Impact of COVID-19 pandemic on retinopathy of prematurity services in low resource settings

Impact of COVID-19 pandemic on retinopathy of prematurity services in low resource settings | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Impact of COVID-19 pandemic on retinopathy of prematurity services in low resource settings Clare Gilbert This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3141875/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 25 Oct, 2023 Read the published version in Eye → Version 1 posted 9 You are reading this latest preprint version Abstract Background and objectives Retinopathy of prematurity is an increasingly important cause of blindness children in low- and middle-income countries. Timely screening and treatment greatly reduce blindness. This study assessed the impact of the COVID-19 pandemic on ROP services in low- and middle-income countries. Methods An online survey with closed and open-ended questions in Microsoft Teams was sent to 304 ophthalmologists providing screening, treatment and/or vitreoretinal services(January 15 to March 12 2021). Categories were used to report impact on services. 28 participants were purposively selected for interview. Results 184/201 completed forms from 32 countries were received. Two thirds of participants worked in government facilities and 45.6% were pediatric ophthalmologists. A moderate to severe impact was reported by 13% for screening, 9% for treatment and 16% for vitreoretinal surgery with some variation between government, private and not-for-profit sectors. 22% thought services would take a year to recover. Fifteen ophthalmologists from 12 countries were interviewed. Many reported fewer neonatal admissions, and several reported more ROP blind infants once restrictions lifted. Themes associated with services continuing included limited lockdown, autonomy and flexibility, commitment, advocacy and technology. Themes associated with a negative impact include fear and panic, closure of facilities, COVID infection or quarantining of health workers and parents, lack of transport and exacerbation of poverty. Conclusions The COVID pandemic had a very variable impact on the provision of ROP services. In some countries where the impact was great, more infants became blind from ROP. Lessons can be learnt for planning pandemic preparedness. Health sciences/Health care/Paediatrics Health sciences/Diseases/Eye diseases Figures Figure 1 Figure 2 INTRODUCTION More than 32,000 preterm infants became blind or visually impaired from retinopathy of prematurity (ROP) in 2010.( 1 ) Control requires high quality neonatal care, screening to detect vision-threatening ROP and urgent treatment when required, with follow up. Screening can be by indirect ophthalmoscopy in the NICU by an ophthalmologist, or using widefield retinal imaging with or without remote image grading.( 2 , 3 ) Retinal images can also be taken using smartphones( 4 ) and shared on social media. Treatment of Type 1 ROP requires urgent peripheral retinal laser photocoagulation, or intravitreal injection of anti-vascular endothelial growth factor (anti-VEGF), sometimes under general anesthesia.( 5 ) The COVID 19 pandemic has disrupted multiple aspects of health care through multiple mechanisms. This study was undertaken to explore the impact of the pandemic on ROP services in low, and lower- and upper- middle-income countries (LICs, LMICs and UMICs, respectively). METHODS Mixed methods were used. After preliminary analysis of an eSurvey, 15 participants were interviewed. eSurvey particpants Work Bank categories in January 2021 defined eligible countries.( 6 ) Participants, all ophthalmologists, were recruited as follows: Group 1. known to one of the authors (CG); Group 2. authors of publications on ROP, and Group 3. snowballing by Group 1 contacts. All were sent an email invitation, and those responding were sent a link to the online survey (eSurvey). At least one reminder was sent. eSurvey A draft questionnaire, with closed and open questions, was pre-tested by an ophthalmologist from an UMIC and subsequently amended. The eSurvey in Microsoft Teams was sent to participants between January 15 and March 12 2021. Data were collected on where participants worked and in which sector (i.e., government, private or not-for-profit); their subspecialty, the number of NICUs where they screen and the timing and duration of lockdown in 2021. Seven categories were used to describe the impact of the pandemic on screening, treatment and vitreoretinal (VR) services (Table 1 ). Participants were also asked whether they had observed any changes in neonatal care and to indicate their willingness to be interviewed. Table 1 Categories to assess the impact of the COVID pandemic on ROP services 1. No impact 2. No impact, but more difficult / takes longer 3. Mild/moderate impact, such as services are not as regular or frequent as before 4. Serious impact: services largely stopped for personal/financial/logistical reasons 5. Serious impact: services largely stopped as I was/am not permitted to work as before 6. Have stopped providing services, for personal/financial/ logistical reasons 7. Have stopped providing services, as I was/am not permitted to work as before 8. I did not screen/treat/provide VR services for ROP before the pandemic Data analysis eSurvey data were imported into Excel to check completeness. Names were used to identify duplicates but de-identified data were analysed. The data are presented as frequencies; proportions were compared using Chi square tests (Social Science Statistics, https://www.socstatistics.com ). Online interviews Interviews were undertaken to understand factors which influenced the impact of the COVID pandemic on services. The following eSurvey data were used to purposively select participants: impact of the pandemic, country and health sector; 28 were invited by email, 20 of whom agreed. Fifteen were interviewed after sending reminders. The interviews (August 2021), which lasted 20–40 minutes, were undertaken by one of the authors (CG) using Zoom and were audio-recorded and saved using eSurvey numbers. Participants were asked to describe their usual practices before the pandemic, and to expand on their eSurvey responses. Audio recordings were initially transcribed using speech-to-text software (otter.ai, https://otter.ai/ , Los Altos, California) and names or locations were redacted. Transcripts were checked against the audio recording by both authors. Data analysis Emerging themes were identified and manually coded by CG using inductive content analysis after immersion in the text. As interviewees were purposively selected according to whether ROP services had or had not been disrupted by the pandemic, subthemes were identified under these two main themes. Further themes and subthemes emerged from the data. Comments in the online survey were extracted verbatim and analyzed to identify new themes. Themes and subthemes were reviewed by the second author. Ethics Ethical approval was obtained from the London School of Hygiene & Tropical Medicine who waived informed consent. In the initial email invitation potential participants were asked to ascertain whether local ethical approval was required. All audio-recordings were deleted after the transcripts were finalized. The CHERRIES checklist was used in reporting.( 7 ) RESULTS 1. Quantitative findings eSurvey participants 201/305 questionnaires were completed; 104 did not respond; 17 were excluded (nine from high-income countries; seven duplicates; one incomplete data) leaving 184 for analysis: 30 (16.4%) in Group 1, 8 (4.3%) in Group 2, and 146 (79.3%) in Group 3. Participants lived in 32 countries (Supplementary Table A); 103 (56%) were UMICs, 77 (42%) were LMICs and four (2%) were LICs. Most worked in government hospitals (67%), with fewer in private (24%) or not-for-profit hospitals (9%); 42% participants worked in government facilities in UMICs. Most participants were pediatric ophthalmologists or VR surgeons (Table 2 ) who provided services in 929 NICUs (range 1-127). Before the pandemic, most participants screened and treated ROP, with variable provision of VR surgery. Table 2 Services for retinopathy of prematurity provided by eSurvey participants Characteristics N % Subspeciality Pediatric ophthalmologist 84 45.6% Vitreoretinal surgeon 78 42.4% General ophthalmologist 22 12.0% Services provided for ROP Screening only 21 11.4% Screening and treatment 159 86.4% Treatment / surgery only 4 2.2% Provision of vitreoretinal services Referred to another hospital 80 43.5% Performed by responding ophthalmologist 48 26.1% Performed by colleague in same hospital 28 15.2% Provision of vitreoretinal services Not available 24 13.0% Mix of the above* 2 1.1% No data 2 1.1% Total 184 100% *Where multiple units were involved, different approaches were used Duration of lockdown In most countries lockdown started towards the end of March 2020, with further lockdowns thereafter in some. Lockdown lasted from 0–9 (mean 2.6) months with variation between economic regions (LICs: mean 1.3 months; LMICs: mean 5.8 months; UMICs mean 3.7 months) The pandemic had no or only minimal impact (categories 1 and 2) on ROP screening (50%), treatment (61%) and VR services (65%)(Table 3 ). Differences between health sectors did not reach statistical significance (Fig. 1 A). However, differences were more pronounced between World Bank regions (Fig. 1 B). No impact on neonatal care was reported by 47% participants (some changes, 39%; major changes, 10%). Differences between health sectors were not statistically significant. Approximately equal proportions considered recovery of ROP services would take a few weeks (18%) or up to a year (22%). Table 3 Impact of the COVID pandemic of services for ROP in low- and middle-income countries amongst eSurvey participants and the subset who were interviewed sSurvey participants (184) Subset interviewed (15) Category Screening Treatment VR surgery None/minimal [1,2] 92 50% 112 61% 120 65% 5 33% 7 47% 9 60% Mild/moderate [3] 66 36% 47 26% 30 16% 4 27% 3 20% 3 20% Severe [4,5] 22 12% 15 8% 30 16% 3 20% 4 27% - - Stopped [6,7] 2 1% 1 1% 0 0% 3 20% 0 0% 1 7% No data [8,9] 2 1% 9 5% 4 2% 0 0% 1 6% 2 13% Total 184 100% 184 100% 184 100% 15 100 15 100 15 100 2. Qualitative findings Participants interviewed In the eSurvey 28 participants declined interview and non-English speakers were excluded; 28 of the remaining 154 participants were purposively selected. Twenty agreed to be interviewed and were sent a date; five did not respond. Fifteen participants from 12 countries were interviewed (response rate 54%). Seven were pediatric ophthalmologists, five were VR surgeons and three were general ophthalmologists; seven were in Group 1 and eight in Group 3. Eight worked in government facilities, five in private, and two in not-for-profit hospitals; 13 provided ROP screening and treatment, and two only screened. One was a national ROP coordinator, and three managed large telemedicine screening programs. Most other ophthalmologists screened using indirect ophthalmoscopy. Participants provided ROP services in 184 NICUs (range 1-127, median 2). The first lockdown ranged from 0–6 (mean 3.6, median 3) months and the restrictions imposed also varied. Some were involved in longstanding ROP programs whereas others had recently started services. In the eSurvey, five (33%) participants reported that the pandemic had no impact ROP screening whereas three (20%) reported that screening stopped (Table 3 ). The impact was less marked for treating ROP and on VR services. Findings are presented under the following headings: 1. impact of the pandemic overall; factors which 2. enabled services to continue or 3. had a negative impact on services 4. resumption of services, and 5. other comments. 1. Impact overall Number screened Several participants reported a fall in the number of babies screened, particularly after discharge from the NICU. The first quote is from an ophthalmologist who manages a large telemedicine screening program. “We averaged 2500–3000 screenings a month pre COVID. In April 2020 this was down to 650” (48 eSurvey (eS) quote/LMIC) “We would normally screen about 120 in a month, but during the pandemic the number had gone down to 50, 40.” (7/LMIC) Number treated The impact on the number of infants treated for acute ROP or who had VR surgery varied: “Any usual year….we treat approximately 50 babies….Last year….it was 25 or 30.” (79/LMIC) “The proportion of babies requiring treatment was the same despite the pandemic.” (48/LMIC) “There was a higher incidence of ROP and severe ROP in my hospital…..compared to previous years” (4eS/UMIC) In one setting, an increase in referrals from ophthalmologists who stopped treating during the pandemic led to a marked increase in the number of infants treated for two to three months.. More ROP blind babies Several ophthalmologist reported that they saw more ROP blind infants once travel restrictions lifted as parents could travel. “June to August we were flooded by babies with advanced disease that were not screened or treated on time in neighbouring states….” (48eS/LMIC) “….screening was not very effective in 2020. As a result, many patients have gone blind due to lack of proper screening” (41eS/LMIC) 2. Factors which enabled ROP services to continue Not a strict lockdown All but one interviewee described strict lockdowns. In this country physicians were permitted to travel freely after showing their institutional identity. Autonomy and flexibility Ophthalmologists providing ROP services in their institution’s NICU could continue as travel was not required. Participants working in the private sector reported several advantages, as the NICUs tended to be smaller with fewer visitors, which reduced the risk and fear of COVID. “Nothing changed…..When I look at my [private] hospitals, the fact that they're a lot smaller, there's not as many people coming in and out, I think that definitely played a role.” (117 UMIC) Another private hospital created a separate facility for COVID patients, which reduced infection amongst staff in the main hospital. An ophthalmologist from a not-for-profit hospital, who screens in government and private NICUs, commented that the impact was much greater in government than in private facilities, as the latter were not included in government COVID control strategies. An additional factor was that families of private patients were better educated and wealthier and could adhere to advice after discharge from the NICU. “Private [patients] were from more educated and well to do families - they can come to our hospital with their own transportation. The government sector of poor patients were late to reach us compared to private babies.” (79/LMIC) Commitment Several participants showed great commitment. For example, one drove long distances to provide services when domestic flights stopped, while others replaced colleagues who were sick, vulnerable or not willing to screen. Advocacy Several continued providing services because ROP was classified as an emergency. In one country, the ophthalmologists successfully advocated that ROP be classified an emergency, which allowed services to continue. Technology Several participants used telemedicine or took images using Smartphones. These individuals were often part of a network who communicated using social media which enabled them to share images and plan how to cover colleagues who had COVID or were quarantining. In one country, all 99 screening ophthalmologists were connected in a network, and could communicate with the three ophthalmologists who could treat acute ROP. 3. Factors which had a negative impact on ROP services A range of inter-connected factors led to negative impacts on ROP services (Fig. 2 ). Fear and panic Several participants described great fear and panic amongst parents, NICU staff and ophthalmologists when the pandemic started, as so much was unknown. “When COVID came, there was a lot of panic and confusion. Everyone [neonatal unit staff] was panicking [saying] ‘Okay, doctor, okay. But people are dying from COVID. Do you think that [ROP screening] is important while we have this problem?’ (201/LMIC) “There was tremendous panic, even amongst healthcare workers. We were not clear about the mode of transmission. Our team was feeling as if we are going onto a battlefield, because we didn't know what kind of risks we were carrying” (7/LMIC) “The factor which [caused the] most panic was… in babies, you can't put a mask on their face, and they're crying all the time. And there was a lot of discussion about this droplet transmission and how you're going to prevent it …when you're screening or treating [ROP] (7/LMIC) One participant described the protective clothing he wore during early lockdown when he visited another NICU to treat an infant using laser. “..it was like a war zone…I had to wear something.. like an astronaut…No one knew how the disease spread and everyone believed that if you were not in that suit you would either get or give the disease.” (48/LMIC) One infant with advanced ROP went blind because the anesthetic staff refused to give a general anesthetic. A reduction in NICU admissions during lockdown, and often for a prolonged period thereafter, was reported by most participants as there was fear of attending hospitals. “Institutional deliveries were markedly decreased during the first 3–4 months COVID.” (201/LMIC) “In the last week of March 2020 there was mandatory leave and widespread panic which forced doctors and patients to stay at home. The number of neonates in the NICUs were reduced drastically in all the NICUs I visited initially” (150eS/LMIC) Closure of facilities Early in the pandemic some government hospitals or their NICUs closed down, while others were converted to COVID hospitals. In some instances, staff were transferred from NICUs to care for patients with COVID. These factors had a major impact on all aspects of ROP services. “So when the lockdown came the university closed… this whole [ROP] service stopped” (11/LMIC) “Of the 17 services that I attended before the pandemic, three ended the activities of the NICU to accommodate COVID beds.” (179eS/UMIC) “We used to refer babies with Stage 4 and 5 (ROP) [for VR surgery]. However, the ….institute …was converted to a designated COVID hospital….” (102eS/LMIC) Staff infection Sickness amongst hospital staff also had a major impact on services in some settings. “The other [maternity] hospital…about 80% of [staff] caught COVID within a week. It was a Ministry of Health emergency - the whole hospital was closed down - all the patients were discharged.” (11/LMIC) “Screening stopped in one unit as several staff became infected and this led to closure. The kangaroo mother's room was closed, reducing numbers of babies screened drastically.” (11eS/LMIC) COVID infection amongst NICU staff meant that remaining staff were overworked and could not assist ROP screening. “…nurses just forgot to dilate the babies [pupils] because they were overwhelmed with so many babies..” (7/LMIC) Ophthalmologists also developed COVID. In one eye department, the screening ophthalmologist was the head of department. COVID infection amongst the residents because of inadequate PPE his focus was on keeping the eye department running. Quarantine and PCR testing. Health care professionals and parents sometimes had to go into quarantine after contact with an infected individual. “One infant’s father's was detected with COVID the day before [VR] surgery and the whole family was quarantined….. for 17 days…By the time they came back, it was inoperable.” (7 LMIC) Several participants reported that later in the pandemic PCR testing was required, particularly before ROP treatment or VR surgery, which also caused delays. Lack of public transport and travel restrictions Lack of public transport and/or travel restrictions during lockdown had a major impact on NICU staff, ophthalmologists, and parents of infants who needed to be screened or treated after discharge. Several ophthalmologists were given passes/permission to travel within their city or district but could not travel further afield. “Transport completely stopped. And we needed government passes to move….but patients were unable to reach the centre for screening.” (79/LMIC) “…inter-district travel was completely banned. And twice, our vehicle (for the screening team) was sent back by the police at the district border so there was nothing we could do.” (7/LMIC) Several said that the cost of private transport was prohibitive for poor families. “…follow up was a very big challenge….Many of them could not afford [a taxi].” (34/LIC) Some infants with Type 1 ROP could not move from one district to another for treatment. “Babies referred from outside my city sometimes took longer to get to me….and some progressed to higher stages.” (20eS/LMIC) One participant gave a graphic account of the impact of the inter-district travel ban on access to treatment. In this setting, some ophthalmologists only screen for ROP and refer infants needing treatment to an ophthalmologist in another district. However, during the pandemic when local treatment was not available, some babies were treated by inexperienced ophthalmologists. “There were a lot of incomplete treatments, late treatments who were coming to us with bad-looking ROP. In some we could just salvage one eye after treatment. It was like dealing with victims of war.” (48/LMIC) Several African participants had only recently started ROP services. Because they did not have lasers, they used anti-VEGF treatment which often had to be sourced from overseas as these drugs were not on their Essential Drugs List. Restrictions on air travel made this even more difficult. Poorer quality neonatal care Shortages of NICU staff, for whatever reason, led to worse nurse to baby ratios. Several participants observed poorer quality of care, particularly in oxygen administration. Poverty exacerbated During the pandemic people not formally employed or in non-essential jobs were particularly vulnerable to loss of income. This, combined with the need to pay for private transport, impacted parent’s ability to access treatment. “Quite a few parents said they had lost their job or their income had reduced, and they could not afford treatment. Even if we said ‘treatment would be free, you just come’, they just didn't have money to come” (7/LMIC) Change in treatment Several ophthalmologists modified how they treated infants. Fear of COVID transmission during laser treatment meant that some used anti-VEGF agents instead, which is quicker. Some started using laser after anti-VEGF treatment as follow up after monotherapy could not be guaranteed. 4. Resumption of services Several participants reported that ROP services had almost returned to normal. Others thought it would take longer, or would be difficult, as COVID vaccination was being prioritized by Ministries of Health and the backlog of ophthalmic outpatients hampered resumption of normal ROP services. 5. Other comments Several ophthalmologists said that plans to expand ROP services stalled during 2020 as they could not travel to train, or the authorities were focusing on COVID. One participant commented on the advantages that telemedicine would have offered during the pandemic, as one trained individual could visit several NICUs. Some reported positive impacts in relation to neonatal care, and in one country the screening guidelines were modified. “[Nurses worked in] “bubbles”….We noticed we had less residents and observers and less sepsis cases. The units were quiet, no noise. Communication between the NICU teams was stronger.” (5/UMIC) “We streamlined the screening [guidelines] and created a lot of awareness among people to take on ROP (services)…. There's a lot of sharing of information now….” (48/LMIC) DISCUSSION The COVID pandemic affected health in many ways globally both directly and indirectly. Routine health services were often curtailed during lockdown, including surgery for congenital conditions.( 8 , 9 ) We identified six studies on the impact on ROP services, from the USA,( 10 ) India( 11 , 12 , 13 , 14 ) and China.( 15 ) Two described the mitigation measures adopted which allowed services to continue.( 10 , 14 ) The other studies all report that fewer infants were screened during lockdown, with a variable impact on the number treated. This may reflect publication bias, as half of the eSurvey participants in our study reported no or only minimal impact on screening or treatment. Our study is the first to report that in some countries more preterm babies were likely to have gone blind from ROP because of the pandemic, but participants did not have data to support their statements. Fewer NICU admissions during lockdown were reported by many participants and in publications( 14 ). This is likely to reflect fear and panic, COVID infection among staff, NICUs being converted to COVID care and travel restrictions. This may, in part, explain why some participants reported fewer infants needing treatment. However, several high-income countries and China have reported lower preterm birth rates during lockdown,( 16 , 17 , 18 , 19 ) which has led to international collaborative research on interventions to prevent preterm birth.( 20 ) In our study, the impact on screening was greater in government than in private hospitals, but differences were not statistically different, which may reflect the small sample size. Explanations given were that families accessing private neonatal care could afford to travel, neonatal staff were not transferred for COVID duties, and managers had greater autonomy to make changes. Differences between economic regions were more pronounced which may, in part, reflect the scarcity of ophthalmologists skilled in ROP, particularly in LICs in Africa.( 21 ) Half of the participants were able to provide ROP services throughout lockdown despite PPE making this more difficult, which is testament to their commitment. Several mentioned the role of social media, which ensured continuity of care when screeners became sick, or were quarantining or vulnerable. Others thought that telemedicine would be advantageous, but there are considerable resource and infrastructure implications.( 22 ) Several ophthalmologists changed how they treated ROP during lockdown, which was influenced by lack of general anesthesia because anesthetists were either caring for COVID patients or they feared droplet transmission. Another factor was anxiety that infants treated with anti-VEGF would not return regularly for follow up. To address this challenge, some started routine laser a few weeks after anti-VEGF treatment. Several African ophthalmologists said they routinely use anti-VEGF agents as lasers are not available,( 21 ) but accessing the agents was often difficult during the pandemic. There is an urgent need to ensure that all treatment modalities for ROP are accessible and affordable. The impact on VR services is more difficult to interpret, as several participants referred infants for surgery before the pandemic and continued to do so during the pandemic. In MIC and LIC parents of preterm infants are often poorly educated and are poor, and compliance with outpatient screening and treatment is challenging even under normal circumstances.( 23 , 24 ) Loss of income during the pandemic would have made compliance even more difficult, particularly for those in the informal labour market. The economic impact of the COVID pandemic on households and the ensuing recession( 25 ) is likely to continue to affect access to health care, including for ROP services. Ensuring that ROP services are covered by health insurance would help to mitigate the economic burden on parents. There are several limitations in our study. Response rates to the eSurvey and interviews were low which may have introduced selection bias. Non-responders to the interview were not replaced, as no new themes emerged during the last few interviews. Almost half of those interviewed were known to the interviewer, which may have introduced bias, and including neonatal staff and parents would have given a more complete picture. Another limitation is that most ophthalmologists could not provide data on the number of infants screened or treated before and during the pandemic. Conclusion This study has highlighted the limitations of ROP services in some locations, such as lack of lasers, and the limited number of ophthalmologists with skills to treat ROP, which accentuated the impact of the pandemic. The study also highlighted lack of pandemic preparedness, and how mitigation strategies were developed as the pandemic evolved. Ideally ROP screening and treatment should be included as an essential service in pandemic preparedness plans, as in India.( 26 ) This might include adapting national ROP guidelines, advocating that infants requiring treatment be permitted to travel and developing networks of ROP service providers to maintain continuity of care. Abbreviations eS eSurvey LIC Low income country LMIC Lower middle-income country ROP Retinopathy of prematurity NICU Neonatal intensive care unit UMIC Upper middle-income country VEGF Vascular endothelial factor VR Vitreoretinal Declarations Funding support None Author contribution statement Clare Gilbert conceptualized and designed the study, collected and analyzed the data and wrote the first draft of the manuscript and takes responsibility for the intellectual content. Joshua Todd assisted in data management and analysis and reviewed and revised the manuscript. Data Sharing Statement Deidentified individual participant data will not be made available. ACKNOWLEDGEMENTS We thank all the participants for contributing to this study. Conflict of interest disclosure The authors have no conflicts of interest relevant to this article to disclose References Blencowe H, Lawn JE, Vazquez T, Fielder A, Gilbert C. 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The international Perinatal Outcomes in the Pandemic (iPOP) study: protocol. Wellcome Open Res. 2021;6:21. Ademola-Popoola DS, Fajolu IB, Gilbert C, Olusanya BA, Onakpoya OH, Ezisi CN, et al. Strengthening retinopathy of prematurity screening and treatment services in Nigeria: a case study of activities, challenges and outcomes 2017–2020. BMJ Open Ophthalmol. 2021;6(1):e000645. Al-Khaled T, Valikodath NG, Patel SN, Cole E, Chervinko M, Douglas CE, et al. Addressing the Third Epidemic of Retinopathy of Prematurity Through Telemedicine and Technology: A Systematic Review. J Pediatr Ophthalmol Strabismus. 2021;58(4):261–9. Taqui AM, Syed R, Chaudhry TA, Ahmad K, Salat MS. Retinopathy of prematurity: frequency and risk factors in a tertiary care hospital in Karachi, Pakistan. J Pak Med Assoc. 2008;58(4):186–90. Vinekar A, Jayadev C, Mangalesh S, Kurian M, Dogra M, Bauer N, et al. Initiating Retinopathy of Prematurity Screening before Discharge from the Neonatal Care Unit: Effect on Enrolment in Rural India. Indian Pediatr. 2016;53 Suppl 2:S107-S11. Sumner AH, Chris; Ortiz-Juarez, Eduardo (2020): Estimates of the impact of COVID-19 on global poverty, WIDER Working Paper, No. 2020/43, ISBN 978-92-9256-800-9, The United Nations University World Institute for Development Economics Research (UNU-WIDER), Helsinki. https://doi.org/10.35188/UNU-WIDER/2020/800-9 . Sengupta S, Honavar SG, Sachdev MS, Sharma N, Kumar A, Ram J, et al. All India Ophthalmological Society - Indian Journal of Ophthalmology consensus statement on preferred practices during the COVID-19 pandemic. Indian J Ophthalmol. 2020;68(5):711–24. Supplementary Table A Supplementary Table A is not available with this version. Additional Declarations There is no conflict of interest Cite Share Download PDF Status: Published Journal Publication published 25 Oct, 2023 Read the published version in Eye → Version 1 posted Editorial decision: revise 27 Sep, 2023 Review # 2 received at journal 13 Sep, 2023 Reviewer # 2 agreed at journal 13 Sep, 2023 Review # 1 received at journal 06 Sep, 2023 Reviewer # 1 agreed at journal 02 Aug, 2023 Reviewers invited by journal 27 Jul, 2023 Editor assigned by journal 13 Jul, 2023 Submission checks completed at journal 13 Jul, 2023 First submitted to journal 05 Jul, 2023 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3141875","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":222111940,"identity":"d7db2d1f-bb5c-4321-a9fd-5e72b4f63dec","order_by":0,"name":"Clare Gilbert","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABEUlEQVRIiWNgGAWjYDACdgjFwycBoiosGAxgMhK4tDBDtbCBVBw4I8FgwEakFgawloNtRGjhb2Z+9uEDQ60Mm3Tzsc8f50nYm8t3JzD8qGFInNmAXYvEYTbjmTMYjvOwyRxLnnFwm0TizjbeDYw9xxgSZ+OwxYCZwZiZh+EY0C85xgxALQkGx3g3MPA2MCTOw6mF/TPzH7CW/M8MB+dI2IO0MP7Fq4XHGBgCNSBbmBkONkgwbgBqYQbZgsthEod5ihl7DA6A/GLMcOaYROKGY7kbDssckzDG5X3+9vbNDD8q6uz5pZsfM1TU2NgbHD678eGbGhvZGQdwWANx3mFU/gE8EQkDdYQUjIJRMApGwUgGAPqrUEex7IzmAAAAAElFTkSuQmCC","orcid":"","institution":"London School of Hygiene and Tropical Medicine","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Clare","middleName":"","lastName":"Gilbert","suffix":""}],"badges":[],"createdAt":"2023-07-05 09:41:58","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3141875/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3141875/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1038/s41433-023-02784-6","type":"published","date":"2023-10-25T04:00:00+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":40967523,"identity":"de1aa798-8fae-4034-aba7-67b0c4c98805","added_by":"auto","created_at":"2023-08-02 16:29:39","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":126545,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eImpact of COVID 19 pandemic on services for ROP by A) health sector B) World Bank Economic Region\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"Figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-3141875/v1/095c6b9ab744e77f804bfe10.png"},{"id":40967522,"identity":"05e57c0d-46a4-4354-844b-3a86a27e88d0","added_by":"auto","created_at":"2023-08-02 16:29:38","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":39830,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eInterconnected pathways in which the COVID pandemic negatively impacted services for ROP\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"Figure2.png","url":"https://assets-eu.researchsquare.com/files/rs-3141875/v1/03d57b9875b74942ec92776c.png"},{"id":45300556,"identity":"7f7e6cca-e22e-44a8-b4b2-90343ccc5e64","added_by":"auto","created_at":"2023-10-27 07:20:47","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":620630,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3141875/v1/d318bd7a-4e31-46f8-829c-a05a315bfc0a.pdf"}],"financialInterests":"There is no conflict of interest","formattedTitle":"Impact of COVID-19 pandemic on retinopathy of prematurity services in low resource settings","fulltext":[{"header":"INTRODUCTION","content":"\u003cp\u003eMore than 32,000 preterm infants became blind or visually impaired from retinopathy of prematurity (ROP) in 2010.(\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e) Control requires high quality neonatal care, screening to detect vision-threatening ROP and urgent treatment when required, with follow up.\u003c/p\u003e \u003cp\u003eScreening can be by indirect ophthalmoscopy in the NICU by an ophthalmologist, or using widefield retinal imaging with or without remote image grading.(\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e, \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e) Retinal images can also be taken using smartphones(\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e) and shared on social media. Treatment of Type 1 ROP requires urgent peripheral retinal laser photocoagulation, or intravitreal injection of anti-vascular endothelial growth factor (anti-VEGF), sometimes under general anesthesia.(\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e)\u003c/p\u003e \u003cp\u003eThe COVID 19 pandemic has disrupted multiple aspects of health care through multiple mechanisms. This study was undertaken to explore the impact of the pandemic on ROP services in low, and lower- and upper- middle-income countries (LICs, LMICs and UMICs, respectively).\u003c/p\u003e"},{"header":"METHODS","content":"\u003cp\u003eMixed methods were used. After preliminary analysis of an eSurvey, 15 participants were interviewed.\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eeSurvey particpants\u003c/h2\u003e \u003cp\u003eWork Bank categories in January 2021 defined eligible countries.(\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e) Participants, all ophthalmologists, were recruited as follows: Group 1. known to one of the authors (CG); Group 2. authors of publications on ROP, and Group 3. snowballing by Group 1 contacts. All were sent an email invitation, and those responding were sent a link to the online survey (eSurvey). At least one reminder was sent.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eeSurvey\u003c/h2\u003e \u003cp\u003eA draft questionnaire, with closed and open questions, was pre-tested by an ophthalmologist from an UMIC and subsequently amended. The eSurvey in Microsoft Teams was sent to participants between January 15 and March 12 2021. Data were collected on where participants worked and in which sector (i.e., government, private or not-for-profit); their subspecialty, the number of NICUs where they screen and the timing and duration of lockdown in 2021. Seven categories were used to describe the impact of the pandemic on screening, treatment and vitreoretinal (VR) services (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Participants were also asked whether they had observed any changes in neonatal care and to indicate their willingness to be interviewed.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eCategories to assess the impact of the COVID pandemic on ROP services\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003e1. No impact\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e2. No impact, but more difficult / takes longer\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e3. Mild/moderate impact, such as services are not as regular or frequent as before\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e4. Serious impact: services largely stopped for personal/financial/logistical reasons\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e5. Serious impact: services largely stopped as I was/am not permitted to work as before\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e6. Have stopped providing services, for personal/financial/ logistical reasons\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e7. Have stopped providing services, as I was/am not permitted to work as before\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e8. I did not screen/treat/provide VR services for ROP before the pandemic\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cp\u003eeSurvey data were imported into Excel to check completeness. Names were used to identify duplicates but de-identified data were analysed. The data are presented as frequencies; proportions were compared using Chi square tests (Social Science Statistics, \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://www.socstatistics.com\u003c/span\u003e\u003cspan address=\"https://www.socstatistics.com\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eOnline interviews\u003c/h2\u003e \u003cp\u003eInterviews were undertaken to understand factors which influenced the impact of the COVID pandemic on services. The following eSurvey data were used to purposively select participants: impact of the pandemic, country and health sector; 28 were invited by email, 20 of whom agreed. Fifteen were interviewed after sending reminders.\u003c/p\u003e \u003cp\u003eThe interviews (August 2021), which lasted 20\u0026ndash;40 minutes, were undertaken by one of the authors (CG) using Zoom and were audio-recorded and saved using eSurvey numbers. Participants were asked to describe their usual practices before the pandemic, and to expand on their eSurvey responses. Audio recordings were initially transcribed using speech-to-text software (otter.ai, \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://otter.ai/\u003c/span\u003e\u003cspan address=\"https://otter.ai/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e, Los Altos, California) and names or locations were redacted. Transcripts were checked against the audio recording by both authors.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cp\u003eEmerging themes were identified and manually coded by CG using inductive content analysis after immersion in the text. As interviewees were purposively selected according to whether ROP services had or had not been disrupted by the pandemic, subthemes were identified under these two main themes. Further themes and subthemes emerged from the data. Comments in the online survey were extracted verbatim and analyzed to identify new themes. Themes and subthemes were reviewed by the second author.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eEthics\u003c/h2\u003e \u003cp\u003e \u003cstrong\u003eEthical approval\u003c/strong\u003e \u003cp\u003ewas obtained from the London School of Hygiene \u0026amp; Tropical Medicine who waived informed consent. In the initial email invitation potential participants were asked to ascertain whether local ethical approval was required. All audio-recordings were deleted after the transcripts were finalized. The CHERRIES checklist was used in reporting.(\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e)\u003c/p\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"RESULTS","content":"\u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003e1. Quantitative findings\u003c/h2\u003e \u003cdiv id=\"Sec11\" class=\"Section3\"\u003e \u003ch2\u003eeSurvey participants\u003c/h2\u003e \u003cp\u003e201/305 questionnaires were completed; 104 did not respond; 17 were excluded (nine from high-income countries; seven duplicates; one incomplete data) leaving 184 for analysis: 30 (16.4%) in Group 1, 8 (4.3%) in Group 2, and 146 (79.3%) in Group 3. Participants lived in 32 countries (Supplementary Table A); 103 (56%) were UMICs, 77 (42%) were LMICs and four (2%) were LICs. Most worked in government hospitals (67%), with fewer in private (24%) or not-for-profit hospitals (9%); 42% participants worked in government facilities in UMICs.\u003c/p\u003e \u003cp\u003eMost participants were pediatric ophthalmologists or VR surgeons (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e) who provided services in 929 NICUs (range 1-127). Before the pandemic, most participants screened and treated ROP, with variable provision of VR surgery.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eServices for retinopathy of prematurity provided by eSurvey participants\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e \u003cp\u003eCharacteristics\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eN\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003e%\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e\u003cb\u003eSubspeciality\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003ePediatric ophthalmologist\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e84\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e45.6%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eVitreoretinal surgeon\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e78\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e42.4%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eGeneral ophthalmologist\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e22\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e12.0%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e\u003cb\u003eServices provided for ROP\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eScreening only\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e21\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e11.4%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eScreening and treatment\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e159\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e86.4%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eTreatment / surgery only\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2.2%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e\u003cb\u003eProvision of vitreoretinal services\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eReferred to another hospital\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e80\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e43.5%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003ePerformed by responding ophthalmologist\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e48\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e26.1%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003ePerformed by colleague in same hospital\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e15.2%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e\u003cb\u003eProvision of vitreoretinal services\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eNot available\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e24\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e13.0%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMix of the above*\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.1%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eNo data\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.1%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eTotal\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e184\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e100%\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003e*Where multiple units were involved, different approaches were used\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eDuration of lockdown\u003c/h2\u003e \u003cp\u003eIn most countries lockdown started towards the end of March 2020, with further lockdowns thereafter in some. Lockdown lasted from 0\u0026ndash;9 (mean 2.6) months with variation between economic regions (LICs: mean 1.3 months; LMICs: mean 5.8 months; UMICs mean 3.7 months)\u003c/p\u003e \u003cp\u003eThe pandemic had no or only minimal impact (categories 1 and 2) on ROP screening (50%), treatment (61%) and VR services (65%)(Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). Differences between health sectors did not reach statistical significance (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA). However, differences were more pronounced between World Bank regions (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eB). No impact on neonatal care was reported by 47% participants (some changes, 39%; major changes, 10%). Differences between health sectors were not statistically significant. Approximately equal proportions considered recovery of ROP services would take a few weeks (18%) or up to a year (22%).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eImpact of the COVID pandemic of services for ROP in low- and middle-income countries amongst eSurvey participants and the subset who were interviewed\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"13\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c10\" colnum=\"10\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c11\" colnum=\"11\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c12\" colnum=\"12\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c13\" colnum=\"13\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"6\" nameend=\"c7\" namest=\"c2\"\u003e \u003cp\u003esSurvey participants (184)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"6\" nameend=\"c13\" namest=\"c8\"\u003e \u003cp\u003eSubset interviewed (15)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCategory\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eScreening\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c5\" namest=\"c4\"\u003e \u003cp\u003eTreatment\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c7\" namest=\"c6\"\u003e \u003cp\u003eVR surgery\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c9\" namest=\"c8\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c11\" namest=\"c10\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c13\" namest=\"c12\"\u003e\u0026nbsp;\u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNone/minimal [1,2]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e92\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e50%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e112\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e61%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e120\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e65%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e33%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e47%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e60%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMild/moderate [3]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e66\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e36%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e47\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e26%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e30\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e16%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e27%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e20%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e20%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSevere [4,5]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e22\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e12%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e8%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e30\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e16%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e20%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e27%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eStopped [6,7]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e0%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e20%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e0%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e7%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNo data [8,9]\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e5%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e2%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e0%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e6%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e13%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eTotal\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003e184\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e100%\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e184\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e100%\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e184\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e\u003cb\u003e100%\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e\u003cb\u003e15\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e\u003cb\u003e100\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e\u003cb\u003e15\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e\u003cb\u003e100\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e\u003cb\u003e15\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e\u003cb\u003e100\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003e2. Qualitative findings\u003c/h2\u003e \u003cdiv id=\"Sec14\" class=\"Section3\"\u003e \u003ch2\u003eParticipants interviewed\u003c/h2\u003e \u003cp\u003eIn the eSurvey 28 participants declined interview and non-English speakers were excluded; 28 of the remaining 154 participants were purposively selected. Twenty agreed to be interviewed and were sent a date; five did not respond. Fifteen participants from 12 countries were interviewed (response rate 54%). Seven were pediatric ophthalmologists, five were VR surgeons and three were general ophthalmologists; seven were in Group 1 and eight in Group 3. Eight worked in government facilities, five in private, and two in not-for-profit hospitals; 13 provided ROP screening and treatment, and two only screened. One was a national ROP coordinator, and three managed large telemedicine screening programs. Most other ophthalmologists screened using indirect ophthalmoscopy. Participants provided ROP services in 184 NICUs (range 1-127, median 2). The first lockdown ranged from 0\u0026ndash;6 (mean 3.6, median 3) months and the restrictions imposed also varied. Some were involved in longstanding ROP programs whereas others had recently started services. In the eSurvey, five (33%) participants reported that the pandemic had no impact ROP screening whereas three (20%) reported that screening stopped (Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). The impact was less marked for treating ROP and on VR services.\u003c/p\u003e \u003cp\u003eFindings are presented under the following headings: 1. impact of the pandemic overall; factors which 2. enabled services to continue or 3. had a negative impact on services 4. resumption of services, and 5. other comments.\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003e1. Impact overall\u003c/h2\u003e \u003cdiv id=\"Sec16\" class=\"Section3\"\u003e \u003ch2\u003eNumber screened\u003c/h2\u003e \u003cp\u003eSeveral participants reported a fall in the number of babies screened, particularly after discharge from the NICU. The first quote is from an ophthalmologist who manages a large telemedicine screening program.\u003c/p\u003e \u003cp\u003e\u0026ldquo;We averaged 2500\u0026ndash;3000 screenings a month pre COVID. In April 2020 this was down to 650\u0026rdquo; (48 eSurvey (eS) quote/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;We would normally screen about 120 in a month, but during the pandemic the number had gone down to 50, 40.\u0026rdquo; (7/LMIC)\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec17\" class=\"Section2\"\u003e \u003ch2\u003eNumber treated\u003c/h2\u003e \u003cp\u003eThe impact on the number of infants treated for acute ROP or who had VR surgery varied:\u003c/p\u003e \u003cp\u003e\u0026ldquo;Any usual year\u0026hellip;.we treat approximately 50 babies\u0026hellip;.Last year\u0026hellip;.it was 25 or 30.\u0026rdquo; (79/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;The proportion of babies requiring treatment was the same despite the pandemic.\u0026rdquo; (48/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;There was a higher incidence of ROP and severe ROP in my hospital\u0026hellip;..compared to previous years\u0026rdquo; (4eS/UMIC)\u003c/p\u003e \u003cp\u003eIn one setting, an increase in referrals from ophthalmologists who stopped treating during the pandemic led to a marked increase in the number of infants treated for two to three months..\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec18\" class=\"Section2\"\u003e \u003ch2\u003eMore ROP blind babies\u003c/h2\u003e \u003cp\u003eSeveral ophthalmologist reported that they saw more ROP blind infants once travel restrictions lifted as parents could travel.\u003c/p\u003e \u003cp\u003e\u0026ldquo;June to August we were flooded by babies with advanced disease that were not screened or treated on time in neighbouring states\u0026hellip;.\u0026rdquo; (48eS/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;\u0026hellip;.screening was not very effective in 2020. As a result, many patients have gone blind due to lack of proper screening\u0026rdquo; (41eS/LMIC)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec19\" class=\"Section2\"\u003e \u003ch2\u003e2. Factors which enabled ROP services to continue\u003c/h2\u003e \u003cdiv id=\"Sec20\" class=\"Section3\"\u003e \u003ch2\u003eNot a strict lockdown\u003c/h2\u003e \u003cp\u003eAll but one interviewee described strict lockdowns. In this country physicians were permitted to travel freely after showing their institutional identity.\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec21\" class=\"Section2\"\u003e \u003ch2\u003eAutonomy and flexibility\u003c/h2\u003e \u003cp\u003eOphthalmologists providing ROP services in their institution\u0026rsquo;s NICU could continue as travel was not required. Participants working in the private sector reported several advantages, as the NICUs tended to be smaller with fewer visitors, which reduced the risk and fear of COVID.\u003c/p\u003e \u003cp\u003e\u0026ldquo;Nothing changed\u0026hellip;..When I look at my [private] hospitals, the fact that they're a lot smaller, there's not as many people coming in and out, I think that definitely played a role.\u0026rdquo; (117 UMIC)\u003c/p\u003e \u003cp\u003eAnother private hospital created a separate facility for COVID patients, which reduced infection amongst staff in the main hospital. An ophthalmologist from a not-for-profit hospital, who screens in government and private NICUs, commented that the impact was much greater in government than in private facilities, as the latter were not included in government COVID control strategies. An additional factor was that families of private patients were better educated and wealthier and could adhere to advice after discharge from the NICU.\u003c/p\u003e \u003cp\u003e\u0026ldquo;Private [patients] were from more educated and well to do families - they can come to our hospital with their own transportation. The government sector of poor patients were late to reach us compared to private babies.\u0026rdquo; (79/LMIC)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec22\" class=\"Section2\"\u003e \u003ch2\u003eCommitment\u003c/h2\u003e \u003cp\u003eSeveral participants showed great commitment. For example, one drove long distances to provide services when domestic flights stopped, while others replaced colleagues who were sick, vulnerable or not willing to screen.\u003c/p\u003e \u003cdiv id=\"Sec23\" class=\"Section3\"\u003e \u003ch2\u003eAdvocacy\u003c/h2\u003e \u003cp\u003eSeveral continued providing services because ROP was classified as an emergency. In one country, the ophthalmologists successfully advocated that ROP be classified an emergency, which allowed services to continue.\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec24\" class=\"Section2\"\u003e \u003ch2\u003eTechnology\u003c/h2\u003e \u003cp\u003eSeveral participants used telemedicine or took images using Smartphones. These individuals were often part of a network who communicated using social media which enabled them to share images and plan how to cover colleagues who had COVID or were quarantining. In one country, all 99 screening ophthalmologists were connected in a network, and could communicate with the three ophthalmologists who could treat acute ROP.\u003c/p\u003e \u003cdiv id=\"Sec25\" class=\"Section3\"\u003e \u003ch2\u003e3. Factors which had a negative impact on ROP services\u003c/h2\u003e \u003cp\u003eA range of inter-connected factors led to negative impacts on ROP services (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec26\" class=\"Section3\"\u003e \u003ch2\u003eFear and panic\u003c/h2\u003e \u003cp\u003eSeveral participants described great fear and panic amongst parents, NICU staff and ophthalmologists when the pandemic started, as so much was unknown.\u003c/p\u003e \u003cp\u003e\u0026ldquo;When COVID came, there was a lot of panic and confusion. Everyone [neonatal unit staff] was panicking [saying] \u0026lsquo;Okay, doctor, okay. But people are dying from COVID. Do you think that [ROP screening] is important while we have this problem?\u0026rsquo; (201/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;There was tremendous panic, even amongst healthcare workers. We were not clear about the mode of transmission. Our team was feeling as if we are going onto a battlefield, because we didn't know what kind of risks we were carrying\u0026rdquo; (7/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;The factor which [caused the] most panic was\u0026hellip; in babies, you can't put a mask on their face, and they're crying all the time. And there was a lot of discussion about this droplet transmission and how you're going to prevent it \u0026hellip;when you're screening or treating [ROP] (7/LMIC)\u003c/p\u003e \u003cp\u003eOne participant described the protective clothing he wore during early lockdown when he visited another NICU to treat an infant using laser.\u003c/p\u003e \u003cp\u003e\u0026ldquo;..it was like a war zone\u0026hellip;I had to wear something.. like an astronaut\u0026hellip;No one knew how the disease spread and everyone believed that if you were not in that suit you would either get or give the disease.\u0026rdquo; (48/LMIC)\u003c/p\u003e \u003cp\u003eOne infant with advanced ROP went blind because the anesthetic staff refused to give a general anesthetic.\u003c/p\u003e \u003cp\u003eA reduction in NICU admissions during lockdown, and often for a prolonged period thereafter, was reported by most participants as there was fear of attending hospitals.\u003c/p\u003e \u003cp\u003e\u0026ldquo;Institutional deliveries were markedly decreased during the first 3\u0026ndash;4 months COVID.\u0026rdquo; (201/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;In the last week of March 2020 there was mandatory leave and widespread panic which forced doctors and patients to stay at home. The number of neonates in the NICUs were reduced drastically in all the NICUs I visited initially\u0026rdquo; (150eS/LMIC)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec27\" class=\"Section3\"\u003e \u003ch2\u003eClosure of facilities\u003c/h2\u003e \u003cp\u003eEarly in the pandemic some government hospitals or their NICUs closed down, while others were converted to COVID hospitals. In some instances, staff were transferred from NICUs to care for patients with COVID. These factors had a major impact on all aspects of ROP services.\u003c/p\u003e \u003cp\u003e\u0026ldquo;So when the lockdown came the university closed\u0026hellip; this whole [ROP] service stopped\u0026rdquo; (11/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;Of the 17 services that I attended before the pandemic, three ended the activities of the NICU to accommodate COVID beds.\u0026rdquo; (179eS/UMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;We used to refer babies with Stage 4 and 5 (ROP) [for VR surgery]. However, the \u0026hellip;.institute \u0026hellip;was converted to a designated COVID hospital\u0026hellip;.\u0026rdquo; (102eS/LMIC)\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec28\" class=\"Section2\"\u003e \u003ch2\u003eStaff infection\u003c/h2\u003e \u003cp\u003eSickness amongst hospital staff also had a major impact on services in some settings.\u003c/p\u003e \u003cp\u003e\u0026ldquo;The other [maternity] hospital\u0026hellip;about 80% of [staff] caught COVID within a week. It was a Ministry of Health emergency - the whole hospital was closed down - all the patients were discharged.\u0026rdquo; (11/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;Screening stopped in one unit as several staff became infected and this led to closure. The kangaroo mother's room was closed, reducing numbers of babies screened drastically.\u0026rdquo; (11eS/LMIC)\u003c/p\u003e \u003cp\u003eCOVID infection amongst NICU staff meant that remaining staff were overworked and could not assist ROP screening.\u003c/p\u003e \u003cp\u003e\u0026ldquo;\u0026hellip;nurses just forgot to dilate the babies [pupils] because they were overwhelmed with so many babies..\u0026rdquo; (7/LMIC)\u003c/p\u003e \u003cp\u003eOphthalmologists also developed COVID. In one eye department, the screening ophthalmologist was the head of department. COVID infection amongst the residents because of inadequate PPE his focus was on keeping the eye department running.\u003c/p\u003e \u003cp\u003e \u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003eQuarantine and PCR testing.\u003c/span\u003e \u003c/p\u003e \u003cp\u003eHealth care professionals and parents sometimes had to go into quarantine after contact with an infected individual.\u003c/p\u003e \u003cp\u003e\u0026ldquo;One infant\u0026rsquo;s father's was detected with COVID the day before [VR] surgery and the whole family was quarantined\u0026hellip;.. for 17 days\u0026hellip;By the time they came back, it was inoperable.\u0026rdquo; (7 LMIC)\u003c/p\u003e \u003cp\u003eSeveral participants reported that later in the pandemic PCR testing was required, particularly before ROP treatment or VR surgery, which also caused delays.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec29\" class=\"Section2\"\u003e \u003ch2\u003eLack of public transport and travel restrictions\u003c/h2\u003e \u003cp\u003eLack of public transport and/or travel restrictions during lockdown had a major impact on NICU staff, ophthalmologists, and parents of infants who needed to be screened or treated after discharge. Several ophthalmologists were given passes/permission to travel within their city or district but could not travel further afield.\u003c/p\u003e \u003cp\u003e\u0026ldquo;Transport completely stopped. And we needed government passes to move\u0026hellip;.but patients were unable to reach the centre for screening.\u0026rdquo; (79/LMIC)\u003c/p\u003e \u003cp\u003e\u0026ldquo;\u0026hellip;inter-district travel was completely banned. And twice, our vehicle (for the screening team) was sent back by the police at the district border so there was nothing we could do.\u0026rdquo; (7/LMIC)\u003c/p\u003e \u003cp\u003eSeveral said that the cost of private transport was prohibitive for poor families.\u003c/p\u003e \u003cp\u003e\u0026ldquo;\u0026hellip;follow up was a very big challenge\u0026hellip;.Many of them could not afford [a taxi].\u0026rdquo; (34/LIC)\u003c/p\u003e \u003cp\u003eSome infants with Type 1 ROP could not move from one district to another for treatment.\u003c/p\u003e \u003cp\u003e\u0026ldquo;Babies referred from outside my city sometimes took longer to get to me\u0026hellip;.and some progressed to higher stages.\u0026rdquo; (20eS/LMIC)\u003c/p\u003e \u003cp\u003eOne participant gave a graphic account of the impact of the inter-district travel ban on access to treatment. In this setting, some ophthalmologists only screen for ROP and refer infants needing treatment to an ophthalmologist in another district. However, during the pandemic when local treatment was not available, some babies were treated by inexperienced ophthalmologists.\u003c/p\u003e \u003cp\u003e\u0026ldquo;There were a lot of incomplete treatments, late treatments who were coming to us with bad-looking ROP. In some we could just salvage one eye after treatment. It was like dealing with victims of war.\u0026rdquo; (48/LMIC)\u003c/p\u003e \u003cp\u003eSeveral African participants had only recently started ROP services. Because they did not have lasers, they used anti-VEGF treatment which often had to be sourced from overseas as these drugs were not on their Essential Drugs List. Restrictions on air travel made this even more difficult.\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003ePoorer quality neonatal care\u003c/h3\u003e\n\u003cp\u003eShortages of NICU staff, for whatever reason, led to worse nurse to baby ratios. Several participants observed poorer quality of care, particularly in oxygen administration.\u003c/p\u003e \u003cdiv id=\"Sec31\" class=\"Section2\"\u003e \u003ch2\u003ePoverty exacerbated\u003c/h2\u003e \u003cp\u003eDuring the pandemic people not formally employed or in non-essential jobs were particularly vulnerable to loss of income. This, combined with the need to pay for private transport, impacted parent\u0026rsquo;s ability to access treatment.\u003c/p\u003e \u003cp\u003e\u0026ldquo;Quite a few parents said they had lost their job or their income had reduced, and they could not afford treatment. Even if we said \u0026lsquo;treatment would be free, you just come\u0026rsquo;, they just didn't have money to come\u0026rdquo; (7/LMIC)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec32\" class=\"Section2\"\u003e \u003ch2\u003eChange in treatment\u003c/h2\u003e \u003cp\u003eSeveral ophthalmologists modified how they treated infants. Fear of COVID transmission during laser treatment meant that some used anti-VEGF agents instead, which is quicker. Some started using laser after anti-VEGF treatment as follow up after monotherapy could not be guaranteed.\u003c/p\u003e \u003cdiv id=\"Sec33\" class=\"Section3\"\u003e \u003ch2\u003e4. Resumption of services\u003c/h2\u003e \u003cp\u003eSeveral participants reported that ROP services had almost returned to normal. Others thought it would take longer, or would be difficult, as COVID vaccination was being prioritized by Ministries of Health and the backlog of ophthalmic outpatients hampered resumption of normal ROP services.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec34\" class=\"Section3\"\u003e \u003ch2\u003e5. Other comments\u003c/h2\u003e \u003cp\u003eSeveral ophthalmologists said that plans to expand ROP services stalled during 2020 as they could not travel to train, or the authorities were focusing on COVID. One participant commented on the advantages that telemedicine would have offered during the pandemic, as one trained individual could visit several NICUs.\u003c/p\u003e \u003cp\u003e Some reported positive impacts in relation to neonatal care, and in one country the screening guidelines were modified.\u003c/p\u003e \u003cp\u003e\u0026ldquo;[Nurses worked in] \u0026ldquo;bubbles\u0026rdquo;\u0026hellip;.We noticed we had less residents and observers and less sepsis cases. The units were quiet, no noise. Communication between the NICU teams was stronger.\u0026rdquo; (5/UMIC)\u003c/p\u003e \u003cp\u003e \u0026ldquo;We streamlined the screening [guidelines] and created a lot of awareness among people to take on ROP (services)\u0026hellip;. There's a lot of sharing of information now\u0026hellip;.\u0026rdquo; (48/LMIC)\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e"},{"header":"DISCUSSION","content":"\u003cp\u003eThe COVID pandemic affected health in many ways globally both directly and indirectly. Routine health services were often curtailed during lockdown, including surgery for congenital conditions.(\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e) We identified six studies on the impact on ROP services, from the USA,(\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e) India(\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e) and China.(\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e) Two described the mitigation measures adopted which allowed services to continue.(\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e) The other studies all report that fewer infants were screened during lockdown, with a variable impact on the number treated. This may reflect publication bias, as half of the eSurvey participants in our study reported no or only minimal impact on screening or treatment. Our study is the first to report that in some countries more preterm babies were likely to have gone blind from ROP because of the pandemic, but participants did not have data to support their statements.\u003c/p\u003e \u003cp\u003eFewer NICU admissions during lockdown were reported by many participants and in publications(\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e). This is likely to reflect fear and panic, COVID infection among staff, NICUs being converted to COVID care and travel restrictions. This may, in part, explain why some participants reported fewer infants needing treatment. However, several high-income countries and China have reported lower preterm birth rates during lockdown,(\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e, \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e, \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e) which has led to international collaborative research on interventions to prevent preterm birth.(\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e)\u003c/p\u003e \u003cp\u003eIn our study, the impact on screening was greater in government than in private hospitals, but differences were not statistically different, which may reflect the small sample size. Explanations given were that families accessing private neonatal care could afford to travel, neonatal staff were not transferred for COVID duties, and managers had greater autonomy to make changes. Differences between economic regions were more pronounced which may, in part, reflect the scarcity of ophthalmologists skilled in ROP, particularly in LICs in Africa.(\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e)\u003c/p\u003e \u003cp\u003eHalf of the participants were able to provide ROP services throughout lockdown despite PPE making this more difficult, which is testament to their commitment. Several mentioned the role of social media, which ensured continuity of care when screeners became sick, or were quarantining or vulnerable. Others thought that telemedicine would be advantageous, but there are considerable resource and infrastructure implications.(\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e)\u003c/p\u003e \u003cp\u003eSeveral ophthalmologists changed how they treated ROP during lockdown, which was influenced by lack of general anesthesia because anesthetists were either caring for COVID patients or they feared droplet transmission. Another factor was anxiety that infants treated with anti-VEGF would not return regularly for follow up. To address this challenge, some started routine laser a few weeks after anti-VEGF treatment.\u003c/p\u003e \u003cp\u003eSeveral African ophthalmologists said they routinely use anti-VEGF agents as lasers are not available,(\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e) but accessing the agents was often difficult during the pandemic. There is an urgent need to ensure that all treatment modalities for ROP are accessible and affordable. The impact on VR services is more difficult to interpret, as several participants referred infants for surgery before the pandemic and continued to do so during the pandemic.\u003c/p\u003e \u003cp\u003eIn MIC and LIC parents of preterm infants are often poorly educated and are poor, and compliance with outpatient screening and treatment is challenging even under normal circumstances.(\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e, \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e) Loss of income during the pandemic would have made compliance even more difficult, particularly for those in the informal labour market. The economic impact of the COVID pandemic on households and the ensuing recession(\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e) is likely to continue to affect access to health care, including for ROP services. Ensuring that ROP services are covered by health insurance would help to mitigate the economic burden on parents.\u003c/p\u003e \u003cp\u003eThere are several limitations in our study. Response rates to the eSurvey and interviews were low which may have introduced selection bias. Non-responders to the interview were not replaced, as no new themes emerged during the last few interviews. Almost half of those interviewed were known to the interviewer, which may have introduced bias, and including neonatal staff and parents would have given a more complete picture. Another limitation is that most ophthalmologists could not provide data on the number of infants screened or treated before and during the pandemic.\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eThis study has highlighted the limitations of ROP services in some locations, such as lack of lasers, and the limited number of ophthalmologists with skills to treat ROP, which accentuated the impact of the pandemic. The study also highlighted lack of pandemic preparedness, and how mitigation strategies were developed as the pandemic evolved. Ideally ROP screening and treatment should be included as an essential service in pandemic preparedness plans, as in India.(\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e) This might include adapting national ROP guidelines, advocating that infants requiring treatment be permitted to travel and developing networks of ROP service providers to maintain continuity of care.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cp\u003eeS\u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp;\u0026nbsp;eSurvey\u003c/p\u003e\n\u003cp\u003eLIC\u0026nbsp; \u0026nbsp; \u0026nbsp;\u0026nbsp;Low income country\u003c/p\u003e\n\u003cp\u003eLMIC\u0026nbsp;\u0026nbsp;Lower middle-income country\u003c/p\u003e\n\u003cp\u003eROP\u0026nbsp; \u0026nbsp;\u0026nbsp;Retinopathy of prematurity\u003c/p\u003e\n\u003cp\u003eNICU\u0026nbsp;\u0026nbsp;Neonatal intensive care unit\u003c/p\u003e\n\u003cp\u003eUMIC\u0026nbsp;\u0026nbsp;Upper middle-income country\u003c/p\u003e\n\u003cp\u003eVEGF\u0026nbsp;\u0026nbsp;Vascular endothelial factor\u003c/p\u003e\n\u003cp\u003eVR \u0026nbsp; \u0026nbsp; \u0026nbsp; Vitreoretinal\u0026nbsp;\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eFunding support \u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp;\u0026nbsp; \u003c/strong\u003eNone\u003c/p\u003e\n\u003ch3\u003eAuthor contribution statement\u003c/h3\u003e\n\u003cp\u003eClare Gilbert conceptualized and designed the study, collected and analyzed the data and wrote the first draft of the manuscript and takes responsibility for the intellectual content.\u003c/p\u003e\n\u003cp\u003eJoshua Todd assisted in data management and analysis and reviewed and revised the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData Sharing Statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eDeidentified individual participant data will not be made available.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eACKNOWLEDGEMENTS\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe thank all the participants for contributing to this study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest disclosure\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors have no conflicts of interest relevant to this article to disclose\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eBlencowe H, Lawn JE, Vazquez T, Fielder A, Gilbert C. Preterm-associated visual impairment and estimates of retinopathy of prematurity at regional and global levels for 2010. Pediatr Res. 2013;74 Suppl 1:35\u0026ndash;49.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eChan-Ling T, Gole GA, Quinn GE, Adamson SJ, Darlow BA. Pathophysiology, screening and treatment of ROP: A multi-disciplinary perspective. Prog Retin Eye Res. 2018;62:77\u0026ndash;119.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVinekar A, Gilbert C, Dogra M, Kurian M, Shainesh G, Shetty B, et al. The KIDROP model of combining strategies for providing retinopathy of prematurity screening in underserved areas in India using wide-field imaging, tele-medicine, non-physician graders and smart phone reporting. Indian J Ophthalmol. 2014;62(1):41\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePatil J, Patil L, Parachuri N, Kumar N, Bandello F, Kuppermann BD, et al. 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World Bank Country and Lending Groups. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://datahelpdesk.worldbank.org/knowledgebase/articles/906519-world-bank-country-and-lending-groups\u003c/span\u003e\u003cspan address=\"https://datahelpdesk.worldbank.org/knowledgebase/articles/906519-world-bank-country-and-lending-groups\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e. Accessed June 2022 [\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eEysenbach G. Improving the quality of Web surveys: the Checklist for Reporting Results of Internet E-Surveys (CHERRIES). J Med Internet Res. 2004;6(3):e34.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRossell-Perry P, Gavino-Gutierrez A. Cleft Lip and Palate Surgery during COVID-19 Pandemic. Plast Reconstr Surg Glob Open. 2021;9(6):e3692.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRangasamy K, Mehta R, Gopinathan NR, Aroojis A, Behera P, Dhillon MS. Changes in the Management of Clubfoot Cases During COVID-19 Pandemic-A Survey Among Orthopaedic Specialists. Indian J Orthop. 2021;55(1):188\u0026ndash;94.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMantagos IS, Wu C, Griffith JF, Jastrzembski BG, Gonzalez E, Goldstein S, et al. Retinopathy of prematurity screening and risk mitigation during the COVID-19 pandemic. J AAPOS. 2021;25(2):91 e1- e5.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKatoch D, Singh SR, Kumar P. Impact of the COVID-19 Pandemic on Retinopathy of Prematurity Practice: An Indian Perspective. Indian Pediatr. 2020;57(10):979\u0026ndash;80.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSarkar S, Kaur A, Gokhale T, Jossy A, Suneel S, Deb AK. Impact of COVID-19 pandemic on retinopathy of prematurity screening at a tertiary care center of South India. Indian J Ophthalmol. 2022;70(2):702\u0026ndash;3.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKaur R, Sachan A, Thukral A, Chandra P. Impact of COVID-19 pandemic lockdowns on retinopathy of prematurity services at a tertiary eye care center in India. Indian J Ophthalmol. 2021;69(10):2903\u0026ndash;4.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSahu SK, Mishra P. Challenge Accepted: Retinopathy of Prematurity (ROP) During COVID-19. Cureus. 2023;15(2):e35260.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGuo Z, Ma N, Wu Y, Yuan H, Luo W, Zeng L, et al. The safety and feasibility of the screening for retinopathy of prematurity assisted by telemedicine network during COVID-19 pandemic in Wuhan, China. BMC Ophthalmol. 2021;21(1):258.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBeen JV, Burgos Ochoa L, Bertens LCM, Schoenmakers S, Steegers EAP, Reiss IKM. Impact of COVID-19 mitigation measures on the incidence of preterm birth: a national quasi-experimental study. Lancet Public Health. 2020;5(11):e604-e11.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePhilip RK, Purtill H, Reidy E, Daly M, Imcha M, McGrath D, et al. Unprecedented reduction in births of very low birthweight (VLBW) and extremely low birthweight (ELBW) infants during the COVID-19 lockdown in Ireland: a 'natural experiment' allowing analysis of data from the prior two decades. BMJ Glob Health. 2020;5(9).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHedermann G, Hedley PL, Baekvad-Hansen M, Hjalgrim H, Rostgaard K, Poorisrisak P, et al. Danish premature birth rates during the COVID-19 lockdown. Arch Dis Child Fetal Neonatal Ed. 2021;106(1):93\u0026ndash;5.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBian Z, Qu X, Ying H, Liu X. Are COVID-19 mitigation measures reducing preterm birth rate in China? BMJ Glob Health. 2021;6(8).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eStock SJ, Zoega H, Brockway M, Mulholland RH, Miller JE, Been JV, et al. The international Perinatal Outcomes in the Pandemic (iPOP) study: protocol. Wellcome Open Res. 2021;6:21.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAdemola-Popoola DS, Fajolu IB, Gilbert C, Olusanya BA, Onakpoya OH, Ezisi CN, et al. Strengthening retinopathy of prematurity screening and treatment services in Nigeria: a case study of activities, challenges and outcomes 2017\u0026ndash;2020. BMJ Open Ophthalmol. 2021;6(1):e000645.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAl-Khaled T, Valikodath NG, Patel SN, Cole E, Chervinko M, Douglas CE, et al. Addressing the Third Epidemic of Retinopathy of Prematurity Through Telemedicine and Technology: A Systematic Review. J Pediatr Ophthalmol Strabismus. 2021;58(4):261\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eTaqui AM, Syed R, Chaudhry TA, Ahmad K, Salat MS. Retinopathy of prematurity: frequency and risk factors in a tertiary care hospital in Karachi, Pakistan. J Pak Med Assoc. 2008;58(4):186\u0026ndash;90.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVinekar A, Jayadev C, Mangalesh S, Kurian M, Dogra M, Bauer N, et al. Initiating Retinopathy of Prematurity Screening before Discharge from the Neonatal Care Unit: Effect on Enrolment in Rural India. Indian Pediatr. 2016;53 Suppl 2:S107-S11.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSumner AH, Chris; Ortiz-Juarez, Eduardo (2020): Estimates of the impact of COVID-19 on global poverty, WIDER Working Paper, No. 2020/43, ISBN 978-92-9256-800-9, The United Nations University World Institute for Development Economics Research (UNU-WIDER), Helsinki. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.35188/UNU-WIDER/2020/800-9\u003c/span\u003e\u003cspan address=\"10.35188/UNU-WIDER/2020/800-9\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSengupta S, Honavar SG, Sachdev MS, Sharma N, Kumar A, Ram J, et al. All India Ophthalmological Society - Indian Journal of Ophthalmology consensus statement on preferred practices during the COVID-19 pandemic. Indian J Ophthalmol. 2020;68(5):711\u0026ndash;24.\u003c/span\u003e\u003c/li\u003e \u003c/ol\u003e"},{"header":"Supplementary Table A","content":"\u003cp\u003eSupplementary Table A is not available with this version.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"eye","isNatureJournal":false,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"eye","sideBox":"Learn more about [Eye](http://www.nature.com/eye/)","snPcode":"41433","submissionUrl":"https://mts-eye.nature.com/cgi-bin/main.plex","title":"Eye","twitterHandle":"@eye_journal","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-3141875/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3141875/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003eBackground and objectives\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eRetinopathy of prematurity is an increasingly important cause of blindness children in low- and middle-income countries. Timely screening and treatment greatly reduce blindness. This study assessed the impact of the COVID-19 pandemic on ROP services in low- and middle-income countries.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMethods\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAn online survey with closed and open-ended questions in Microsoft Teams was sent to 304 ophthalmologists providing screening, treatment and/or vitreoretinal services(January 15 to March 12 2021). Categories were used to report impact on services. 28 participants were purposively selected for interview.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eResults\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e184/201 completed forms from 32 countries were received. Two thirds of participants worked in government facilities and 45.6% were pediatric ophthalmologists. A moderate to severe impact was reported by 13% for screening, 9% for treatment and 16% for vitreoretinal surgery with some variation between government, private and not-for-profit sectors. 22% thought services would take a year to recover. Fifteen ophthalmologists from 12 countries were interviewed. Many reported fewer neonatal admissions, and several reported more ROP blind infants once restrictions lifted. Themes associated with services continuing included limited lockdown, autonomy and flexibility, commitment, advocacy and technology. Themes associated with a negative impact include fear and panic, closure of facilities, COVID infection or quarantining of health workers and parents, lack of transport and exacerbation of poverty.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConclusions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe COVID pandemic had a very variable impact on the provision of ROP services. In some countries where the impact was great, more infants became blind from ROP. Lessons can be learnt for planning pandemic preparedness.\u003c/p\u003e","manuscriptTitle":"Impact of COVID-19 pandemic on retinopathy of prematurity services in low resource settings","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-08-02 16:29:34","doi":"10.21203/rs.3.rs-3141875/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"revise","date":"2023-09-27T08:19:03+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"This content is not available.","date":"2023-09-13T18:10:13+00:00","index":2,"fulltext":"This content is not available."},{"type":"reviewerAgreed","content":"This content is not available.","date":"2023-09-13T17:57:09+00:00","index":2,"fulltext":"This content is not available."},{"type":"editorInvitedReview","content":"This content is not available.","date":"2023-09-06T08:59:05+00:00","index":1,"fulltext":"This content is not available."},{"type":"reviewerAgreed","content":"This content is not available.","date":"2023-08-02T11:41:17+00:00","index":1,"fulltext":"This content is not available."},{"type":"reviewersInvited","content":"","date":"2023-07-27T16:59:15+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2023-07-13T09:09:28+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2023-07-13T09:08:48+00:00","index":"","fulltext":""},{"type":"submitted","content":"Eye","date":"2023-07-05T09:39:13+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"eye","isNatureJournal":false,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"eye","sideBox":"Learn more about [Eye](http://www.nature.com/eye/)","snPcode":"41433","submissionUrl":"https://mts-eye.nature.com/cgi-bin/main.plex","title":"Eye","twitterHandle":"@eye_journal","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"d6eda425-4423-4eba-944a-eec30488957d","owner":[],"postedDate":"August 2nd, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[{"id":23613916,"name":"Health sciences/Health care/Paediatrics"},{"id":23613917,"name":"Health sciences/Diseases/Eye diseases"}],"tags":[],"updatedAt":"2023-10-27T07:20:42+00:00","versionOfRecord":{"articleIdentity":"rs-3141875","link":"https://doi.org/10.1038/s41433-023-02784-6","journal":{"identity":"eye","isVorOnly":false,"title":"Eye"},"publishedOn":"2023-10-25 04:00:00","publishedOnDateReadable":"October 25th, 2023"},"versionCreatedAt":"2023-08-02 16:29:34","video":"","vorDoi":"10.1038/s41433-023-02784-6","vorDoiUrl":"https://doi.org/10.1038/s41433-023-02784-6","workflowStages":[]},"version":"v1","identity":"rs-3141875","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3141875","identity":"rs-3141875","version":["v1"]},"buildId":"FbvkV6FR0MCFSLy54lSbu","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}