key: cord-0837908-a9r6lvv5
authors: Chung, Y. Grace; Person, Christie M.; O’Banion, Jacquelyn; Primo, Susan A.
title: COVID-19 Related Health Disparities in Ophthalmology with a Retrospective Analysis at a Large Academic Public Hospital
date: 2022-04-22
journal: Adv Ophthalmol Optom
DOI: 10.1016/j.yaoo.2022.04.005
sha: f7d073f9afd5e6f6c9237ac7f2e43da7569b01fb
doc_id: 837908
cord_uid: a9r6lvv5

The COVID-19 pandemic has disproportionately affected racial and ethnic minorities in the United States, especially Black, Latinx and Native American communities. While recent meta-analyses have identified the prevalence of ocular manifestations in COVID-19 infection, no studies with these potential findings, to the authors’ knowledge, have been implemented in examining ophthalmic disparities in racial and ethnic minorities. It is additionally clear that patient access to eye care from COVID-19 has been disproportionate in underserved communities. Large public hospitals and urban academic medical centers provide a unique opportunity to further study ocular disease presentation and health disparities from COVID-19 in these populations.

Initially detected and identified in Wuhan, China in late 2019, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has rapidly progressed to the Coronavirus disease 2019 pandemic, officially declared on March 22, 2020. 1 The severity of this disease has had devastating fatality rates globally 2 and has had an extensive range of presentations, not solely limited to the respiratory system. 3 Asymptomatic transmission of the virus was discovered early on with ophthalmic care being limited in most practices across the world to primarily emergency services, particularly due to the close physical proximity needed to properly conduct a diagnostic eye examination. [4] [5] [6] Ultimately, ocular manifestations were found to be prevalent among COVID-19 patients, most commonly dry eye or foreign body sensation, redness, tearing, itching, eye pain, and discharge. 7 These manifestations may be the initial symptoms of a COVID-19 infection; greater understanding of COVID-19 related ocular signs may lead to earlier diagnosis and improved ophthalmic care. 8 COVID-19 has disproportionately affected racial and ethnic minority groups, specifically resulting in much higher rates of death from disease in Black, Latinx, and Native American communities. 9 Alongside the impact of COVID-19 on patients, the pandemic has drastically impacted healthcare delivery, particularly at the beginning of the pandemic, with an increase in the use of telemedicine and a large decline in outpatient visits. [10] [11] [12] While access to telemedicine had been shown to alleviate the disruptions in outpatient care 13, 14 , racial and socioeconomic J o u r n a l P r e -p r o o f disparities have been prevalent in patient engagement to telemedicine and in outpatient visits, disproportionately affecting Black, Latinx, and Native American ethnic groups and patients with fewer socioeconomic resources. [15] [16] [17] [18] [19] These disparities in access to telemedicine have also been studied specifically within ophthalmology. 20 In one study, Black patients were less likely to be seen in a retina clinic, despite no increase in telemedicine visits. 21 Even with the disproportionate impact on Black, Latinx, and Native American populations of COVID-19, ophthalmic manifestations of this virus have not specifically been studied in these communities. Large public hospitals may serve as a unique opportunity to study COVID-19 ocular disease presentation in underrepresented minorities. To further elucidate the effects of COVID-19 on patient demographics and health disparities in ophthalmology, the authors performed an analysis of patient demographics and ocular findings among COVID-19 positive patients at a public academic tertiary healthcare center primarily serving underserved populations during the height of the first wave of the COVID-19 pandemic. A retrospective chart review of ambulatory ophthalmology outpatient visits, as well as inpatient consultations, during this initial surge of the virus was undertaken as there is a dearth of research of COVID-19 related ocular manifestations in underserved populations to better define its impact on currently present health disparities.

COVID-19 has disproportionately impacted all minority racial and ethnic groups, including Black, Latinx, Asian, Native Hawaiian and Pacific Islanders, and American Indian and Alaska Native communities in both infection and mortality rates. 22 A systematic review found Black and Latinx individuals also disproportionately have higher rates of hospitalization with moderate to high-strength evidence. 23 Most studies attribute poverty, low household income, housing insecurity, education level, and language barriers as risk factors for higher rates of infection, death, and hospitalization. 23 With multivariable analyses, the excess burden of COVID-19

infections is not fully explained by other variables, such as underlying comorbidities and socioeconomic factors. 24 Other studies also have identified higher rates of infection for Black and Latinx patients compared to White patients; however, once hospitalized, lower rates of J o u r n a l P r e -p r o o f critical illness and death, indicating the presence of previously known existing structural barriers in accessing care. 25 These disparities are compounded by racial and ethnic minority communities also experiencing lower vaccination rates; Black and Latinx vaccination rates were shown to be approximately 2.1 and 2.9 times lower, respectively, compared to non-Hispanic White population across the U.S. 26 Lower vaccination rates are not fully attributable to vaccine hesitancy from mistrust resulting from systemic injustices, but rather underlying structural inequities and vaccine accessibility are major contributing factors. 27 Moreover, Black and Latinx populations are underrepresented in vaccine clinical trials and for COVID-19 treatment trials. 28, 29 

Barriers to care exist for underserved patients and racial and ethnic minorities particularly around the constructs of social determinants of health. Factors like cost, transportation, language, and health literacy, to name a few, remain as barriers in normal times, only to be magnified during times of medical crisis, like the COVID-19 pandemic. Eye care delivery is no exception and although alternative methods of evaluation have been attempted, such as telemedicine, missed clinic visits have dramatically increased among elderly and nonwhite patients 12 , particularly in the first wave of the pandemic. Timely interventions for ophthalmic diseases like diabetic retinopathy and macular degeneration can stave off preventable vision loss whereas glaucoma requires continuous monitoring in most cases. Generally speaking, deviation and delay in eye care can be both tragic and insurmountable when urgent ocular diseases either are not identified or when chronic ones miss periodic and appropriate follow up.

Many and most medical disciplines have been able to pivot to telemedicine through incorporating virtual, video and/or phone visits into their daily practices. 30 Innovative hybrid care has allowed for medication check ins, follow ups and even diagnostic capabilities in many instances leading to improved compliance and continuity of care. Those specialties that are technology driven have been able to order tests, scans, images, etc. allowing patients to get the procedure and then have consultation with their provider regarding the results and management.

In many cases, patients can defer in-person care particularly if anxious about physically visiting health care facilities.

For ophthalmological care, while technology driven in many instances, face-to-ace in-person visit is needed to accurately measure and monitor things like vision and eye pressure, although innovative solutions have been proposed and implemented even circumventing the need for the traditional delivery model. 31 However, treatment for retinal diseases such as diabetic retinopathy and age-related macular degeneration rely on periodic intravitreal injections with the significant potential of vision loss if delayed. 32 Retina and glaucoma also require the use of specialized equipment that limit telemedicine use. A study found during COVID-19, cataracts saw greater than 60% reduction in visits with only approximately 1% telemedicine use; glaucoma saw over 50% reduction in visits with only approximately 3% telemedicine use. 30 Telemedicine remains a less prevalent form of delivering eye care in most facilities unlike other areas of medicine and has significant limitations. Sudden painful or painless loss of vision especially in monocular patients, new cases of retinal tumors or cancers, retinopathy of prematurity, recent surgical patients and more all require physical examination of the eye. 33 Ophthalmic disparities will prevail when barriers to care from social determinants of health exist.

The ocular findings associated with COVID-19 are varied and have affected both anterior and posterior structures of the eye. A meta-analysis of 38 studies found that the most common diagnoses from December 2019 through August 2020 were foreign body sensation, redness, tearing, itching, eye pain, and discharge. 7 Another meta-analysis of 20 studies determined that one of the earliest ocular symptoms associated with COVID-19 is viral conjunctivitis and is associated with more severe disease, requiring hospitalization. 34 Microvascular alterations were also noted in the SERPICO-19 study, which cited findings of retinal hemorrhages, cotton wool spots, dilated veins, and tortuous vessels in patients with COVID-19. 35 The most common ICD-10 diagnosis for ambulatory and inpatients were examined (Tables 2   and Table 3 ) with age-related nuclear cataracts, presbyopia, and type 2 diabetes mellitus with ophthalmic complications being the most common for ambulatory patients and viral pneumonia, severe sepsis, and mixed disorder of acid-base balance being the most common for inpatients. COVID-19 should be suspected in any patient who presents with retinal vaso-occlusion, but without known vascular disease risk factors as vasculitis in COVID-19 patients has been identified in the lung, liver, kidney, and skin. 40 A study done in a medical center with similar demographics during the same time period revealed that patients who tested positive for COVID-19 had outcomes comparable to their White counterparts when controlled for age, sex, and co-morbidities. 41 A more recent study found that Black inpatients had a higher mortality rate than White patients, which was due to the different hospitals where each group of patients was admitted. This study adjusted for age, sex, income, and comorbidities. It also included a much larger and more diverse patient sample of 44,217 compared to 5,902 in the earlier study. 42 When reviewing hospitalized patients within our patient population, the two most prevalent in-patient diagnoses include viral pneumonia (60%) and severe sepsis (50%). A similar study at Oschner Health in New Orleans from March to April 2020 reported that a diagnosis of pneumonia along with a co-infection of hypoxic respiratory failure were more commonly observed. 43 The patient demographics were comparable to those of our inpatient population with 70.4% of the COVID-19 positive patients in the study identifying as Black non-Hispanic.

The most common comorbidities identified in this study were tobacco use, hypertension, diabetes mellitus, dyslipidemia, and overweight and obesity. Hypertension and diabetes reflect the most common comorbidities found in meta-analysis pertaining to COVID-19; however, the prevalence found in this demographic was much higher than found in literature. 44 The high rate of comorbidities found is especially important to take note in this population in which the J o u r n a l P r e -p r o o f majority of the demographic are minorities disproportionately impacted by COVID-19, as comorbidities have been associated with higher rates of mortality due to While an estimated one out of 10 patients with COVID-19 had at least one ocular manifestation 7 , only two of 116 ambulatory patients with positive COVID-19 tests had ocular complaints directly related to COVID-19. The two symptoms seen in this study were dry eye and conjunctivitis, two of the most common eye concerns related to COVID-19 as stated previously.

The low prevalence of COVID-19 ocular manifestations in comparison to previously described meta-analyses may be a result of several factors, including hospital restrictions for ambulatory visits for patients with a positive COVID-19 tests, symptoms not correctly identified as related to COVID-19, or ocular symptoms overlooked due to other COVID-19 symptoms. This highlights the importance of awareness of COVID-19 ocular symptoms, as the prevalence of COVID-19 ocular symptoms identified may be low even at large institutions.

Our findings present the ocular diagnoses observed during the onset of the COVID-19 pandemic and one of a few studies with patients from an urban, academic hospital. There are limitations to our study, including a relatively small sample size. Additionally, COVID-19 tests included in the study were only those performed at our institution; patients with positive COVID-19 tests performed elsewhere may exist that were not included in our analysis. Another limitation to consider is that the COVID-19 vaccine was not approved during the study time period; therefore, the observed diagnoses may differ from those in breakthrough cases among vaccinated patients. A point-prevalence survey of 100,000 people in England and a randomized trial of the Moderna vaccine both found that fully vaccinated individuals were two-thirds less likely to be asymptomatic COVID-19 carriers than the unvaccinated. 46 There is little in the literature documenting ocular symptoms in these breakthrough cases. It would be beneficial to compare the ocular findings in COVID-19 positive patients before vaccinations were available with those of COVID-19 positive breakthrough cases. This may provide insight on the effectiveness of the current mRNA vaccines in preventing ocular symptoms in patients who test positive for COVID-19. Our retrospective study in an academic setting also was limited by the need to rely on the accuracy of the data entered in the electronic medical record.

Ophthalmic practice requires close physical contact with patients along with proper understanding of potential ocular findings from COVID-19 within various settings and among different populations. COVID-19 related ocular manifestations may not be as commonly seen in an outpatient setting, further underscoring the importance of identifying ocular findings from this virus. The information from our study underscores the importance of local demographic evaluation, particularly from large, urban settings with a predominance of underrepresented minorities who have been disproportionately affected by COVID-19.

The disparities in COVID-19 related diagnoses are due to numerous factors, including socioeconomic status, increased incidence of co-morbidities and lack of access to quality healthcare, all resulting in poor outcomes. 47, 48 Black and Latinx patients are more likely to work in jobs requiring frontline exposure to COVID-19; however, the positions often provide inadequate or no health insurance. These individuals also are more likely to live in crowded housing, thus putting them at risk of COVID-19 infection. 47, 48 Reduced access to quality care was examined in a recent study involving telemedicine practices during the early phase of the pandemic. Older nonwhite patients were less likely to access care largely due to a preference for in-person visits as opposed to video visits or phone calls. Nonwhite patients also were less likely to have access to internet service to facilitate a video visit. 21 to increases in telemedicine, and the impact on vision. 32, 49, 50 One retrospective analysis of medical retina patients in Australia found an average delay of 8 weeks or more in 40% of patients, with patients with neovascular macular degeneration experiencing the greatest vision loss from treatment delay. 32 Another study in Brazil found a decrease in the mean number of visits and medications for glaucoma patients pre-and post-pandemic. 51 There remains a lack of J o u r n a l P r e -p r o o f research on follow-up delay due to COVID-19 in the US and racial and ethnic disparities in regards to follow-up care in ophthalmology during COVID-19. As the pandemic continues and telemedicine remains as a greater part of patient care, ensuring adequate follow-up care to prevent vision loss must be a priority. The burden of canceled visits remains on patients, whether the patient or the provider cancels 52 , and racial and ethnic minorities may be disproportionately affected in follow-up care as seen with other disparities related to COVID-19. Current systemic reviews of racial and ethnic health disparities primarily identify these disparities; however, other articles expand on strategies for addressing them. Such strategies involve multipronged policy approaches, including accessible testing, contact tracing, and vaccination. 48, 53, 54 Evaluating the intersectionality between racial and ethnic health disparities with socioeconomic, environmental, and disability status is crucial for developing effective interventions for equitable access to care.

Studies which present findings from large public hospitals and large urban medical centers are integral in examining gaps in healthcare for Black and Latinx patients and ensure that future management and treatment options during the pandemic will be focused on identifying areas for improvement during ophthalmic examination. Eye care professionals and providers from all disciplines should be aware of the common ocular diagnoses found in all patient populations, particularly minority patients when working in similar settings as the one in our study. Our study serves to inform assessing ocular findings for patients with COVID-19 positive tests expanding on and adding to our current body of literature to date and perhaps for future variants or pandemics.

The question remains as to how this information can be applied during ophthalmic examination. The common diagnoses of age-related nuclear cataracts and diabetic related ophthalmic complications are found in many patients and may not prompt much concern for possible COVID-19 infection. Diabetic-related ophthalmic findings should however cause us to further examine the likelihood that these findings may be due to COVID-19, especially if the diagnosis. Breakthrough cases also must be studied more closely to determine if ophthalmic findings are present in these patients at the same or lower rates. Some patients may be asymptomatic and present to their eye exam with symptoms that prompt COVID-19 testing, further contributing to the identification of these individuals who otherwise would have no awareness of their status.

In summary, opportunities exist in both eye care delivery and implementation of observational studies with intervention-based strategies to examine and evaluate the past, current, and ongoing effects COVID-19 has on our patients. In particular, investigational research in underserved populations should remain a cornerstone for reducing health disparities and improving access to care for those patients most vulnerable. Public hospitals and urban academic medicals must seize this opportunity and are uniquely positioned to do so.

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