Background

In the wake of the spread of COVID-19 in the United States, the practice of ophthalmology has undergone a dramatic and unprecedented shift. The inherent risk of transmission is high due to the need for patient proximity during an ophthalmic exam or surgery, which has led to at least one outbreak in Norway [1,2,3,4,5,6,7,8,9,10,11,12,13]. In March 2020, the American Academy of Ophthalmology (AAO) issued practice guidelines and released a list of emergent ophthalmic surgical procedures to be continued during the COVID-19 pandemic [14, 15]. Subsequently, the rescheduling of routine ocular examinations and limiting procedures to those deemed urgent or emergent has been the basis of many recent publications [16,17,18,19,20,21,22,23,24,25,26,27]. Each has offered specialty specific guidelines to limit transmission moving forward, while allowing for the gradual increase in ophthalmic exams, intraocular injections, and surgeries during the COVID-19 pandemic [16,17,18,19,20,21,22,23,24,25,26,27].

Adherence to these recommendations has resulted in an estimated 75% or more reduction of in-person clinic volumes [28]. Concurrently, the implementation of telemedicine visits resulted in an alternative way to provide continued care [3, 25, 29,30,31]. However, the exact reduction of in-patient visits, increase in telemedicine encounters, and the change in the types of diagnoses seen within in an ophthalmology clinic before and after COVID-19 remains unknown. Herein, we describe these changes in clinic volume over all subspecialists in an academic eye clinic as epiphenomena of COVID-19 in ophthalmic practice.

Methods

This was a retrospective analysis of all the ICD-10 diagnosis codes listed in patient encounters from all of the divisions within the Wilmer Eye Institute, main site and satellite clinics, during the 6 weeks prior to (2/17/20 through 3/21/20) and the 6 weeks after the start of emergency visits (3/22/20 through 4/30/20) in response to COVID-19. Immediate institution of a policy providing care for emergent and urgent ophthalmic care was inititated by department leadership in conjuction with Johns Hopkins Health System administration. There was no progressive ramp down of clinical activities. Patients were rescheduled for 4 weeks after their previously booked clinic appointment during this period. If there were any questions on the severity or condition being treated, the treating physician was contacted to advise on the timing of follow-up. ICD-10 codes allow for specification of eye laterality, affected site, and other complications in systemic diseases. All ICD-10 codes for the same diagnosis were consolidated and divided into categories based on ophthalmic subspecialty service at the Wilmer Eye Institute: cornea, oculoplastic surgery, retina, uveitis, pediatric ophthalmology, neuro-ophthalmology, glaucoma, trauma and general ophthalmology, low vision, and oncology. Included with general ophthalmology were ICD-10 codes associated with screening for systemic diseases affecting the eye. The ICD-10 codes were then subdivided into 177 categories based on anatomic location or mechanism of disease (Supplement 1 and Fig. 1). To compare frequency of visits by subspecialty, retina and oncology were merged due to the dual training of our ocular oncologists. Since they also see other retinal conditions in their clinical practice, it was impossible to completely isolate ocular oncology and retina department visits. The rest of the subspecialties were divided in the same way as previously described.

Fig. 1
figure 1

Diagnostic Categories by Subspecialty

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In addition, the number of patient encounters overall and per department were recorded and subdivided into in-person and telemedicine types. Diagnostic categories and encounter frequencies were analyzed; comparisons were evaluated using the χ2 test or Fisher exact test if expected counts within a category were < 5. Statistical analyses were performed using SPSS software version 22.0 (IBM, Armonk, NY, USA). We considered a p-value below 0.05 to be statistically significant. This study was reviewed and approved by the Johns Hopkins Hospital Institutional Review Board (IRB00250067).

Results

In the 6 weeks prior to the start of emergency visits, there were 25,336 completed in-person visits, which resulted in the use of 5261 ICD-10 codes. This is compared with the drastic reduction of patients seen in the 6 weeks thereafter when 5672 in-person visits were completed, which included 2207 ICD-10 codes.

Analyzing the change in the proportional frequency between the 6 weeks after the start of emergency visits and the 6 weeks prior, the retina, uveitis, and oculoplastic surgery divisions showed a significant increase in in-person visits (p < 0.001, < 0.001, and 0.032, respectively). Low vision, pediatric ophthalmology, general ophthalmology, and the cornea division percentage of in-person visits significantly decreased (p < 0.001, < 0.001, < 0.001, 0.001 respectively). There was no significant change in appointments within the glaucoma or neuro-ophthalmology divisions (Fig. 2). In contrast, the amount of telemedicine visits increased 60 fold in the 6 weeks after the start of emergency visits and accounted for 7.6% of total visits during that period (p < 0.001).

Fig. 2
figure 2

A bar graph depicting the change in the percentage of in-person visits by subspecialty in each study period. Significant differences are marked with an asterisk (*)

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We found significant differences in the proportion of ICD-10 codes used in between the pre- and the post-COVID-19 change to emergency in-patient visits (Supplement 2 and Table 1). Of the anterior segment disorders, conjunctival and corneal malignancies, complications of contact lens use, peripheral corneal disease, viral keratitis (Fig. 3) and corneal ulcer ICD-10 codes were used significantly more frequently in the 6 weeks after the shift to emergency visits. Conversely, pterygium and **uecula, cataract, and refractive surgery ICD-10 codes were used significantly less during the same time period. Specifically related to glaucomatous conditions, there was a significant increase in the use of neovascular, juvenile or congenital, uveitic, and secondary glaucoma ICD-10 codes in the weeks after COVID-19 with a concurrent decline of glaucoma suspect and angle-closure suspect codes.

Table 1 The most significant changes in diagnostic codes by ophthalmic subspecialty
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Fig. 3
figure 3

External photograph of pseudodendrites as seen in a patient with herpetic keratitis

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In the neuro-ophthalmology division, optic disc edema, sixth nerve palsies, optic neuritis, and pseudotumor ICD-10 codes were used more frequently post-COVID-19; whereas, the code for nystagmus decreased significantly in frequency. Within the retina division, there was a significant increase in ICD-10 codes associated with the need for injections, such as vein occlusions with macular edema, active wet age-related macular degeneration, active choroidal neovascular membranes (CNVM), and proliferative diabetes with cystoid macular edema (CME). Conversely, ICD-10 codes associated with chronic chorioretinal diseases and retinal screening exams significantly decreased, which included choroidal scars, retinal dystrophies, diabetic eye exams, and screening for hemoglobinopathies.

The uveitis division showed a decrease in ICD-10 codes associated with screening for ocular complications of HIV disease, but no other uveitis associated codes declined. Rather, ICD-10 codes for primary intraocular lymphoma, Vogt-Koyanagi-Harada disease and sympathetic ophthalmia, traumatic uveitis, non-corneal herpetic diseases, and intermediate uveitis were used signficantly more than in the pre-COVID-19 time period. Ocular oncology, as well, showed a significant decrease in the use of choroidal nevus screening codes and showed a signficant increase in the use of choroidal mass codes.

None of the codes associated with pediatric ophthalmology, low vision, and oculoplastics had a proportional increase after the change in in-person visits associatd with COVID-19 were implemented. The ICD-10 codes that declined the most were ocular screenings for chromosomal abnormalities, phorias, and strabismus. In oculoplastic surgery, ICD-10 codes for dermatochalasis, eyelid malpositions, benign tumors of the lids, and obstructive lacrimal duct disease also declined. Finally, ICD-10 codes associated with low vision decreased 27 fold in the 6 weeks post-COVID-19.

Ocular trauma showed a proportional increase in ruptured globes and intraocular foreign bodies in the 6 weeks after the COVID-19 changes. ICD-10 codes for screening for eye or systemic medical disorders, a family history of eye disease, and refractive error were used significantly less frequently than in the 6 weeks pre-COVID-19.

Discussion

The recommendations by the AAO to limit routine ophthalmic examinations and restrict in-patient evaluations to urgent and emergent ocular conditions have been implemented in all of our divisions during COVID 19 as evidenced by the 60 fold increase in telemedicine visits in the weeks after COVID-19 [14, 15]. While the implementation of telehealth visits was being piloted prior to the epidemic, the need to limit in-person evaluations led to rapid wide-spread adoption in most of the divisions. Equally striking, was the significant decline in ophthalmic screening exams for systemic disorders, research study visits, and low vision services. As a whole, ophthalmic conditions leading to immediate vision change, pain and photophobia, ocular malignancies, and trauma continued to be seen in-person.

The specific ICD-10 code frequency changes within each subspecialty requires individual discussion. For conditions affecting the cornea, a significant increase in the percentage of patients seen with ulcers, complications of contact lens use, and peripheral diseases including ulcerative keratitis occurred in the 6 weeks following the start of emergent visits. This again highlights the continued presentation of patients with ocular pain, photophobia, and change in vision. Despite reports of conjunctivitis and red eyes as symptoms of COVID-19, all types of conjunctivitis continued to have a statistically significant decrease in the 6 weeks following COVID-19, except viral conjunctivitis, which decreased in frequency but not significantly [24,25,26,27,28,29,30,31,5,6,7,8,9,10,11,12, 20, 35]. Even in the subspecialty clinics where a significant decrease of visits was noted, diagnostic codes were still used for patients with acute changes in vision. Thus, a provider within each subspecialty division should remain available for in-patient consultation on a daily basis.

One question that will need to be addressed is whether the pandemic has resulted in the avoidance or delay in care for some individuals, who may as a result be at substantial risk for worse ultimate outcomes. Our finding that fewer patients were being screened for HIV-associated retinal disease and that fewer “glaucoma suspects” were seen during this period may mean that pathology in at least a subset of these individuals will have progressed before they are able or willing to present to the ophthalmologist. We suspect, but our study does not allow us to quantify, that there will be an ultimately greater burden of disease as a result of postponed screening visits and timely therapeutic interventions.

Conclusions

An academic ophthalmology department associated with a tertiary referral hospital should be prepared to experience changes in practice patterns, implementation of telemedicine, and decreased patient volumes during a pandemic. Knowing the changes specific to each subspecialty clinic is vital to correctly redistributing available resources. Looking forward, a cost-effectiveness analysis is needed to discern the best way to address these changes while continuing to provide safe patient care and lessen the economic burden of these trying times.