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. 2022 Dec 1;3(1):33–38. doi: 10.1016/j.aopr.2022.11.001

COVID-19 and ocular complications: A review of ocular manifestations, diagnostic tools, and prevention strategies

Jilian Dong a, Ruida Chen b,c, Hanhe Zhao c, Yirui Zhu c,∗
PMCID: PMC9714126  PMID: 36471811

Abstract

Background

The novel severe acute respiratory syndrome coronavins 2 (SARS-CoV-2) led to the severe Corona Virus Disease 2019 (COVID-19) outbreak that started in December 2019 in China and caused enormous health and economic problems worldwide. Over time, SARS-CoV-2 has demonstrated the capacity for mutation. As the most prevalent new coronavirus variety worldwide, the Omicron variant has supplanted the Delta variant. The COVID-19 primarily damages the immune system and the lungs, but it can also harm other organs secondarily, depending on the patients' co-existing conditions.

Main Text

COVID-19 is associated with ophthalmic manifestations such as conjunctival congestion, tear overflow, and conjunctival edema, with the majority of eye complications occurring in patients with severe infection. The virus may make a patient more susceptible to thrombotic conditions that affect venous and arterial circulation. Meanwhile, it can lead to efferent complications and mucormycosis which is more common in patients with diabetes or who have critical or severe SARS-CoV-2 infection. Significantly, there are a number of ocular side effects following the COVID-19 vaccination, such as herpetic keratitis and facial nerve palsy, which have been reported. These side effects may be caused by the vaccinations' propensity to trigger autoimmune symptoms or thromboembolic events. At present, large-scale nucleic acid testing mainly relies on nasopharyngeal swabs and throat swabs. Tear samples and conjunctival swabs may be helpful samples for the diagnosis of ocular SARS-CoV-2 infection. The eye could be a new route of infection, and finding ways such as effective environmental disinfection, scientific administrative control management, qualified personal protection and other measures to protect the eyes could further reduce the risk of infection.

Conclusions

This review aims to sum up the ocular complications of COVID-19, the possible pathogenesis, and preventive strategies to protect ophthalmology practitioners and patients by reviewing the currently available literature on the topic.

Keywords: COVID-19, Ocular manifestations, Diagnostic tools, Prevention strategies

1. Introduction

The novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) was responsible for the severe Corona Virus Disease 2019 (COVID-19) outbreak that started in December 2019 in Wuhan, Hubei Province, China.1 Due to its strong infectivity, the epidemic quickly spread around the world, and the virus was officially named SARS-CoV-2 based on the results of nucleic acid sequencing of patients’ lower respiratory tract samples. As of October 3, 2022, more than 617 million people have been infected by COVID-19, and the cumulative number of deaths has exceeded 6.53 million globally.2

The most common symptoms of COVID-19 are fever, dry cough, and shortness of breath.3 It mainly causes lung and immune system damage, but it also causes secondary damage to other organs that varies based on co-existing diseases in the patients.4 Studies have shown that SARS-CoV-2 binds to angiotensin-converting enzyme 2 (ACE2) receptors.5 As these receptors are also present in the eye, this may be a possible transmission route and an organ of infection. The study of eye complications related to COVID-19 and effective ways of prevention and treatment may be useful for the control of this pandemic. This article reviews the ocular complications associated with COVID-19 and provides suggestions for healthcare practitioners with regards to protecting themselves from the virus.

2. Characteristics of the novel coronavirus and its variants

SARS-CoV-2 has exhibited the ability for mutation over a period of time.6 Four variants have been identified between December 20, 2020, and May 2021, namely, the Alpha (b.1.1.7), Beta (B.1.351), Gamma (P.1), and Delta (B.1.617.2) variants, which are associated with increasing levels of infectiousness and disease severity.

In late December 2020, according to the results of whole genome sequencing of patients who tested positive for SARS-CoV-2, the Alpha variant (B.1.1.7) was first reported in the United Kingdom.7 A preliminary matching case-control study showed that there was no significant difference in the hospitalization risk or mortality of the B.1.1.7 variant compared with the other variants. However, subsequent studies have shown that patients infected with this variant exhibit more serious symptoms and have a higher risk of death.8, 9, 10

The Delta variant was first discovered in India in December 2020 and caused the second wave of SARS-CoV-2 infection there in April 2021.11 First detected in the United States in March 2021, SARS-COV-2 Delta variant was the dominant strain in the United States in 2021. Studies have shown that the fatality rate of the Delta variant may be related to differences in population characteristics.12

On November 11, 2021, a new variant was discovered in the Republic of Botswana in Africa, and since then, it has also been reported in many parts of South Africa. The World Health Organization designated the mutant as a variable of concern on November 26, 2021, and named it the Omicron variant (B.1.1.529).13 The Omicron variant has undergone more significant mutations than the previous variants.14 The Omicron variant is more infectious and causes milder clinical symptoms, but the risk of secondary infection is six times higher than that with the Delta variant.15,16 Globally, the Omicron variant has replaced the Delta variant as the world's leading novel coronavirus variant.17

3. Virus transmission

SARS-CoV-2 invades the human body by binding to ACE2 receptors on cells.5 Therefore, tissues that express ACE2 receptors are likely to be invaded by the virus. ACE2 receptors have been identified in a wide range of human tissues, including the lungs, small intestines, brain, kidneys, and blood vessels.18 Liulin et al. have detected the expression of ACE2 receptors in the conjunctiva and corneal tissue of the human eye, so it can be inferred that the SARS-CoV-2 may invade the human body through the eyes.19 Zhou Y et al. studied 67 patients with confirmed SARS-CoV-2 infection at the People's Hospital of Wuhan University in China.20 SARS-CoV-2 was detected in the conjunctival sac of three of the patients, but they did not exhibit any ocular symptoms. The research so far indicates that it is almost impossible for COVID-19 to spread through the conjunctiva. Of 72 patients diagnosed with COVID-19 at Tongji Hospital in Wuhan, the virus was detected in the eye secretion of only one person. The researchers concluded that the surface of the eye may be a potential route of infection of SARS-CoV-2, but the probability of infection through this route is extremely low for the general population.21 Thus, it seems that while SARS-CoV-2 may be present in tears or conjunctival sacs, it is unclear whether it can be transmitted via the eyes.

4. Ocular manifestations of COVID-19

Coronavirus disease COVID-19 is associated with ophthalmic manifestations during and after recovery from the disease and may be sight-threatening. Other more serious eye complications associated with COVID-19, such as epiphora, reactivation of quiescent anterior uveitis, anterior sclero-uveitis, cotton wool spots, retinal hemorrhages, retinal artery/vein occlusion, ophthalmic artery occlusion, panuveitis, papillophlebitis, central serous retinopathy, presumed fungal endophthalmitis, and multifocal chorioretinitis, have been reported in clinical cases.22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33

4.1. Anterior segment manifestations of COVID-19

A research study showed that out of 38 COVID-19 patients in Wuhan, Hubei Province in China, 12 had eye abnormalities, which mainly included conjunctival congestion, tear overflow, and conjunctival edema, among other signs. Only one of them had conjunctivitis as the first symptom, and most eye complications occurred in patients with severe infection.34 Another study included 72 COVID-19 patients from Tongji Hospital in Wuhan City in China: only 2 showed symptoms of conjunctivitis, and SARS-CoV-2 was detected in the eye secretion of one patient.35 In a meta-analysis of three studies (1167 patients), the frequency of conjunctivitis was higher in patients with severe COVID-19 at admission (3 vs. 0.7% with an odds ratio of 3.4).36 Another study, which included a total of 16 studies of 2347 confirmed COVID-19 cases, found that the pooled data showed 11.64% of COVID-19 patients had ocular surface manifestations. Ocular pain (31.2%), discharge (19.2%), redness (10.8%), and follicular conjunctivitis (7.7%) were the main features.37 These findings indicates that the likelihood of SARS-CoV-2 infection being transmitted through the ocular surface is extremely low; nonetheless, nosocomial transmission of SARS-CoV-2 infection through the eyes after occupational exposure is a potential route.

Sanjay et al. reported the case of a COVID-19 positive patient presenting with anterior sclero-uveitis and demonstrated that the acute form of this condition could precede the SARS-CoV-2 infection.32 They suggested that in all hitherto first episodes of ocular inflammation, COVID-19 should be considered to be diagnosis as a possible cause because this virus is preceded by ocular inflammation.

4.2. Posterior segment manifestations of COVID-19

Studies have shown that COVID-19 may make patients more vulnerable to thrombotic disease that affects both venous and arterial circulation.38,39 Further, thrombotic disease in these patients is characterized by excessive inflammation, platelet activation, endothelial dysfunction, and stasis. However, due to the complex and interacting vascular risk factors in most patients, the relationship between thrombotic disease and COVID-19 is not clear yet.40 The increased risk of retinal vascular obstruction caused by COVID-19 has yet to be studied. It has been reported that 12 patients with confirmed COVID-19 showed hyper-reflective lesions at the level of the ganglion cell and inner plexiform layers that were more prominent in the papillomacular bundle of both eyes.41 Hyper-reflective features in the inner retina on optical coherence tomography (OCT) images in all 12 patients. The results of OCT angiography and complex analysis of ganglion cells were normal. Fundus examination in four cases revealed the presence of subtle cotton wool spots and microhemorrhages along the retinal arcade. Despite this, all the patients had normal visual acuity and pupillary reflexes and no symptoms or signs of intraocular inflammation. Nevertheless, this results led to some controversy. Frederick T Collison et al. identified the OCT findings reported by Marinho and colleagues represent normal retinal anatomy.42

One case presenting with vitritis had bilateral redness in the eyes, and examination showed a yellowish macular lesion 12 days after the onset of COVID symptoms. OCT displayed hyper-reflective lesions at several sites and fluorescence fundus angiography revealed hyper-fluorescence.43 Moreover, some acute retinal necrosis cases during or after COVID-19 have been reported. Some reactivated cases of varicella zoster virus presented as acute retinal necrosis.44, 45, 46, 47, 48 There are few case reports that detail the reactivation of chorioretinal disease after SARS-CoV-2 infection or COVID-19 vaccination.49, 50, 51 The inflammatory effect of COVID-19 is considered to be the mechanism of action on highly vascularized choroid tissue, resulting in chorioretinal inflammation.51

4.3. Neuro-ophthalmic manifestations of COVID-19

Numerous efferent complications have been reported in association with SARS-CoV-2 infection, including isolated cranial nerve palsies with diplopia, Miller Fisher syndrome and nystagmus or saccadic intrusions in association with either brainstem infarction or hemorrhagic acute necrotizing encephalopathy. Proposed mechanisms include direct neural invasion into the peripheral or central nervous system, parainfectious inflammation provoked by the immunogenicity of novel antigens presented by the SARS-CoV-2 virus, and secondary hypercoagulability and endothelial dysfunction resulting in stroke. Neuro-ophthalmic symptoms have rarely been reported following SARS-CoV-2 vaccination, but evidence for causation is lacking and the benefits of inoculation continue to far outweigh any perceived risks.52

4.4. Orbital manifestations of COVID-19

Rhino-orbital cerebral mucormycosis is the most common orbital involvement in patients with COVID-19, reported in several case series.53, 54, 55 Mucormycosis induced by COVID-19 is more common in patients with diabetes mellitus and who are suffering from critical or severe COVID-19.56 Immunologic changes in diabetic patients are a potential risk factor for such fungal conditions. The main mechanism is the spread from the colonization of nasal mucosa. This disease is a life-threatening infection that can occur in patients with COVID-19, because of their compromised immune system and decreased lymphocytes, due to the disease itself, decompensated pulmonary function, and treatment with corticosteroids.57

4.5. Post-vaccination ocular complications

COVID-19 vaccines can cause transient local post-vaccination reactions. Different types of ocular complications have been reported after COVID-19 vaccination, including herpetic keratitis, facial nerve palsy, abducens nerve palsy, new-onset Graves' disease, episcleritis, anterior scleritis, anterior uveitis, multifocal choroiditis, reactivation of Vogt-Koyanagi-Harada disease, multiple evanescent white dot syndrome, acute macular neuroretinopathy, paracentral acute middle maculopathy, thrombosis, and central serious retinopathy. These complications could be related to SARS-CoV-2 vaccines’ capacity to induce autoimmune manifestations or thromboembolic events.58

5. Ophthalmic detection of COVID-19

Specimens such as nasopharyngeal or oropharyngeal swab, bronchoalveolar lavage fluid, sputum, bronchial aspirate, and blood are generally recommended for early screening or diagnosis of COVID-19.59,60 Studies show that higher viral loads of SARS-CoV-2 are typically detected in the lower respiratory tract,61 and the highest detection rates were reported in bronchoalveolar lavage fluid, sputum, and nasal swabs.62 However, from the viewpoint of comprehensive analysis, convenience of sampling, and patient comfort, nasopharyngeal swabs and throat swabs are more suitable for large-scale nucleic acid determination.

For the diagnosis of ocular SARS-CoV-2 infection, tear samples and conjunctival swabs may be useful samples for obtaining clinical evidence.

5.1. Tear samples

In a recent case series of a prospective interventional study, the tear sample from only 1 of 30 confirmed cases of COVID-19 was positive (according to PCR) for SARS-CoV-2.63 Another study tested both tear samples and nasopharyngeal swabs and showed that the nasopharyngeal swabs were positive and the tear samples were negative. Thus, the hypothesis that nasolacrimal ducts act as a transmission route for the virus may be incorrect. Within the study time frame, only 1 in 17 patients had eye symptoms, but SARS-CoV-2 was not detected in the tear samples of any of the patients.64 This result indicates that the possibility of the virus spreading through tears is really low.

5.2. Conjunctival swab samples

In a prospective study series on 30 COVID-19 patients, only 1 out of 30 conjunctival swab samples were positive for SARS-CoV-2.63 In another study on 67 patients with COVID-19 (63 cases with confirmed COVID-19 and 4 cases of suspected COVID-19), three conjunctival swabs were positive (PCR).20 However, none of the three patients with positive conjunctival swab samples exhibited conjunctivitis. The initial manifestation was conjunctivitis in only one patient, but the conjunctival swab sample was negative for SARS-CoV-2 (PCR). This patient is an anesthesiologist, and he was probably infected because he did not wear protective glasses during the operation. However, the symptoms of conjunctivitis were mild. Based on the findings of this study, it seems unlikely that SARS-CoV-2 can be transmitted through the conjunctival route. However, subsequent study has shown that a small number of patients with confirmed SARS-CoV-2 infection did have conjunctivitis.21 Despite this, only 2 of 72 patients with confirmed COVID had conjunctivitis, and the conjunctival sac secretion was positive according to the virus nucleic acid test in only one of these two patients in Wuhan province. Similarly, in Zhejiang province, only 1 out of 30 patients with COVID-19 had conjunctivitis and a positive result for conjunctival sac secretion.20 Thus, it appears that although there is clinical evidence of the transmission of SARS-CoV-2 through the conjunctival route, the overall positivity rate for ocular infection is low. One study included 21 patients with confirmed novel coronavirus infection from the First Affiliated Hospital of Zhejiang University, but viral RNA was detected in the tears and conjunctival secretions of only one patient. The researchers also collected sputum samples of patients to use as the controls, and 55 of the 60 samples were positive.63 The authors believe that this result shows, to some extent, that COVID-19 patients who do not have conjunctivitis do not transmit the novel coronavirus through their tears and conjunctival secretions.

5.3. Nasolacrimal duct samples

The eyes are directly exposed to the external environment and are also connected to the respiratory tract through the nasolacrimal duct and nasal cavity. Some researchers have speculated that the virus can enter the eyes through droplets and reach the respiratory tract through the nasolacrimal duct, where it can bind to ACE2 receptors and cause SARS-CoV-2 infection.65 A study on rhesus monkeys showed that monkeys inoculated via conjunctival fluid developed mild interstitial pneumonia.66 By determining the virus load in different swabs within 1–7 days after vaccination, the researchers found that in monkeys inoculated through the conjunctival route, the virus was detected only in the conjunctival swab sample obtained on the first day and was not detected later. This indicates that the virus may have caused the infection on first entering the conjunctiva and then later migrated to the respiratory tract.

5.4. Intraocular fluid samples

Bilgic et al. reported that they successfully isolated the SARS-CoV-2 in three patients with endogenous endophthalmitis from vitreous samples.67 In another study by Koo et al., six (19.4%) patients demonstrated detectable SARS-CoV-2 RNA in aqueous samples, fortunately, none of these individuals had any systemic symptoms.68 However, Maya Hada and colleagues detected the presence of SARS-CoV-2 in the aqueous and vitreous humor of seven ocular trauma COVID-19 patients.69 SARS-CoV-2 was not detected by polymerase chain reaction in aqueous or vitreous humor in this pilot study. Similarly, Srinivasan Sanjay and colleagues were unable to isolate the SARS-CoV-2 virus in either aqueous or vitreous samples.70 This may be explained by the fact that SARS-CoV-2 is not detected in a very low percentage of ocular samples in patients who have COVID-19. Therefore, whether current tests are sensitive enough to detect SARS-CoV-2 through intraocular fluid sampling is debatable.

6. Reducing the risk of COVID-19 in the ophthalmology department

In order to control the spread of SARS-CoV-2 infection and reduce the risk of infection among ophthalmological clinicians and patients, medical staff should work closely with local infection control teams to carry out risk assessment and undertake appropriate strategies for infection control in the real-world clinical environment.

SARS-CoV-2 is excreted through respiratory secretions. Inhalation of respiratory droplets and direct contact with contaminated surfaces are the main routes of transmission. The incubation period after infection is 1–14 days, and both symptomatic and asymptomatic COVID-19 patients can spread the virus.71 The virus is transmitted through exhaled droplets that are 5 μm or larger in diameter, such as the droplets produced when coughing, sneezing, singing, and speaking.72 It can also spread via inhalation of aerosols that circulate in relatively closed environments for a long time. One study found that surfaces contaminated by SARS-CoV-2 can also lead to spread of the virus, and the rate of reduction of surface virus concentration is related to the properties of the surface. The estimated half-life of SARS-CoV-2 is approximately 6.8 ​h on plastic surfaces and 5.6 ​h on stainless steel surfaces. However, the virus is not stable on cardboard, and it is especially unstable on copper.73 Therefore, choosing the right material for surfaces in the clinic may help to effectively reduce the risk of viral infection.

Considering the relationship between COVID-19 and eye complications, conjunctivitis may be the first clinical manifestation of COVID-19.74 Although the incidence rate is not high, we believe that indicators of ocular abnormalities, such as conjunctivitis, may help in the diagnosis of this infection. In addition, medical workers should inform patients of the possibility of SARS-CoV-2 transmission through the eyes. Irrespective of whether the patient has eye symptoms, healthcare workers should advise patients to minimize or avoid touching their eyes, nose, and mouth to prevent the spread of the virus. Further, instruments that come into contact with the surface of the eye should be disinfected with ethanol or be replaced with reliable disposable alternatives where possible. In addition, the American Academy of Ophthalmology recommends that framed glasses be used instead of contact lenses as much as possible. Glasses provide a physical barrier for eye mucosal tissue and reduce the possibility of SARS-CoV-2 transmission through the eyes.75 Further, to lower the risk of nosocomial SARS-CoV-2 infection, all healthcare professionals should wear protective goggles.

In Hong Kong, the pandemic was managed via three main levels of control measures: (1) administrative control, such as reducing the number of patients, suspending selective clinical services, and classifying patients; (2) environmental control, such as providing fresh air, regularly and frequently disinfecting surfaces that medical staff often come into contact with, and the use of staff video conferencing, as opposed to face-to-face meetings, as much as possible; (3) qualified use of personal protection equipment and strict disinfection of individuals.76 British scholars believe that during the pandemic, clinical areas should be redesigned, personal protective equipment should be worn, and sufficient social distancing should be maintained. At the same time, new working methods should be considered, such as simplifying services, reducing patient backlog, and telemedicine.77

One study found that surgical masks provided an average aerosol filtration rate of 96% for bacteria and 90% for viruses. The filtering effect of homemade masks varies according to the material used to make the mask-from 60% to 94% for bacteria, and from 49% to 86% for viruses.78 In one study, 492 medical workers from Zhongnan Hospital of Wuhan University were divided into two groups. The first group was mainly responsible for the respiratory medicine department, the intensive care unit, and the infectious diseases department (main isolation area); they wore N95 masks and regularly disinfected themselves and cleaned their hands. The second group included medical staff from other departments; this was a mask-free group that only occasionally disinfected themselves and cleaned their hands. None of the 278 staff members (56 doctors and 222 nurses) in the N95 group were infected, but 10 of the 213 staff members (77 doctors and 136 nurses) in the mask-free group were confirmed to be infected.79 In a pragmatic, clustered randomized clinical trial involving 2862 medical staff, no significant difference was found in the incidence of influenza between medical staff who used N95 respirators (8.2%) and laboratory doctors who used medical masks (7.2%).80

7. Conclusions

Based on clinical evidence of eye complications caused by SARS-CoV-2, more reliable research should be performed to confirm its potential to infect the eye and its specific pathogenesis. Some of the topics for future research are the mechanism of eye complications associated with COVID-19, the relationship between the virus and thrombotic diseases, treatment strategies for eye complications associated with COVID-19, and the feasibility of using tear samples or conjunctival swabs for diagnosis. A larger-scale, crowd-based research with standardized investigation methods is required to answer these questions. In particular, elucidating the relationship between SARS-CoV-2 and the eye not only is conducive to guiding strategies to control the pandemic, but also provides insights into the feasibility of using ocular samples, such as tear samples, for the diagnosis of COVID-19.

At present, many parts of the world are experiencing the fourth wave of the COVID-19 pandemic, and it has become clear that we must be prepared to coexist with SARS-CoV-2 for the foreseeable future. Given this, it is important that eye care practitioners pay attention to practical protection measures to minimize the risk of infection in patients and practitioners until more effective anti-viral therapies or vaccines are created.

Study approval

Not applicable.

Author contributions

Conception and design of study: YZ, JD; Data collection: JD and HZ; Analysis and interpretation of results:YZ, JD and RC; Drafting the manuscript: YZ, JD; All authors reviewed the results and approved the final version of the manuscript.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

Thanks to all the peer reviewers for their opinions and suggestions.

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