign cavernous hemangioma. The eConsult recommendation was observation with serial imaging. The patient was lost to follow-up until 1 year later when he was diagnosed with malignant orbital melanoma. Due to this study’s retrospective design, it was unclear whether the diagnosis would have been detected had the patient been evaluated in-person. It is unlikely that management and outcome would have changed because he was asymptomatic and had a normal eye examination 5 months earlier. More studies that prospectively assign patients to tele– neuro-ophthalmology modalities vs in-person evaluation are needed to assess telemedicine’s quality of care. Limitations of this study included its retrospective design, which contributed to incomplete data collection and loss of follow-up. If further testing was performed at external facilities after eConsult, we might not have had access to the results. If patients were recommended inperson evaluation, they may have sought care with external neuro-ophthalmologists for whom we did not have access to the medical records, particularly because 26% of eConsults were from outside Mayo Clinic. Our findings may have also been limited by referral bias. Because Mayo Clinic is a referral center, these cases could have been skewed toward greater complexity, potentially inflating the proportion of cases recommended to receive in-person care. However, neuro-ophthalmologists tend to practice at larger academic centers; therefore, these cases may reflect the diagnostic complexity that other neuro-ophthalmologists encounter. Finally, our results were largely dependent on the experience of 3 neuro-ophthalmologists. Given varying comfort levels with telemedicine, providers might be less comfortable with evaluating patients without in-person evaluation. Xu et al: J Neuro-Ophthalmol 2023; 43: 34-39 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Nonetheless, most neuro-ophthalmologists incorporated some form of telemedicine into their practice in light of the COVID-19 pandemic (4). In summary, these findings demonstrate the utility of eConsults in triaging patients requiring in-person neuroophthalmology evaluation, increasing access to neuroophthalmic care, and providing diagnosis and treatment direction to non–neuro-ophthalmology providers. eConsults most frequently evaluated vision/visual field disturbances, optic neuropathies, and optic disc edema. Neuroophthalmologists provided definitive management decisions at the time of eConsult in nearly half the cases. Before eConsults, referring providers should ideally obtain pertinent testing to maximize the value and efficiency of the eConsult. Future studies should investigate clinical outcomes of neuro-ophthalmic disorders managed through telemedicine versus conventional care and identify sources of telemedicine-related diagnostic errors. 5. 6. 7. 8. 9. 10. 11. STATEMENT OF AUTHORSHIP Conception and design: T. T. Xu, J. J. Chen; Acquisition of data: T. T. Xu, F. F. Kung, J. J. Chen; Analysis and interpretation of data: T. T. Xu, F. F. Kung, K. E. Lai, M. W. Ko, M. C. Brodsky, M. T. Bhatti, J. J. Chen; Drafting the manuscript: T. T. Xu, J. J. Chen; Revising the manuscript for intellectual content: T. T. Xu, F. F. Kung, K. E. Lai, M. W. Ko, M. C. Brodsky, M. T. Bhatti, J. J. Chen; Final approval of the completed manuscript: T. T. Xu, F. F. Kung, K. E. Lai, M. W. Ko, M. C. Brodsky, M. T. Bhatti, J. J. Chen. 12. 13. REFERENCES 1. DeBusk A, Subramanian PS, Scannell Bryan M, Moster ML, Calvert PC, Frohman LP. Mismatch in supply and demand for neuro-ophthalmic care. J Neuroophthalmol. 2022;62:67. 2. 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