ROP is a leading cause of preventable childhood blindness in middle-income countries [3]. In this study, we aimed at examining the management of this preventable disease during the COVID-19 pandemic. In this international survey on the ROP practice patterns during the COVID-19 pandemic, we found that during this period the number of ROP exams performed on premature infants decreased dramatically. A total of 11.6% of physicians reported that the number of inpatient exams in the NICU during COVID-19 was between 0 and 25%, compared to the pre-COVID-19 number (Fig. 2), and 15.8% reported that the number of outpatient follow-up visits during COVID-19 was between 0 and 25%, compared to the pre- COVID-19 number (Fig. 2). Katoch et al. described similar results in India [5]. Similar results were also found in other ophthalmology fields [6,7,8]. COVID-19 currently affects 219 countries, and all continents. A total of 292 ophthalmologists from 226 different institutions around the world participated in this survey (Fig. 1 and Table S1). Hence, the patterns seen in this study reflect the global ROP practice during this period. The decrease in ROP screening and treatment during COVID-19 could be attributed to several factors, including a shortage of health care staff [3, 9], transportation of teams deployed for general care [9] parents or guardians unwilling or unable to bring their infant to the hospital, and/or clinics being closed [10]. In addition, in this global study, we found that 23% of ophthalmologists examined less than 75% of inpatients in the NICU, compared with the pre-COVID-19 exams. This may indicate that in-house pediatric ophthalmologists were less available because physicians were deployed to other departments or ophthalmologists did not arrive due to the lockdown [11]. Furthermore, Ireland and Denmark reported that fewer premature babies were born in the spring of 2020. They indicated substantial reductions in the number of extremely preterm and very low birthweight births during this time [12, 13]. Our study also found a 47% reduction in the follow-up visits of outpatients during the pandemic. Other explanations for these findings, other than a lower rate of preterm births, include the parents or guardians being too afraid to come in for exams, as well as a higher rate of anxiety [14].

Only 14% of ophthalmologists adopted new guidelines that reduced the number of ROP screening patterns, compared to the pre-COVID-19 numbers, including switching to a risk-based follow-up, based on the Growth and the Retinopathy of Prematurity (G-ROP) guidelines [15], stopping follow-ups for immature zone 3 of low-risk patients, and changing the follow-up intervals of infants treated with VEGF injection to every 2 weeks instead of every week, which is the pre-COVID-19 follow-up pattern.

Only 7% of ophthalmologists reported changing their preferred treatment modality for ROP patients after the first wave of the COVID-19 pandemic (May 2020). The changes made included treating borderline cases by reducing the number of follow-up appointments and avoiding delayed treatment if a family member becomes ill with COVID-19. This finding is similar to the study of Leng et al. demonstrating that although a significant decrease in ophthalmology-related patient visit volume as a result of the COVID-19 pandemic was noted, it did not greatly impact age-related macular degeneration, diabetic macular edema, and macular edema secondary to retinal vein occlusion patients receiving intravitreal injections of anti-VEGF agents to stabilize and improve vision [16].

Unsurprisingly, 73% of ophthalmologists reported that surgical masks were part of their PPE requirements during ROP exams at the NICU, 74.1% reported gloves, and 43% reported that gowns were part of their requirements. These requirements were common in NICUs even prior to the COVID-19 pandemic. However, only 34% reported an N-95 mask or an equivalent mask as part of the PPE requirements. This could result from the limited global supply and competition for these masks; this led to severe shortages during the COVID-19 pandemic (May 2020), and it remains a major challenge and concern [17].

The benefits of anti-VEGF therapy, including the possibility of reduced permanent peripheral visual field loss, reduced anterior segment abnormalities, and less myopia [18] have made anti-VEGF therapy the preferred mode for many ROP patients. Interestingly, our results show that laser photocoagulation was still the preferred first mode of treatment during the COVID-19 pandemic and that the combination of laser photocoagulation and anti-VEGF treatment was used in 35% of the cases. Laser treatment of ROP has the advantage of fewer post-treatment visits; in contrast, anti-VEGF injections enable a shorter treatment session, with higher safety standards for both the infants and staff.

Traditionally, screening for ROP consists of an ophthalmologist examining the baby at the bedside using an indirect ophthalmoscope. In the last few years, telemedicine has been introduced as an alternative using remote interpretation of digital fundus images. Telemedicine enables mildly ill patients to receive the supportive care they need while minimizing their exposure to other acutely ill patients [19, 20]. This can explain the significant rise in telemedicine usage in May 2020 and emphasizes the importance of using technological measures to decrease the risk of exposure to contagious diseases during pandemics while maintaining screening protocols for ROP. Because retinal photography can be stored and forwarded to a remote expert for advice on the urgency of the referral, the use of these devices was expected to increase during the pandemic. Surprisingly, this did not happen. Sood et al. conducted a multicenter study in the US and found significantly more infants were screened with indirect ophthalmoscopy, compared to digital imaging, during the lockdown [21], similar to our study. This could result from several factors, including difficulty in purchasing cameras during the lockdown. In addition, using the equipment requires a learning curve; also, photography requires sterilization and may extend the exam duration, especially when initiated. Not using existing technologies could stem from the fact that this technological platform is less well known and unfamiliar to many ophthalmologists [22]. In addition, some physicians prefer using indirect ophthalmoscopy as it may still be required after using imaging due to the varying sensitivity of screening in cases of peripheral disease and media opacities. Another important factor could be the financial impact COVID-19 has caused on hospitals. While fewer patients were seen throughout every hospital system, in many cases, the health care workers were maintained on salary. With this increased burden, investing in relatively expensive retinal imaging systems and not being able to provide educational sessions on retinal imaging could have been important barriers to potentially increased demand.

In this study, the overall ROP outpatient follow-up visits and the number of inpatient visits at the NICU during the COVID-19 pandemic (May 2020) were significantly greater in North America, compared with the number of pre-COVID-19 ROP examinations in Asia. Most responders to our survey from Asia practiced medicine in India (Table S1). As India held the world’s longest lockdown starting in March 2020 until August 2020 [23] that left millions of people stranded in different parts of the nation with no means of transportation to reach clinics and hospitals [24, 25]. This could be the main reason for our finding. The pandemic first appeared in China, thus, the preparation for dealing with COVID-19 was very limited there and in neighboring countries [26]. This could also contribute to the lower outpatient and inpatient follow-up visits seen in our study. In contrast, in North America, lockdowns were not enforced, and hence follow up visits were possible, explaining the higher percentage of ROP exams.

This survey carries several limitations. Most importantly, the study included self-reported data from self-selected participants. The study was conducted in May 2020, a lockdown period in many countries, and this could be a significant constraint for people wishing to participate in the survey. Moreover, practice patterns may have changed in subsequent corona waves, which were not included in this study. In addition, the present study included only AAOE and IPOSC members that include only a small percentage of the population from each country, so caution should be exercised in generalizing the results to all ROP treating physicians globally. Furthermore, no data on screening numbers were collected, and the only estimate of the percentage change before and during the pandemic is subject to recollection bias. Longitudinal study of the important questions asked in this survey is needed, to fully understand the effect the COVID-19 pandemic had on ROP patients.