key: cord-0943074-6ea1t94m
authors: Tan, Tien-En; Chodosh, James; McLeod, Stephen D.; Parke, David W.; Yeh, Steven; Wong, Tien Yin; Ting, Daniel Shu Wei
title: Global Trends in Ophthalmic Practices in Response to COVID-19
date: 2021-08-17
journal: Ophthalmology
DOI: 10.1016/j.ophtha.2021.07.027
sha: 7ac3ab1df5d541c87d70847eb720f37d441250fa
doc_id: 943074
cord_uid: 6ea1t94m

nan

It has now been more than 18 months since the first case of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection was reported in December 2019. The coronavirus disease 2019 (COVID-19) pandemic remains ongoing, with more than 150 million cases and 3 million deaths worldwide. 1 COVID-19 has had a significant impact on health care, the economy, and society.

Clearly, COVID-19 poses a significant risk to ophthalmologists and patients, and disrupts the routine delivery of ophthalmic care. The initial response to the pandemic involved the cessation of all nonurgent ophthalmic services; the American Academy of Ophthalmology released a statement recommending this on March 18, 2020. This temporary cessation was intended to preserve scarce personal protective equipment and to reduce the risk of transmission of the virus. As it became apparent that the pandemic was going to persist, along with the ever-present need to provide timely ophthalmic care for patients at risk of visual morbidity, the American Academy of Ophthalmology called for the careful and calibrated reopening of ophthalmic care approximately 1 month later. Around the world, most ophthalmic institutions followed similar patterns, with initial closures followed by careful reopening of services in subsequent months. At the time, some early reports of conjunctivitis occurring in COVID-19 infection appeared, and a few reports of SARS-CoV-2 RNA detected from ocular secretions of these patients also appeared. 2e4 This limited, but concerning, information on the potential risk of COVID-19 transmission via the eye, and the lack of clear consensus guidelines, resulted in a large variation in practice patterns among ophthalmic practices globally.

We published an editorial in May 2020 surveying risk mitigation strategies to prevent COVID-19 transmission in various ophthalmic practices around the world. 5 At the time, it was unclear how long the COVID-19 pandemic would last. More than one year later, it is clear that the pandemic will persist beyond 2021, but there have also been significant new developments in the fight against COVID-19. Therefore, we provide herein an updated review of practice patterns across a diversity of ophthalmic clinics and institutions globally, to better inform risk mitigation measures around the world.

The most significant development in the last year has been the successful development of effective vaccines against the virus. The BNT162b2 mRNA vaccine developed by Pfizer and BioNTech SE was the first vaccine against COVID-19 approved for emergency use by the Medicines and Healthcare Products Regulatory Agency in the United Kingdom on December 2, 2020, and by the Food and Drug Administration in the United States on December 11, 2020. 6 Multiple other vaccines against COVID-19 have been approved since for emergency use and are in use worldwide. To date, more than 1.4 billion doses of COVID-19 vaccines have been delivered worldwide. 1 Achieving widespread vaccination is seen as a key pillar in the overall strategy to combat the pandemic. 7 Nevertheless, the relative scarcity of COVID-19 vaccines and unequal access to vaccination programs have resulted in a significant geographic variation in population vaccination rates worldwide. Furthermore, local COVID-19 incidence and transmission are dependent on a multitude of factors, including vaccination rates, public health control measures, social distancing restrictions, and international travel patterns, along with other as-yet unknown factors. This has also led to a significant geographic variation in the incidence of COVID-19 in different countriesdwith numbers of new COVID-19 cases reported over 7 days per 100 000 population varying from 0 in some countries, to more than 1000 in others. 1 Therefore, health care systems in certain countries, such as India, recently were overwhelmed by surges in COVID-19 cases, resulting in widespread shortages in hospital beds and oxygen supply, whereas other countries, such as Israel, have (at the time of writing) returned primarily to non-COVID-19 patient care and are currently almost going about "business as usual." Nevertheless, even in countries with currently low levels of COVID-19 incidence, the possibility of resurgent waves of infection exists.

More recently, the emergence of new COVID-19 variants has threatened to derail some of the progress made toward gaining control over the pandemic. Some new COVID-19 variants are more transmissible, whereas early data suggest 

Ophthalmology Volume -, Number -, Month 2021 Editorial 7 that current vaccines may have minimally reduced rates of efficacy against these variants. 8, 9 The impact of these variants on ocular transmission remains unclear. Design of new vaccines and updates to current vaccines are thought to be important strategies to deal with emerging dominant variants, in addition to potentially achieving herd immunity.

Initial case reports of conjunctivitis occurring as a feature of COVID-19, and SARS-CoV-2 RNA being detected in ocular secretions, led to early recommendations for eye protection with goggles or shields for health care providers examining patients. 2, 3 Since then, larger series have confirmed that bilateral follicular conjunctivitis is the most common ocular manifestation of COVID-19, with isolated reports of other, much rarer, manifestations, including hemorrhagic or pseudomembranous conjunctivitis, keratitis, and retinal abnormalities. 10 Various published series have reported the prevalence of conjunctivitis in COVID-19, with a typical range being from 0% to 8%. 4, 11, 12 One study reported ocular involvement in 31.6% of COVID-19 patients, but this high prevalence rate is a far outlier and likely related to cohort selection, because the study included only hospitalized, mostly ill patients, without a corresponding control group. 13 A recent meta-analysis provided an overall prevalence estimate of 6.2% for conjunctivitis among patients with laboratory-confirmed COVID-19, although even this was skewed heavily by the aforementioned outlier. 14 The overall consensus from the existing literature is that ocular manifestations of COVID-19 are uncommon. 4, 11, 12, 14 In addition, only a small minority (estimated 2.7% in the same meta-analysis) of these patients will have detectable SARS-CoV-2 RNA in their ocular secretions. 11, 14, 15 Nevertheless, data that have emerged from multiple in vitro studies on conjunctival explants and postmortem tissues seem to demonstrate clearly that SARS-CoV-2 does exhibit tropism for tissues of the ocular surface and that the ocular surface is possibly a portal for entry and transmission of COVID-19. 16e18 Therefore, the American Academy of Ophthalmology continues to recommend the routine use of slit-lamp shields, as well as eye protection (goggles or shields) when examining patients "to the extent practical," acknowledging that wearing eye protection is not feasible during certain aspects of ophthalmoscopy and examination. 19 Guidelines published by other professional ophthalmic bodies such as the Asia Pacific Academy of Ophthalmology, the Spanish Society of Ophthalmology, and the All India Ophthalmological Society provide similar guidance. 20e25 However, it remains to be seen if these guidelines will be modified in future for clinicians and patients who are fully vaccinated.

Given the absence of overall consensus guidelines, we anticipated that significant heterogeneity and variation in COVID-19 mitigation measures remain among ophthalmic institutions worldwide. We also expected that the COVID-19 pandemic might have catalyzed the increased adoption of digital health solutions in ophthalmic practice, in efforts to reduce face-to-face consultations. Therefore, we set out to survey practice patterns for COVID-19 risk mitigation in a number of diverse ophthalmic practices, clinics, and institutions around the world. Members of the COVID-19 Ophthalmology Interest Group were surveyed via e-mail in May 2021 and were asked to detail the COVID-19 mitigation measures in their respective ophthalmic institutions in mid 2020 and to detail latest practice in 2021. A summary of these measures for 2020 and 2021 can be found in Tables 1 and 2, respectively. Recognizing that local factors such as COVID-19 incidence and vaccination rates are likely to influence the intensity of these measures significantly, the countries in Table 2 have been categorized into low-risk, moderate-risk, and high-risk locations based on the number of new COVID-19 cases reported over 7 days per 100 000 population from the World Health Organization COVID-19 Dashboard, which was accessed on May 23, 2021. 1 A number of trends in practice patterns were noted from 2020 to 2021. First, in general, a de-escalation of the initial COVID-19 mitigation measures seems to have occurred in 2021. In terms of personal protective equipment, most institutions that initially mandated the use of gloves, caps, and eye protection for ophthalmologists since have ceased this practice. This is likely because of the overall reduction in COVID-19 incidence compared with the peak of the pandemic in 2020. In certain institutions, eye protection is still recommended, but is not used frequently in practice because of difficulties with regard to examination. A number of institutions also have ceased routine temperature screening for both staff and patients. Second, despite an overall de-escalation, certain measures remain virtually universal. These include mandatory use of face masks for all staff, face masks for all patients (except for 1 center in Australia, which had very low levels of community transmission at the time of the survey), and use of slit-lamp shields, which are in line with current published professional guidance. 19e22,24,26 Third, vaccination of staff also seems to have been adopted universally, with almost all countries having prioritized vaccination for health care workers. However, vaccination levels of outpatients vary significantly based on availability and access in different countries. Finally, survey of practice in 2021 does seem to suggest increased adoption of digital health solutions. Furthermore, most centers that did adopt virtual clinics and digital home monitoring in their ophthalmic care for patients at the peak of the pandemic in 2020 do seem to have continued these practices into 2021, although the degree to which these digital health solutions are used is unclear.

In 2020, the COVID-19 pandemic necessitated drastic reductions in ophthalmic service delivery, with reductions of up to 70% to 99% seen in outpatient visits and elective surgical procedures. 27, 28 This forced reduction in traditional face-to-face consultations for provision of ophthalmic care accelerated the development and implementation of digital health solutions such as virtual consultations, artificial intelligence-enabled care, and digital home monitoring in many ophthalmic centers worldwide. 29 For example, virtual consultations were used successfully to triage and manage acute ophthalmic conditions during the height of the pandemic in London, United Kingdom. 30 Li et al 30 demonstrated that video consultations for emergency ophthalmic diseases could reduce effectively the subsequent need for traditional face-to-face review by 45%. More importantly, the video consultation method exhibited a safety profile (0% harm rate) equivalent to the face-to-face review, with perfect intergrader correlation and high patient satisfaction. In terms of home-based monitoring, Mansouri et al 31 used data from an ongoing multicenter study in Switzerland, Germany, and the United Kingdom to show that home-based monitoring of intraocular pressure in patients with glaucoma was feasible, impacted clinical decision-making such as adjustment of glaucoma medical therapy, and helped to avoid in-person consultations during the COVID-19 pandemic. Artificial intelligence algorithms have been shown to be powerful automated diagnostic tools for a wide range of anterior and posterior segment diseases in ophthalmology. Together with virtual consultations, artificial intelligence algorithms have immense potential as effective triaging tools in the COVID-19 pandemic as well as any other future widespread pandemics. 32e34 The COVID-19 pandemic clearly has provided an impetus for rapid implementation of digital health solutions in ophthalmology. We hope that these positive changes will continue to be used for better ophthalmic service delivery for our patients, even in the "new normal" of the COVID-19 aftermath. Collaborative efforts by ophthalmic institutions in the United States, United Kingdom, India, and Singapore are ongoing to develop a global interinstitutional teleophthalmology program to share best practices, new technical innovations, and regulatory approaches to teleophthalmology. Nevertheless, significant barriers to more widespread adoption of digital health solutions remain, including technology access and country-specific payment or reimbursement mechanisms. Furthermore, the large variety of emerging digital health solutions available to us necessitates some clear guidance in the near future to determine which types of digital solutions are most appropriate for which kinds of ophthalmic visits in the aftermath of the pandemic, or in the next widespread public emergency.

In conclusion, despite the development of effective vaccines, better understanding of the relationship between COVID-19 and the eye, and the implementation of digital health solutions in ophthalmology, significant challenges lie ahead of us. Inequalities in vaccine access, the threat of resurgent waves of infection, and the emerging new variants are some of the ongoing challenges that ophthalmology practices will face in the second year of this pandemic. With greater international collaboration, sharing of best practices, and a continued push toward innovation in ophthalmic care delivery, we can continue to provide the highest quality ophthalmic care for our patients, whilst also safely mitigating the risks relating to COVID-19.

Jost B. Jonas (Department of Ophthalmology

The authors also thank the following, who have contributed valuable content to the section on digital health solutions in ophthalmology: Ranya Habash

References 1. World Health Organization. WHO coronavirus (COVID-19) dashboard

Evaluation of coronavirus in tears and conjunctival secretions of patients with SARS-CoV-2 infection

Ocular manifestations of a hospitalised patient with confirmed 2019 novel coronavirus disease

Clinical characteristics of coronavirus disease 2019 in China

Preparedness among Ophthalmologists: during and beyond the COVID-19 pandemic

Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine

World Health Organization. COVID-19 strategic preparedness and response plan

Novel SARS-CoV-2 variants: the pandemics within the pandemic

National Study Group for COVID-19 Vaccination. Effectiveness of the BNT162b2 Covid-19 vaccine against the B.1.1.7 and B.1.351 variants

An update on COVID-19 related ophthalmic manifestations

Coronavirus disease 2019 (SARS-CoV-2) and colonization of ocular tissues and secretions: a systematic review

Ocular findings and proportion with conjunctival SARS-COV-2 in COVID-19 patients

Characteristics of ocular findings of patients with coronavirus disease 2019 (COVID-19

An eye on COVID-19: a meta-analysis of positive conjunctival reverse transcriptase-polymerase chain reaction and SARS-CoV-2 conjunctivitis prevalence

The presence of SARS-CoV-2 in conjunctival secretions of COVID-19 patients

replication competence, and innate immune responses of the coronavirus SARS-CoV-2 in human respiratory tract and conjunctiva: an analysis in ex-vivo and in-vitro cultures

Co-expression of SARS-CoV-2 entry genes in the superficial adult human conjunctival, limbal and corneal epithelium suggests an additional route of entry via the ocular surface

SARS-CoV-2 infects human adult donor eyes and hESC-derived ocular epithelium

Important coronavirus updates for ophthalmologists

COVID-19: ocular manifestations and the APAO prevention guidelines for ophthalmic practices

Recommendations for ophthalmologic practice during the easing of COVID-19 control measures

All India Ophthalmological SocietydIndian Journal of Ophthalmology consensus statement on preferred practices during the COVID-19 pandemic

The use of personal protective equipment in clinical ophthalmology during corona virus disease-2019: a review of international guidelines and literature

COVID-19: special precautions in ophthalmic practice and FAQs on personal protection and mask selection

Evolving practice patterns in Singapore's public sector ophthalmology centers during the COVID-19 pandemic

Considerations in the use of slit lamp shields to reduce the risk of respiratory virus transmission in coronavirus disease 2019

The impact of COVID-19 pandemic on ophthalmology services: are we ready for the aftermath?

To evaluate the effect of COVID-19 pandemic and national lockdown on patient care at a tertiary-care ophthalmology institute

Teleophthalmology: an essential tool in the era of the novel coronavirus 2019

Safety of video-based telemedicine compared to in-person triage in emergency ophthalmology during COVID-19

Intraocular pressure telemetry for managing glaucoma during the COVID-19 pandemic. Ophthalmol Glaucoma

New digital models of care in ophthalmology, during and beyond the COVID-19 pandemic

Big data in ophthalmology

Deployment of artificial intelligence in real-world practice: opportunity and challenge

The authors thank the following, who have contributed information on practice patterns at their respective eye institutions from 2020 and 2021: Massimo Busin (Ospedali Privati Forlì "Villa Igea," 

Disclosure(s): All authors have completed and submitted the ICMJE disclosures form.Stephen D. McLeod, the Editor-in-Chief of this journal, was recused from the peer-review process of this article and had no access to information regarding its peer-review.Daniel Shu Wei Ting, an editorial board member of this journal, was recused from the peer-review process of this article and had no access to information regarding its peer-review.