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Ocular manifestations of COVID-19

COVID-19 is a disease caused by a SARS-CoV-2 viral infection, a disease that was first detected in December 2019 in Wuhan, Hubei Province, China. COVID-19, formerly known as 2019 Novel Coronavirus (2019-nCoV) respiratory disease, was officially named COVID-19 by the World Health Organization (WHO) in February 2020. By 25 May 2021, there were 33,579,116 confirmed cases with 599,109 COVID-19 deaths worldwide. The purpose of this review article is to provide an update on what is currently known about COVID-19 ocular symptoms in adults, the elderly, and children in the literature. Finally, this article will review the eye protection precautions that should be implemented in our clinics. To assess the current literature, PubMed was searched from December 2019 to 25 May 2021. Randomized trials, observational studies, case series or case reports, letters of research, and letters to editors were selected for confirmed cases of COVID-19. According to current scientific literature since the outbreak in December 2019, 205 articles have been published. Conjunctivitis, conjunctival hyperemia, and chemosis have been reported in adults with COVID-19. There have been few studies on children and elderly patients, and further research in these age groups is needed. Finally, wearing eye protection when seeing patients on a daily basis during the pandemic is essential.

Conjunctival irritation was the most prevalent ophthalmological finding (50.8%), followed by diplopia (27.8%) and cotton wool patches (27.8%). 14 Males have been diagnosed with viral conjunctivitis at a higher rate than females. 15 The majority of the cases were acute COVID-19 cases, with some chronic COVID-19 cases observed in each case. Chronic COVID-19 cases have been termed 'Long COVID' or 'COVID Long-Haulers'. 16 In China, Long COVID-19 has been reported, with COVID-19 symptoms lasting 6 months after the hospital discharge. 17 A number of literature reviews in ocular manifestations have been published, 13 and couple of the review articles concluded that further studies are required to determine the ocular manifestations in children and geriatric patients. 13 This article will examine the gaps by including ocular manifestations in children and geriatric patients, in addition to currently reported ocular manifestations in adults. Finally, the eye protection precautions that should be applied in our clinics will be covered.

Search strategy
PubMed search was performed from December 2019 to 25 May 2021. The key words 'COVID-19', 'Ocular Manifestations' and 'SARS-COV-2' were used individually or in combination. Randomized trials, observational studies, case series or case reports, letters of research, and letters to editors for confirmed cases of COVID-19 were covered. According to current scientific literature since the outbreak in December 2019, 205 papers have been written (Figure 1).

Adults' ocular manifestations
Anterior segment According to several studies, ocular symptoms are uncommon and unlikely to represent the presenting clinical impression in COVID-19 infection. 19 Furthermore, no epiphora, no secretion, or decreased vision has been reported. 20 Other studies concluded no eye problem reports in Thailand that could be related to the severity of the disease and low sample size. 21  Ocular symptoms were found to be present in 2-32% of COVID-19-infected patients. 15,25 The prevalence rate of acute conjunctivitis has been shown to range from 1.1% to 31.6%. 2 The study by Bozkurt et al. 30 found that COVID-19 patients showed pathological conjunctival abnormalities and that pathological ocular surface abnormalities can occur even before clinically relevant ocular manifestations. Because viral RNA was found in 7% of patients' conjunctival secretions, the possibility of ocular transmission should be considered even in the absence of visual symptoms. 22,31 Conjunctivitis was the most common ocular condition among COVID-19 patients, accounting for 88.8% of all reported ocular disorders such as foreign body sensation, tearing, and dry eyes. According to the findings, one out of every 10 COVID-19 patients had at least one eye symptom. The sensitivity of COVID-19 detection among patients can be improved by paying attention to ocular symptoms, particularly conjunctivitis. 32 Positive upper respiratory infection symptoms were linked with conjunctival congestion in these patients. 3 Conversely, meta-analysis study showed that the non-severe COVID-19 patients appearing to be more likely to develop conjunctivitis. 33 Ocular symptoms might develop as a prodromal symptom in the presymptomatic phase (12.5%, 13/104 cases), implying viral transfer through the conjunctiva 34 and due to viral shedding of tears, extreme care must be taken. 22,35,36 Conjunctival injection was the most frequent ocular abnormality, followed by visual changes and ocular irritation. 37 Méndez Mangana et al. 38 reported the first 31 White female who had episcleritis in a COVID-19-positive patient. Sriwastava et al. 39 reported the first case of myasthenia gravis in a 65-year-old female COVID-19positive patient. HSV-1 keratitis had been reported in five cases. 40 Other ocular manifestations include dry eye syndrome and episcleritis. 41 Follicular conjunctivitis, 9,41-44 conjunctival hyperemia, 11 chemosis, epiphora, and increased secretions have been reported. 2,28 Increased conjunctival secretions, ocular pain, 9 ocular discharge and redness, 9 photophobia, dry eye, tearing, and conjunctival congestion, as well as xerophthalmia and keratitis, are chronic COVID-19 ocular manifestations. 26 Acute follicular conjunctivitis with preauricular lymphadenopathy (LAP) and anterior uveitis were observed. 45 Other study reported severe viral conjunctivitis with pseudomembranes on the tarsal conjunctiva with enlarged submaxillaries and preauricular lymph nodes. 46 Hemorrhagic conjunctivitis with pseudomembranes was reported in a 63-year-old male COVID-19 patient. 47 In one case study, a 53-year-old white male COVID-19 patient was diagnosed with blepharitis, and he was advised to keep using the warm compresses and take 100 mg of doxycycline if the symptoms persisted or did not improve. 48 This study found the same rate of positive findings in groups with and without conjunctivitis, indicating that identifying SARS-CoV-2 in ocular secretions is not dependent on conjunctivitis. 5 The SARS-CoV-2 virus can produce ocular symptoms such as viral conjunctivitis. Infected individuals with conjunctivitis and fever may benefit from conjunctival sampling. 49 As a diabetic, hypertensive, and asthmatic 65-year-old COVID-19 patient, while on a ventilator, he developed severe follicular conjunctivitis of the right eye. The resolution of visual symptoms was observed over a period of 2 weeks with no problems. This case discussed and illustrated the sequence of events in individuals with COVID-19 infection who have long COVID-19 late ophthalmic symptoms. 50 During a lengthy COVID-19 lockdown, contact lens compliance was low, particularly in terms of handwashing and storage case cleanliness, emphasizing the necessity for patient-practitioner communication methods to reduce the risk of ocular transmission and viral tropism. 51 Despite the fact that the influence of eye allergy on everyday activities and emotions was limited, the influence of eye allergy symptoms during the quarantine period was determined to be considerable. 52 In conclusion, long-term COVID-19 patient follow-up is recommended to identify any posterior segment manifestations that may develop over time.

Neuro-ophthalmology and neurological manifestations
Diplopia, ocular pain, and myasthenia gravis are among the reported neuro-ophthalmology signs and symptoms. 66,67 Vertical diplopia has been present for 10 days in a 58-year-old male. Internuclear ophthalmoplegia was suspected based on extraocular movement testing findings. 68 Fever, cough, and headache were followed by retro-ocular pain and reading impairment in a 51-year-old woman. She was diagnosed with Adie's syndrome and multifocal chorioretinitis. 66 Lidder et al. 69 reported the first case of a Kawasakilike syndrome in a COVID-19-infected adult.
A 25-year-old man with no history of coagulopathy was reported to have experienced a COVID-19 cytokine storm, which resulted in Lock In Syndrome secondary to pontine strokes. 70 The neurological symptoms linked with acute COVID-19 include acute cerebellar ataxia and myoclonus (ACAM) with or without opsoclonus. 71 Myasthenia gravis has been diagnosed in a 21-year-old female COVID-19 patient. 67 Table 1 summarizes the ocular manifestations.
The risk factors of ocular involvement include older age, high fever, elevated neutrophil/lymphocyte ratio, and elevated levels of acute phase reactants. 81 Finally, the presence of neuro-ophthalmologic symptoms may increase the viral infection likelihood, especially if fever and respiratory symptoms are present.

Ocular COVID-19 and children
The

Geriatric
Bilateral conjunctivitis Colavita et al. 72 Pirraglia et al. 78 Conjunctival hyperemia Abrishami et al. 79 Meduri et al. 80 Chemosis Abrishami et al. 79 Meduri SARS-CoV-2 transmission through tears may be possible, despite the low incidence and rapid resolution of viral presence in the conjunctiva, even in patients who do not appear to have ocular involvement. 77 Late-onset rash and transient loss of taste were reported by a 15-year-old boy. Furthermore, infection with the SARS-CoV-2 virus in children and adolescents can be asymptomatic, but it can also cause fever, dry cough, tiredness, and gastrointestinal symptoms. 86 Conversely, some studies did not report any ocular manifestations of COVID-19 in children. 73,87 The most common symptoms and signs in 551 COVID-19 children aged 1-17.5 years old were 53% fever, 39% cough, and 14% sore throat/pharyngeal erythema; however, 18% were asymptomatic. 73 74% of patients were administrated antivirals, six patients required invasive mechanical ventilation, and one of them died.

Future research
Only a few studies in the geriatric population and children have been published. To assess the ocular symptoms in children and geriatric patients, more retrospective studies are needed.

Conclusion
The probability of viral transmission through tears is much higher in patients with moderate to severe COVID-19. For RT-PCR tear collection, the conjunctival swab remains the gold standard. In addition, wearing eye protection when seeing patients on a daily basis during the pandemic is essential. Follicular conjunctivitis, conjunctival hyperemia, chemosis, and epiphora are the most prevalent ocular symptoms in adults. Optic neuritis, disk edema, retinal artery occlusions, intraretinal hemorrhages, cotton wool spots, and uveitis have all been reported in COVID-19 patients as posterior segment ocular manifestations. Finally, neuro-ophthalmology signs and symptoms include ocular pain, diplopia, and myasthenia gravis. Long-term follow-up is advised to determine the long-term COVID-19 ocular manifestations that may develop over time. Finally, more retrospective studies in the geriatric and pediatric populations are required.

Conflict of interest statement
The author declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding
The author received no financial support for the research, authorship, and/or publication of this article.