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. 1A). However, differences were more pronounced between World Bank regions (Fig. 1B). 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)