Nonmydriatic Retinal Photography in the Outpatient Neurology Resident Clinic

Background: The funduscopic examination is an essential component of the neurologic examination. However, examination of the ocular fundus with a direct ophthalmoscope is often difficult. Nonmydriatic ocular fundus photography allows direct visualization of the ocular fundus with high-quality photographs. We used nonmydriatic ocular fundus photography to improve patient care and funduscopy skills of residents in the Neurology Resident Clinic. Methods: At the time of triage, funduscopic photographs of all new neurology resident clinic patients were taken. The images were imported into the hospital's imaging software. The residents completed a full neurologic examination, including a funduscopic examination with a handheld ophthalmoscope. At the time of staffing the patients with the attendings, the residents received immediate feedback and teaching on retina photograph evaluation. Results: A total of 255 patients were enrolled. Of those, 230 (90%) had at least one high-quality funduscopic photograph. Retinal photographs were normal in 161 (70%). Out of the 69 abnormal photographs, only 7% of abnormalities were detected by the residents. Ninety-three percent of residents found the retinal photographs useful. Conclusions: Nonmydriatic ocular fundus photography improved the care in patients presenting to a Neurology resident clinic and facilitated residents in recognizing funduscopic findings. Its benefits are clear when one considers (1) the high risk of negative patient outcomes and possible medicolegal consequences due to missed findings, (2) the ease of incorporating retinal photographs into the patients' medical records, and (3) the benefit of improving resident education in regard to the ophthalmologic examination.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Nonmydriatic Retinal Photography in the Outpatient Neurology Resident Clinic Nataliya Pyatka, MD, Matthew K. Banks, DO, Neel Fotedar, MD, Sarah J. DeLozier, PhD, Michael Morgan, MD, PhD, David C. Preston, MD Background: The funduscopic examination is an essential component of the neurologic examination. However, examination of the ocular fundus with a direct ophthalmoscope is often difficult. Nonmydriatic ocular fundus photography allows direct visualization of the ocular fundus with highquality photographs. We used nonmydriatic ocular fundus photography to improve patient care and funduscopy skills of residents in the Neurology Resident Clinic. Methods: At the time of triage, funduscopic photographs of all new neurology resident clinic patients were taken. The images were imported into the hospital’s imaging software. The residents completed a full neurologic examination, including a funduscopic examination with a handheld ophthalmoscope. At the time of staffing the patients with the attendings, the residents received immediate feedback and teaching on retina photograph evaluation. Results: A total of 255 patients were enrolled. Of those, 230 (90%) had at least one high-quality funduscopic photograph. Retinal photographs were normal in 161 (70%). Out of the 69 abnormal photographs, only 7% of abnormalities were detected by the residents. Ninety-three percent of residents found the retinal photographs useful. Conclusions: Nonmydriatic ocular fundus photography improved the care in patients presenting to a Neurology resident clinic and facilitated residents in recognizing funduscopic findings. Its benefits are clear when one considers (1) the high risk of negative patient outcomes and possible medicolegal consequences due to missed findings, (2) the ease of incorporating retinal photographs into the patients’ medical records, and (3) the benefit of improving resident education in regard to the ophthalmologic examination. Journal of Neuro-Ophthalmology 2022;42:68–72 doi: 10.1097/WNO.0000000000001236 © 2021 by North American Neuro-Ophthalmology Society Neurology Department, University Hospitals Cleveland Medical Center, Cleveland, Ohio. This work was published in part as an abstract at the American Academy of Neurology meeting, in Philadelphia, PA in May 2019. The authors report no conflicts of interest. Address correspondence to Nataliya Pyatka, MD, Neurological Institute, University Hospitals Cleveland Medical Center, 11100 Euclid Avenue, Cleveland, OH 44106; E-mail: [e-mail] 68 T he funduscopic examination is an essential component of the neurologic examination (1). Recognition of certain retinal abnormalities is crucial because they often reflect underlying vision-threatening or life-threatening neurologic conditions (2). For example, papilledema in a headache patient or retinal arterial emboli in a stroke patient may markedly change patient management (3). In Neurology Residency training, the Accreditation Council for Graduate Medical Education (ACGME) includes among its milestones the expectation that residents can competently perform the funduscopic examination and detect abnormal findings, including papilledema (4). The Center for Medicare & Medicaid Services (CMS) requires documentation of the funduscopic examination in all moderate- and highcomplexity new patient evaluations (5). However, examination of the ocular fundus with a direct ophthalmoscope is often difficult, even for a skilled neurologist (6,7). Many residents are not proficient at reliably performing a funduscopic examination (8). In addition, not having direct and simultaneous confirmation of the trainee’s findings with the attending’s assessment is an inherent limitation of learning direct ophthalmoscopy (6). Nonmydriatic ocular fundus photography allows direct visualization of the ocular fundus with high-quality photographs. It has been proposed as a promising alternative to direct ophthalmoscopy in fields outside of ophthalmology (7). In 2011, the FOTO-ED study first demonstrated the value of a retinal camera in the emergency department (ED). Patients presenting with headache, focal neurologic deficits, elevated diastolic blood pressure, and visual complaints were studied. Acutely relevant abnormalities were present on fundus photography in 13% of patients (9). All were missed by the ED physicians, who examined only 14% of these patients by direct ophthalmoscopy (9). We hypothesized that 1) the use of ocular fundus photography would improve patient care in the outpatient neurology resident clinic by assisting in patient management (diagnosis, treatment, and subsequent evaluation) and Pyatka et al: J Neuro-Ophthalmol 2022; 42: 68-72 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Any data not published within the article is available, and anonymized data will be shared by request from any qualified investigator. record (EMR) note of each visit was reviewed to determine if the funduscopic examination was performed, and what funduscopic findings were documented. All retinal photographs were reviewed by the principal investigators within 24 hours of the examination. Ocular fundus photographs of nondiagnostic quality were excluded. Any findings that were equivocal, unclear, or showed significantly abnormal findings were adjudicated or confirmed by a neuro-ophthalmologist (M.M.). When an abnormal finding was missed during the clinic visit, the resident and the attending were informed, and formal neuro-ophthalmology referral was recommended. The following major findings were tabulated: papilledema definite; papilledema questionable; increased cup:disc ratio; arteriovenous nicking; peripapillary atrophy; and optic atrophy. All other ophthalmologic findings were tabulated under an “other” category. Survey feedback from residents was anonymously obtained on their perception of the usefulness of the retinal camera in improving patient care as well as their funduscopy skills. Study Design Statistical Analysis Photographs of the ocular fundus (optic disc, macula, and major retinal vessels) were obtained from both eyes using a commercially available, FDA cleared, nonmydriatic ocular fundus camera (Topcon, TRC-NW400). Images were taken by a trained medical assistant at the time of triage. The medical assistant was instructed to attempt to obtain one high-quality photograph per eye; up to 3 attempts were allowed per each eye. The study subjects were new neurology resident clinic patients that presented from May 2018 to July 2019 at University Hospitals Cleveland Medical Center. Patients who were not able to sit up were excluded from the study. Eye dilation or a dark environment were not required. There was no associated cost to the patients. Images were automatically imported into patients’ record in the radiology Picture Archiving and Communication System (PACS). All the photographs were stored in PACS as Joint Photographic Experts Group images with a resolution of 981 · 693 pixels. The patient visit then proceeded as normal. The residents completed a full neurologic examination, including a funduscopic examination with a handheld ophthalmoscope. They documented their interpretation of the funduscopic examination findings. The residents then reviewed the retinal camera photographs in PACS and documented their interpretation of the images. When residents staffed the patients with their attendings, they discussed their funduscopic examination findings and their interpretation of the retinal photographs. The attendings made final interpretations of the retinal photographs. Residents and attendings were then asked to complete a questionnaire of their interpretation of the PACS photographs. In addition, the final signed electronic medical Data were managed with Microsoft Excel (Microsoft Inc). Statistical analyses were conducted using SPSS version 25 (IBM), R version 3.6.1. Demographics are reported as means and standard deviations or as count data and percentages; comparisons between groups were conducted using Fisher exact tests. 2) would improve resident performance and interpretation of funduscopic findings when performing the direct funduscopic examination. METHODS Standard Protocol Approvals, Registrations, and Patient Consents The study protocol was reviewed by the University Hospitals Cleveland Medical Center Institutional Review Board (IRB). The IRB determined that the project activities did not require IRB oversight or approval. Thus, no patient consent was required. Patients were provided with verbal information about the retinal camera and were allowed to decline. Data Availability Statement Pyatka et al: J Neuro-Ophthalmol 2022; 42: 68-72 RESULTS Two hundred fifty-six sets of photographs were taken; 25 were excluded due to nondiagnostic image quality. Two hundred thirty patients were analyzed (Table 1). Median age was 43; 71% were female and 53% were Black. The most common presenting complaint was headache (49%), followed by seizures (17%). The most frequent medical comorbidities were smoking (43%), HTN (35%), and prior headaches (34%). Nonmydriatic fundus photography detected abnormalities in 69 of 230 patients (30%) and are tabulated in Table 2. Of the 161 patients with normal funduscopy, 134 (83%) were diagnosed correctly by the residents, based on EMR documentation. The fundus could not be visualized in 12% of patients (18 of 161) for various reasons, such as miosis, light sensitivity, cataracts, and poor cooperation. No funduscopic examination was documented in 5% of cases (9 of 161). Based on EMR documentation, residents correctly identified the abnormal findings only 7% of the time (5 of 69). In 14% of these cases (10 of 69), the funduscopic examination could not be done for similar reasons in the group with normal funduscopy. 69 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Demographics Age, yr Sex (%) Male Female Race (%) Caucasian Black Other Complaint (%) Headache Visual disturbances Seizures Neuromuscular Dizziness Pain Cognitive issues Movement disorder Medical comorbidities (%) DM HTN HLD Headaches Stroke Smoker Glaucoma Cataracts TABLE 2. Retinal abnormalities Mean: 45 Range: 18–89 66 (29) 164 (71) 104 (45) 121 (53) 5 (2) 112 (49) 15 (7) 39 (17) 34 (15) 18 (8) 14 (6) 12 (5) 2 (1) 31 (13) 80 (35) 33 (14) 78 (34) 10 (4) 98 (43) 5 (2) 16 (7) The questionnaire forms documenting the PACS photograph interprepations were completed in full for 73 cases by residents and attendings. In these cases, attendings correctly diagnosed 88% of normal cases (46 of 52) and 43% of abnormal cases (9 of 21). They incorrectly diagnosed 11 (52%) abnormal cases as normal. One of the abnormal cases (5%) was misinterpreted. Attendings significantly more often incorrectly diagnosed normal cases (P = 0.008). Based on the questionnaire forms, residents correctly diagnosed 91% of normal cases (51 of 56) and 25% of abnormal cases (5 of 20). They incorrectly diagnosed 13 (65%) abnormal cases as normal. Two of the abnormal cases (10%) were misinterpreted. No significant difference was found between residents’ incorrect and correct diagnoses (P = 0.13). Significantly fewer increased cup:disc ratios were identified as compared with definite papilledema (P = 0.03); no other comparisons were significant. Notably, many types of abnormalities went completely undetected and thus could not be used in statistical comparisons of detectability. Among these, questionable papilledema, peripapillary atrophy, optic atrophy and other had no detected cases by the residents. The survey conducted on resident’s perceptions of the helpfulness of the retinal camera photographs indicated that the residents found the photographs helpful (Table 3). Of 14 residents surveyed, 13 (93%) reported the photographs 70 Abnormality Increased cup/disc ratio Papilledema—definite Papilledema—questionable Peripapillary atrophy Optic atrophy AV nicking Other Total Total Detected 19 8 8 9 6 3 16 69 1 (5) 3 (38) 0 (0) 0 (0) 0 (0) 1 (33) 0 (0) 5 (7) as useful, and 13 (93%) recommended use at other neurology clinics. Regarding improvement, 11 (79%) reported improved comfort level of attempting funduscopy, 6 (43%) reported improved frequency of attempting funduscopy, 12 (86%) reported improved success in visualizing retina, and 12 (86%) reported improved confidence in describing funduscopy findings. DISCUSSION This study demonstrated clear advantages of using a nonmydriatic ocular fundus photography in the outpatient neurology resident clinic. Although many findings were missed by the neurology residents, a substantial number were also missed by neurology attendings. This underscores the difficulty in learning and mastering direct ophthalmoscopy during residency and then practicing it as an attending neurologist. Many funduscopic findings are key to the neurological evaluation, formation of a differential diagnosis, and subsequent testing and treatment. Even papilledema, often considered among the most important of neurologic funduscopic findings, was frequently missed. However, the most common abnormality not recognized was an increased cup:disk ratio. Although not indicative of a primary neurologic problem, an increased cup:disk ratio is associated with glaucoma, one of the most common causes of irreversible blindness. In some cases, acute angle closure glaucoma may be associated with headache and visual obscurations, leading to a neurological evaluation. This study builds on the previous literature on the use of fundus photography in practice and training. The FOTOED (Fundus photography vs Ophthalmoscopy Trial Outcomes) study assessed the feasibility, quality, and diagnostic accuracy of nonmydriatic fundus photography in the ED (9,10). In phase I of this study, 350 patients were studied who presented with headache, focal neurological deficits, acute visual change, or a diastolic blood pressure $120 mm Hg). Concerning ocular fundus findings on nonmydriatic fundus photographs were present in 33; none were identified by ED physicians during their assessment. Overall, ED physicians performed direct ophthalmoscopy only on 48 patients (14%) of the total enrolled in the trial (9). Findings identified on the fundus photography Pyatka et al: J Neuro-Ophthalmol 2022; 42: 68-72 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 3. Resident perceptions of retinal photograph helpfulness Find the Retinal photographs useful? (%) Should retinal camera be used on other neurology clinics? (%) Improved comfort level of attempting funduscopy? (%) Improved frequency of attempting funduscopy? (%) Improved success in visualizing retina? (%) Improved confidence in describing funduscopy findings? (%) included high-grade hypertensive retinopathy, optic disc edema, intraocular hemorrhage, retinal vascular occlusion, and optic disc pallor. During phase II of the study, 354 patients with the same clinical presentation as in phase I were enrolled. Nonmydriatic photographs were reviewed by ED physicians instead of performing direct ophthalmoscopy. In this phase, ED physicians evaluated fundus photographs of 239 patients (68%) as opposed to performing direct ophthalmoscopy on only 14% of patients in phase I (10). ED physicians identified 16 of 35 relevant ocular fundus findings through their review of the photographs, as opposed to identifying none out of 33 ocular findings in the earlier phase when using direct ophthalmoscopy (10). In a subsequent study, obtaining high-quality retinal photographs was demonstrated as feasible using written material and only 15–30 minutes of camera training time (11). Retinal photography has also been shown of value in the training of medical students. In the TOTeMS (Teaching Ophthalmoscopy To Medical Students) study, 70% of 138 first-year medical students who received training on direct ophthalmoscopy, preferred fundus photographs over direct ophthalmoscopy. In addition, students scored better on the photograph posttest compared with an ophthalmoscopy simulator (P , 0.001) (6). More recently, a study looked at nonmydriatic fundus photography in an outpatient neurology setting. Of 206 patients, 44 (21%) had abnormal findings on their fundus photographs, based on independent review by 2 neuroophthalmologists. There was no comparison made between direct ophthalmoscopy findings and the fundus photography findings (12). Our study demonstrated the value of fundus photography in the outpatient neurology resident clinic, both in patients’ care and in resident learning to perform direct funduscopy. The ability to detect pathology markedly improved with fundus photography. The ability to perform the camera examination in nondilated eyes markedly increased its usability. Although nondiagnostic photographs were obtained in a minority of patients, similar or more marked limitations are present with direct ophthalmoscopy. Performing direct ophthalmoscopy skillfully is an ACGME requirement for neurology residents. Based on the resident feedback, the use of nonmydriatic fundus photography in resident clinic not only improved their rate of diagnosing important ocular fundus findings but also improved their comfort level for performing direct ophthalmoscopy and Pyatka et al: J Neuro-Ophthalmol 2022; 42: 68-72 13 13 11 6 12 12 (93) (93) (79) (43) (86) (86) improved the frequency of performing ophthalmoscopy for some residents as well. Overall, the results of our study are similar to prior literature with similar percentages of abnormalities detected with use of nonmydriatic fundus photography. Our data suggest that this technology improves the ability of residents to detect relevant ocular fundus findings, which might be missed on conventional direct ophthalmoscopy. As a large number of patients presented with headaches (49% of our sample), it is especially important in those who had evidence of optic disc edema or optic atrophy, where further imaging was warranted. A strong argument for incorporating nonmydriatic ocular fundus photography into a residents clinic can be made when one considers 1) the risk of negative patient outcomes and possible medicolegal consequences due to missed findings, (2) the ease of incorporating retinal photographs into the patients’ EMRs and sharing with other physicians, and (3) the benefit of improving resident education in regards to the ophthalmologic examination. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: N. Pyatka, M. K. Banks, N. Fotedar, and D. C. Preston; b. Acquisition of data: N. Pyatka, M. K. Banks, and N. Fotedar; c. Analysis and interpretation of data: N. Pyatka, M. K. Banks, N. Fotedar, Sarah J DeLozier, Michael Morgan, and D. C. Preston; Category 2: a. Drafting the manuscript: N. Pyatka, N. Fotedar, Sarah J DeLozier, and D. C. Preston; b. Revising it for intellectual content: N. Pyatka, N. Fotedar, and D. C. Preston. Category 3: a. Final approval of the completed manuscript: N. Pyatka, N. Fotedar, and D. C. Preston. ACKNOWLEDGMENTS The authors specially thank Carol McLaurin for taking the retinal photographs and Eileen Caskovic for scheduling patient encounters in the radiology software. REFERENCES 1. Schneiderman H. The funduscopic examination. In: Walker HK, Hall WD, Hurst JW, eds. Clinical Methods: The History, Physical, and Laboratory Examinations. 3rd edition. Boston, MA: Butterworths, 1990. Available at: https://www.ncbi.nlm. nih.gov/books/NBK221/. Accessed August 3, 2019. 2. Bruce BB, Biousse V, Newman NJ. Nonmydriatic ocular fundus photography in neurologic emergencies. JAMA Neurol. 2015;72:455–459. 71 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution 3. Wang JJ, Baker ML, Hand PJ, Hankey GJ, Lindley RI, Rochtchina E, Wong TY, Liew G, Mitchell P. Transient ischemic attack and acute ischemic stroke: associations with retinal microvascular signs. 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