The COVID-19 global pandemic, caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), presents unique challenges to the practice of ophthalmology. Ophthalmologists routinely work in high-volume, office-based settings in close proximity to patients, which puts them at increased risk of exposure to respiratory viruses. While ophthalmologists, like many providers, rapidly transitioned to offering care through video- and phone-based telehealth visits, many patients still require in-person evaluation and management to maintain their sight, even during a pandemic.

This article describes modifications our practice adopted to enhance safety in eye-care delivery in the COVID-19 era. The strategies we implemented are based on Centers for Disease Control and Prevention (CDC) and AAO guidelines, as well as on primary scientific and industry sources. These changes to our practice are likely to be maintained as an enhanced standard-of-care, even after a vaccine or other solution to the SARS-CoV-2 virus emerges.

Social distancing in eye care

SARS-CoV-2 is a novel coronavirus passed primarily through respiratory droplets.¹ Transmission is enhanced by talking, sneezing, or coughing, and the virus is often spread by individuals before the manifestation of symptoms or by asymptomatic carriers.² Though the virus mainly travels in airborne droplets, contact transmission through the eyes, nose, and mouth may also occur.¹ Spread of COVID-19, like other respiratory viruses, has been shown to decrease when people physically distance themselves from others.³ Implementing “social distancing” during the COVID-19 pandemic has led to a reduction in the reproduction rate of the virus in populations, leading to both delayed and reduced peaks.⁴ Three strategies for social distancing in eye care are to reduce the number of in-person patient appointments, to transition to telehealth consultation when appropriate and to reconfigure the clinic to make possible physical distancing.

On March 16, 2020, Massachusetts issued a stay-at-home order to control the spread of the virus. The United States has been heavily impacted by the novel coronavirus and has suffered the greatest number of COVID-19-related cases and deaths worldwide.⁵ Among the states, Massachusetts is a COVID-19 hot spot with the third highest mortality and cases per capita at the time of this article.^5,6 On March 18, 2020, two days after the Massachusetts stay-at-home order was issued, the AAO issued a guidance that advised: "Due to the COVID-19 pandemic, the American Academy of Ophthalmology now finds it essential that all ophthalmologists cease providing any treatment other than urgent or emergent care immediately".⁷ Maintaining only emergency and urgent visits, including those for patients with conditions that required time-sensitive and necessary in-person management, led to an 86.5% reduction in our in-clinic volume within the first 6 weeks following the Massachusetts stay-at-home order in comparison with the preceding 6 weeks (Figure 1A). The prioritization of urgent and emergent visits led to a shift in care delivery in our clinic, with a steep reduction in service provision by the optometry service and a relative increase in the percentage of patients managed by the retina service (Figure 1B). After this transition, 86% of retina encounters involved the intravitreal injection of medications, which was a greater than 50% increase over the preceding 6 weeks. At the same time, a 90% decline in imaging occurred in an effort to streamline injection visits.

During this reconfiguration of the clinic, office-based staffing was adjusted to match the reduction in total number of in-person services delivered, and providers were instructed to work from their offices or offsite to reduce clinic density and allow for increased physical distancing. Providers and staff were grouped and rotated in separate weekly teams to limit the number of individuals potentially exposed to COVID-19 in any given week. The teams included our physicians, optometrists, technicians and administrative staff. This division of available staff reduced the risk of having an entire cross-section of our critical workforce incapacitated by a single spreading event or exposure that would require quarantining.

Next, we implemented telehealth visits whenever feasible to replace traditional in-person visits (Table). This transition took place rapidly over the course of a 2-week period, with telehealth visits comprising more than 75% of all appointments (Figure 1B) and eclipsing the number of in-person encounters during the first 6 weeks after implementation of COVID-19 practice modifications. Patients were scheduled for telehealth visits based on the reason for their visit as reviewed by their assigned eye-care provider. These patients were contacted by staff to ensure that they did not unnecessarily present to clinic and to confirm their availability and willingness to have a telehealth consultation. Staff also determined the patients’ preferred method of contact, such as video conference or telephone. When patients could not be reached until the day of their scheduled appointment, the providers themselves called patients to offer eye care and to check on their well-being. For patients seeking unscheduled eye care, our clinic established an onsite “doctor of the day” responsible for triage of both new and existing patients with eye issues. In some cases, telehealth visits were converted to same-day, in-office examinations; others were scheduled for in-person follow-up appointments based on the patients’ needs.

Another important step to promote physical distancing was the reconfiguration of our waiting rooms. Safety measures added in the waiting rooms included the spacing of seating 6 feet apart and facing in opposite directions. Patient access to hand sanitizer was also increased by placing alcohol-based sanitizer bottles prominently throughout the clinic, including at check-in, in the waiting room areas, and anywhere patients or staff might need them (Table). During this period, visitors were not allowed in the hospital. Similarly, our hospital-based eye clinic only allowed individuals to accompany patients to the clinic if the patient had a special need, such as a physical limitation, language barrier, or a requirement for a healthcare proxy or assistant to be present. This measure significantly reduced the clinic population density without restricting patient visits that would otherwise be unable to take place without these critical supports. Finally, access to the confined space of the eye exam room itself was limited to only the patient and the care provider. Any individuals who accompanied a patient were asked to wait in the main waiting room whenever possible. This reduced density within the exam rooms to one provider and one patient for most appointments. Providers also limited the role of scribes within the practice, often removing them from face-to-face roles in the provision of eye care.

Protective barriers and equipment

The eye exam, along with ophthalmic testing and procedures, often requires close physical proximity to the head and neck of the patient, far closer than physical distancing guidelines recommend. Given that the SARS-CoV-2 virus can be found in conjunctival secretions and tears,⁸ routine eye examinations pose a risk for transmission. Furthermore, patients with COVID-19 may first present to ophthalmology, especially if they have a COVID-19-related conjunctivitis, a sign found in less than 1% of patients⁹ but believed to be more common in severe cases.¹⁰

Given that physical distancing cannot be maintained during all portions of the ophthalmic encounter, especially the eye exam, measures to mitigate risk of transmission were put into place. One of the most important strategies is the use of masks. Providers and staff are required to wear surgical masks at all times in our facility (Table). Evidence suggests that mask wearing can prevent illness by preventing asymptomatic transmission and thereby decreasing infection rates.¹¹ Patients are allowed to bring their own masks, and those who do not have their own face coverings are given a paper surgical or cone mask at no cost. In addition, for high-risk patients defined as those with a positive COVID-19 test, recent COVID-19 exposure, or positive symptom screen (Table), our providers wear N95 respirators for additional protection. This is in keeping with AAO guidelines, which recommend N95 utilization for providers under circumstances with increased aerosol risk, such as during operations requiring intubation or during an encounter with a patient who is COVID-19 positive.¹² This differs from the Joint Commission statement that surgical masks are an acceptable alternative to respirators when seeing a patient who is either COVID-19 positive or suspected and when no procedures with increased aerosol risk are performed.¹³

Standard protective equipment also includes eye protection comprising a face shield or goggles. COVID-19 droplets can be spread through contact with mucous membranes of the eyes, passing through the nasolacrimal ducts into the respiratory tract to cause infection. Though the incidence of COVID-19 spread through the eye is likely to be extremely low, it still presents a risk to healthcare workers.³ Eye protection decreases this risk.¹⁴ Since eye protection can make it difficult to carry out some portions of an eye exam, protective barriers attached to standard ophthalmic equipment provide a means of mitigating the risk of transmission. We also have fitted custom-designed breath shields to our tower slit lamps (Figure 2A) and indirect ophthalmoscopes (Figure 2B) and attached commercially available barriers to our imaging systems and YAG lasers. Plastic barriers have also been put in place to shield front desk staff. Use of barriers has been endorsed by the AAO¹² as well as by the CDC.¹⁵ A recent study showed that at least 46% of overspray from a simulated sneeze could be blocked by a conventional slit lamp shield.¹⁶

In addition to these mandated strategies, many providers have also chosen to decrease the risk of transmission from work to home by applying additional measures modeled on precautions taken in our operating rooms. Though not required, providers have elected to wear scrubs or a separate set of clothes and shoes in the clinic. Often these are changed before leaving work, and most providers shower immediately upon arriving home. Use of jewelry such as watches and rings that may impede hand washing have been reduced. Several providers have also reported discontinuing contact lenses in favor of glasses for the perceived benefit of an additional barrier. Finally, sharing of food and beverage has been discouraged, and shared coffee service and water dispensers have been removed. Other non-essential common area items that are frequently handled and difficult to sanitize, such as reading materials, have also been eliminated (Table). Though the benefits of these environmental changes are not known at this time, it is important to promote a culture of safety.

Changes in the clinical encounter

Many changes were also made to the efficiency of clinical encounters and eye examinations after the advent of COVID-19. In addition to decreasing population density within clinic by prioritizing urgent and emergent conditions as discussed above, improving the efficiency of patient flow allowed for shorter, often non-overlapping appointments. Contactless check-in improved the efficiency of registration and reduced time spent in common areas, such as waiting rooms (Table). Some patients with cell phones chose to wait in their cars until called at their appointment time or when the clinic was ready for them. In the future, we plan to implement electronic messaging, both through the EMR and text messaging, to refine patient flow further (Table).

Next, patients are generally kept in one exam room to reduce the total number of steps in clinic and the number of surfaces potentially touched that need cleaning after a visit. This also helps to maintain physical spacing and means that patients spend little to no time in common waiting areas. To reduce face-to-face time, technicians and providers are encouraged to review charts and related testing ahead of time and outside of the exam room. Charting is done apart from the patient and is often completed after the encounter. Additional steps to improve efficiency during a visit include setting up the slit lamp and other equipment before moving in close to a patient. Patients are reminded not to speak during the physical examination, thereby decreasing a likely route of COVID-19 transmission¹⁷ while doctors and patients are in close proximity. Finally, patient education and discussion are deferred until after examination. When more detailed patient instruction or education is required, additional conversations can be done remotely by telephone or electronic communication after the clinic visit has concluded to limit face-to-face discussion in the clinic. Finally, since social distancing and isolation have put a strain on many patients and a visit to the eye clinic may be the only social interaction for some individuals, one thing that we have not curtailed is screening for depression, anxiety and domestic violence.

Results

These steps profoundly reduced the average length of visit. In our hospital-based eye clinic, the average length of a visit from the time of appointment check-in to the time of appointment completion dropped from 80 minutes to 53 minutes (p<0.001). Some visits, such as checks of eye pressure, took as few as 4 minutes; others, like retinal detachments requiring surgical intervention, took more than 4 hours. The retina clinic reduced the average patient visit length by 55% from 105 to 47 minutes (p<0.001), and most visits for intravitreal injections took fewer than 40 minutes.

This enhanced throughput is primarily due to the streamlining of the clinic visit. Appropriate history and physical examination were performed in each encounter, but ancillary testing was deferred as far as possible to streamline the visits. During this period, the proportion of patients undergoing imaging fell from 82% to 24% (p<0.001). Even greater reductions were noted for visual fields and other specialty testing. The average time from check-in to image completion for all imaging declined by 45% from 57 to 31 minutes (p<0.01). Additionally, average check-in to technician time was reduced by 79% from 19 to 4 minutes (p<0.001), and check-in to provider time was also reduced by 63% from 81 to 30 minutes (p<0.01). With our increased efficiency, patients spent less total time in the clinic as a whole and decreased their time in common areas. This allowed us to adhere to physical distancing guidelines and to decrease patient density in close clinical spaces.

Patient communication and expectations

An important part of adapting ophthalmology practices to measures against COVID-19 is educating both patients and staff about standards that are in place and what changes to expect during a clinic visit. As previously mentioned, patients are contacted by phone ahead of their visit to confirm the day, time, provider, and appointment type (telehealth vs. in-person). During these calls, patients are screened with symptom-based questions by phone and reminded to call and cancel if they start to develop any COVID symptoms (Table). The CDC and AAO both recommend symptom-based screening to prevent initial contact with infected patients or staff.^12,15 Patients are asked these screening questions again when they check into the clinic, and their EMR is reviewed for COVID-19 exposures or historical testing on the day of their visit. Similarly, every day before reporting to work, both providers and staff must respond to a series of screening questions by means of a web- or text-based tool (Table). Anyone reporting one or more positive symptoms, or a known COVID-19 exposure, is required to be cleared by the employee health service before reporting to work.

In the clinic, we continue to practice previously established hospital cleaning and disinfection protocols (Table), and we have improved upon communicating these precautionary measures to patients. Patients are made aware of the successful completion of cleaning protocols even when they are not present to witness the activity. For hand hygiene, providers are required to sanitize with either 20 seconds of soap and water or alcohol-based sanitizer immediately before entering and after exiting the exam room, when transferring from computer to patient exam or vice versa, and immediately after making contact with a patient. Sanitizer has been placed in every exam room near the patient to facilitate this protocol without interfering with the flow of the exam.

COVID-19 public health posters have been placed in elevators, waiting rooms, and bathrooms to increase awareness of the importance of disinfection and proper hand washing technique. Provider and staff education have also been increased. Virtual meetings and information updates have been implemented with their frequency adjusting as needed to keep up with a pandemic in flux. Team meetings, or “provider huddles,” occur two to three times per week, or more often as needed, by video chat or phone. These allow our providers to obtain updates and learn about new protocols as well as to ask questions, share difficulties and successes, and make suggestions regarding COVID-19 clinical flow. Protocol changes are sent out by email and posted on a central information board so that staff can refer to these directives during the workday. Asynchronous communications are designed to meet the needs of staff variably scheduled or on different rotations. Small group breakout and training sessions are also done through video conferencing. This allows for visual learning without the risks associated with physical contact.

COVID patients

At times, it is necessary to examine a patient who has tested positive for COVID-19, or is awaiting the results of a COVID-19 test, or is at an increased risk for COVID-19 based on screening or a known exposure. Additional precautions beyond those stated previously are taken with these patients since there may be an increased risk of transmission. These patients are issued surgical masks to wear during the entire visit, a measure recommended by the AAO since cloth masks are less effective at preventing respiratory droplet spread.³ Upon arrival at the clinic, patients in these categories are separated from the general patient population and immediately seated in our largest exam room to promote air exchange (Table). These patients are not examined by technicians, and providers are asked to start their visits as soon as possible to reduce the amount of time that patients are in the clinic. Providers in direct contact with the patient wear N95 respirators and gowns, since the close proximity of ophthalmology exams classifies these visits as higher risk for transmission. Providers also wear additional eye protection with goggles and face shields (Table). After patients leave this exam room, it remains unoccupied for 2 hours per Lahey Environmental Services protocol and is cleaned per protocol before another COVID-19 positive or suspected positive patient can be brought into that room.

Future considerations to decrease transmission risk that are not currently used within our clinic include increased ventilation and humidity as well as portable UV radiation units to kill the virus.^18,19 Ventilation is an important part of infection control with minimum standards²⁰ overseen by The Joint Commission and regulated at Lahey by Environmental Services. Portable HEPA filters can extend capacity by providing additional isolation rooms when hospital capacity is exceeded.²¹ They are one of the more promising ways to address ventilation within the eye clinic.

Conclusion

The advent of COVID-19 has presented a fluid and quickly changing landscape with new information about the virus emerging almost daily. Ophthalmology practice has adapted quickly to the challenges of the pandemic and has taken the steps necessary to enhance safety in eye-care delivery. We have maintained urgent and emergent visits throughout this pandemic. However, many patients, including those with eye conditions considered “routine,” are still in need of eye care, which cannot be postponed indefinitely. Increasing clinic volume to meet the need of in-person examinations will require additional innovations.

For the most up-to-date ophthalmology-related practice and surgical guidelines visit the AAO website (https://www.aao.org/headline/special-considerations-ophthalmic-surgry-during-c .). For the most current information on COVID-19, visit the websites of the CDC (https://www.cdc.gov/coronavirus/2019-ncov/index.html ) and the World Health Organization (https://www.who.int/emergencies/diseases/novel-coronavirus-2019 ).For the most up-to-date COVID safety practices at Beth Israel Lahey Health please visit our BILH Safe Care website (https://www.bilh.org/safecare ). OM

This paper is dedicated to the memory of Richard P. Mills, MD, MPH, past president of the AAO, and to all physicians who have been impacted by the COVID-19 pandemic.

The authors thank Dr. Fina Barouch, Timothy. B. Tivnan, Ed. Momplaisir, as well as Carol Spencer, Lahey Hospital Librarian, for research support. 

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About the Authors

Jonah Goldblatt is a senior medical student in the Tufts University School of Medicine.

Shiyoung Roh, MD, is chair of the Division of Ophthalmology at Lahey Hospital and Medical Center and an associate clinical professor of ophthalmology at Tufts University School of Medicine.

Karan Sethi is a senior medical student in the Tufts University School of Medicine.

David J. Ramsey, MD, PhD, MPH, is director of ophthalmic research and the Harry N. Lee Family Chair in Innovation at Lahey Hospital and Medical Center. He is also an assistant clinical professor of ophthalmology at Tufts University School of Medicine. Email him at David.J.Ramsey@Lahey.org

The authors report no relevant disclosures. Financial Support: D.J.R.: Supported by the Harry N. Lee Family Chair in Innovation at the Lahey Hospital & Medical Center, Beth Israel Lahey Health.