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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 60  |  Issue : 3  |  Page : 259-263

Pattern of ophthalmic manifestations among COVID-19 survivors attending eye clinic in a tertiary care centre


Department of Ophthalmology, IMS and SUM Hospital, Bhubaneswar, Odisha, India

Date of Submission25-Aug-2021
Date of Decision05-Apr-2022
Date of Acceptance11-Apr-2022
Date of Web Publication26-Sep-2022

Correspondence Address:
Jasmita Satapathy
Department of Ophthalmology, IMS and SUM Hospital, Bhubaneswar - 751 003, Odisha
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/tjosr.tjosr_134_21

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  Abstract 


Background: Almost every organ of the body including the eye can be affected in post-acute coronavirus disease 2019 (COVID-19) syndrome. Objective: To describe the pattern of ocular manifestations among recovered COVID-19 patients. Materials and Methods: An observational cross sectional study was conducted in the department of ophthalmology by recruiting patients who had recovered from COVID-19 and had attended eye clinic between 1 April 2021 and 30 June 2021. Comprehensive ophthalmological examination was performed in all participants. Results: A total 85 patients were enrolled (53 males and 32 females). Their mean age was 46.03 ± 16.2 years. The mean duration between positive real-time reverse transcription polymerase chain reaction test report for COVID-19 and the day of visit to eye clinic was 47.5±24.1 days. At least one ocular sign was present in 54 (63.5%) patients. The most common presenting ocular symptom was irritation (40%) followed by redness (29.4%). Frequently encountered ocular signs were conjunctival hyperaemia (37.6%), follicular conjunctivitis (30.6%), Keratoconjunctivitis (2.4%), central serous chorioretinopathy (3.5%), branch retinal vein occlusion (1.2%) and rhino-orbital mucormycosis (3.5%). Conclusion: Wide variety of ophthalmic manifestations can occur among COVID-19 survivors, some of which can also be sight threatening and hence they should not be ignored.

Keywords: COVID-19 survivors, COVID-recovered patients, eye clinic, ocular features, post-acute COVID-19


How to cite this article:
Satapathy J, Mishra A, Srija YN, Navyasree C, Thareja J. Pattern of ophthalmic manifestations among COVID-19 survivors attending eye clinic in a tertiary care centre. TNOA J Ophthalmic Sci Res 2022;60:259-63

How to cite this URL:
Satapathy J, Mishra A, Srija YN, Navyasree C, Thareja J. Pattern of ophthalmic manifestations among COVID-19 survivors attending eye clinic in a tertiary care centre. TNOA J Ophthalmic Sci Res [serial online] 2022 [cited 2022 Dec 7];60:259-63. Available from: https://www.tnoajosr.com/text.asp?2022/60/3/259/357103




  Introduction Top


Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), was declared a pandemic by the WHO on 11 March 2020.[1] It can affect almost every organ of the body, even after acute phase of the disease is over. Such long-term effects that may persist or appear are defined as post-acute COVID-19 syndrome or long COVID syndrome by National Institute of Health (NIH), Center of Disease Control (CDC) and the WHO.[2] Some studies have suggested ocular involvement in post-acute COVID-19 syndrome.[3],[4] When the deadly second wave was at its peak, an imminent threat emerged as a challenge in the form of mucormycosis or “black fungus” among recovering and recovered COVID-19 patients.This unpredictable opportunistic infection has resulted in ICU admission of many recovered COVID-19 patients. Some of them lost their lives and, many are left blind and disfigured. Rapid increase in cases of rhino-orbital cerebral mucormycosis (ROCM) and expansive media attention is driving even those with minor ophthalmic ailments to rush to eye clinics, as some of these symptoms mimic early rhino-orbital mucormycosis.

In the present study, we aimed to evaluate the pattern of ophthalmic manifestations among the apprehensive COVID-19 survivors attending eye clinic in a tertiary care centre in eastern India.


  Materials and Methods Top


This is a cross-sectional study conducted in the Department of Ophthalmology. Patients recovered from COVID-19 and attending eye clinic between 1 April 2021 and 30 June 2021 were recruited. For all participants, the diagnosis of COVID-19 at the time of active infection was based on positive real-time reverse transcription polymerase chain reaction (rRT-PCR) for SARS-CoV-2 obtained on throat swab samples and nasopharyngeal specimen. The study was conducted after due permission from Institutional Ethical Committee and a written informed consent was taken from all participants prior to recruitment.

Inclusion criteria

All recovered COVID-19 patients attending eye clinic between 1 April 2021 and 30 June 2021.

Exclusion criteria

Patients recovered from COVID-19 for more than three months were excluded from the study.

All patients were enquired about the demographic profile, time lag between diagnosis of COVID-19 and visit to eye clinic, place of isolation (hospital admission or home) during active infection, need of oxygen therapy, steroid use, associated comorbidities, vaccination status, presenting ocular complaints, awareness about black fungus and any prior ocular history. A complete ophthalmological evaluation was done that included presenting best-corrected visual acuity (BCVA), intraocular pressure (IOP) measurement by non-contact tonometer, assessment of anterior segment of eye including ocular adnexa by slit lamp biomicroscopy and dilated fundus examination using indirect ophthalmoscope. Depending on the history obtained patients were divided into two groups: group A (neither on oxygen support nor on steroid therapy) and group B (either on oxygen support and/or on steroid therapy at the time of active infection). Following detailed ocular examination, all participants were counselled about the potential risk of post-COVID-19 ocular manifestations including mucormycosis.

The data thus collected was entered into Microsoft Excel sheet. Descriptive data has been depicted as actual numbers, percentages and mean ± standard deviation. Statistical analysis was done using frequency distribution and Z test (by using proportions for large sample). Wherever applicable, Chi-square distribution was used to observe the association. A P value less than 0.05 was considered statistically significant.


  Results Top


A total of 85 (53 males and 32 females) COVID-recovered patients were enrolled in the study. Out of them, 49 were from urban areas and 36 were from rural areas. Their mean age was 46.03 ± 16.2 years (ranging from 15 to 92 years). Forty-seven (55.3%) patients needed hospitalisation, 35.3% were on oxygen support and 49.4% required steroid therapy at the time of active infection. Only two patients required intensive care and none of them needed invasive mechanical ventilation. The mean duration between positive rRT-PCR test report for COVID-19 and the day of visit to eye clinic was 47.5 ± 24.1 days (ranging from 17 to 87 days). Patients from urban areas were significantly more aware and visited ophthalmology outpatient department early as compared to patients from rural areas (x2 value 21.8 and P value 0.0001). The clinico-demographic data of all participants is shown in [Table 1].
Table 1: Clinico-demographic profile of all participants (n=85)

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[Table 2] shows various ocular features seen among the COVID-19 survivors. Out of 85 participants, at least one ocular sign was present in 54 (63.5%) patients. The most common presenting ocular symptom was irritation (40%) followed by redness (29.4%). Conjunctival hyperaemia (37.6%) was found to be the most common ocular sign and in 30.6% patients there was follicular conjunctivitis, mostly involving both eyes [Figure 1]. Two patients (2.4%) had unilateral Keratoconjunctivitis along with fine endothelial dusting [Figure 2]. Central serous chorioretinopathy (CSCR) was found in three (3.5%) cases, out of them one patient had bilateral involvement [Figure 3]a and [Figure 3]b. One patient had unilateral branch retinal vein occlusion (BRVO), who presented 21 days after diagnosis and was neither on steroid nor on oxygen support during active phase of infection. In three (3.5%) patients, early features of rhino-orbital mucormycosis were seen, which was later confirmed by MRI and subsequent post-debridement biopsy [Figure 4]a and [Figure 4]b. All the three patients were referred from ENT department. One of them had type II diabetes of 11 years duration, and other two patients had no comorbidities. All patients with early features of mucormycosis had history of hospitalisation and were on oxygen support as well as on steroid therapy for a prolonged period during active COVID-19 infection. Around 62.3% (n = 53) participants were aware about mucormycosis or black fungus infection. Out of them, 33 patients were scared of getting this deadly infection, which forced them to attend eye clinic. Patients from urban areas were found to have better awareness about COVID-associated black fungus infection than patients from villages. This association was found to be statistically significant (x2 value 4.45 and P value 0.034). Ocular signs like senile cataract, pseudophakia, refractive error, pterygium, pinguicula, etc., were not included in the analysis as these are thought to be neither directly nor indirectly related to COVID-19 infection.
Figure 1: Follicular conjunctivitis with conjunctival hyperemia

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Figure 2: Keratitis with fine endothelial dusting

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Figure 3: Central serous chorioretinopathy. [a. Fundus picture and b. OCT]

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Figure 4: Right eye showing features of orbital mucormycosis [a. Lid edema and chemosis b. Axial contrast-enhanced MRI of brain and orbit shows irregular peripherally enhancing collection in right temporal lobe extending into right orbital apex (yellow arrow), muscle edema with post-contrast enhancement of right lateral rectus (red arrow) and right-side mild proptosis with preseptal soft tissue edema.]

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Table 2: Ocular features among all COVID-19-recovered patients attending eye clinic (n=85)

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Based on the data obtained from careful history taking, patients were divided into two groups: group A (neither on oxygen support nor on steroid therapy) and group B (either on oxygen support or on steroid therapy). Group B patients were found to have the ocular findings more frequently than patients of group A. The correlation between need of oxygen support/steroid therapy and the presence of different ocular signs was statistically significant (p < 0.05). This is shown in [Table 3].
Table 3: Comparison of ocular features between group A and group B

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  Discussion Top


Long-term effects of coronavirus may persist or appear in different body systems including the eye.[2],[3],[5] However, there is paucity of data available in the literature regarding ocular manifestations among COVID-19 survivors. A recent study has been conducted by Costa et al.[6] from the USA with a sample size of 64 patients, where the mean interval between onset of COVID-19 symptoms and the day of ocular examination was 82 ± 36.4 days. In the present study, the mean interval was 47.5 ± 24.1 days.

Around 8.2% patients were found to have decrease in presenting BCVA in our study, which was mostly due to CSCR and keratoconjunctivitis. Many studies have reported occurrence of CSCR in covid patients which could be due to steroid use during active phase of the disease.[7] Psychological stress during COVID-19 can also be a risk factor.[8] We found presence of CSCR in 3.5% COVID-recovered patients, which was similar (2%) to Tohamy et al.[4] Keratoconjunctivitis was reported in around 2.2% cases with active COVID-19 infection.[9] It can also be the presenting manifestation.[10] In a case report from China, Guo et al.[11] observed an unilateral case of conjunctivitis developing ten days after COVID-19 symptoms, which soon progressed to bilateral keratoconjunctivitis. In the present study, we found keratoconjunctivitis as a late manifestation in 2.4% cases.

A meta-analysis by Nasiri et al.[9] found conjunctivitis as the most prevalent ocular feature (88.8%). In another study by Abrishami et al.,[12] the most prevalent ocular finding was conjunctival hyperemia (31%). However, in these studies ophthalmic assessment was done in active phase of the disease. We have performed ocular examination among COVID-recovered patients and found follicular conjunctivitis in 30.6% cases and conjunctival hyperaemia in 37.6% cases. Chen et al.[13] reported bilateral acute follicular conjunctivitis in a patient on 13th day of illness and suggested that ocular manifestations are more common during middle phase of the disease. Nayak et al.[14] reported delayed onset of follicular conjunctivitis four weeks following severe COVID-19 infection in a 65-year-old male with diabetes, hypertension and asthma.

Some studies have suggested posterior segment involvement in post-acute COVID-19 syndrome in the form of yellowish white dots in retina, anterior ischaemic optic neuropathy, CSCR, retinal vascular occlusion, endophthalmitis, etc.[4],[6] However, in our study fundus examination was unremarkable in all patients other than three cases of CSCR and one case of BRVO.

There was a rapid increase in reported mucormycosis cases during second wave of COVID-19. It was found to be associated with moderate to severe disease having compromised immune system, associated comorbidities such as diabetes mellitus, decompensated pulmonary functions and the use of steroid therapy for the management.[15] In a multicentric case series, the authors have observed that symptoms of rhino-orbital mucormycosis developed as late as 30-42 days after the diagnosis of COVID-19.[16] In the present study, early features of mucormycosis was seen in 3.5% cases. All of them had visited eye clinic 21-32 days after the diagnosis of COVID-19.


  Conclusion Top


Physicians as well as the general public should be aware about the manifestations of post-COVID-19 syndrome. Our results suggest that wide variety of ophthalmic manifestations can occur among COVID-19 survivors, some of which can also be sight threatening and hence they should not be ignored. Moreover, all recovered patients should be counselled by the healthcare providers to have eye check up as and when they develop any symptom.

Limitations

Our study has some limitations. These include small sample size and lack of follow-up. Also, we have not studied the association of abnormal parameters including raised inflammatory markers during active infection and the occurrence of post-COVID ocular features. So, more longitudinal studies are needed with larger samples for better analysis.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Acknowledgements

We acknowledge Mr. P. K. Brahma for his help in statistical analysis.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
World Health Organization. Coronavirus disease 2019 (COVID-19): Situation report, 51. World Health Organization; 2020. https://apps.who.int/iris/handle/10665/331475.  Back to cited text no. 1
    
2.
Chippa V, Aleem A, Anjum F. Post acute coronavirus (COVID-19) syndrome. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2021.  Back to cited text no. 2
    
3.
Augustin M, Schommers P, Stecher M, Dewald F, Gieselmann L, Gruell H, et al. Post-COVID syndrome in non-hospitalised patients with COVID-19: A longitudinal prospective cohort study. Lancet Reg Health Eur 2021;6:100122.  Back to cited text no. 3
    
4.
Tohamy D, Sharaf M, Abdelazeem K, Saleh MGA, Rateb MF, Soliman W, et al. Ocular manifestations of post-acute COVID-19 syndrome, upper egypt early report. J Multidiscip Healthc 2021;14:1935-44.  Back to cited text no. 4
    
5.
Maltezou HC, Pavli A, Tsakris A. Post-COVID syndrome: An insight on its pathogenesis. Vaccines (Basel) 2021;9:497. doi: 10.3390/vaccines9050497.  Back to cited text no. 5
    
6.
Costa ÖF, Bonifácio LP, Bellissimo-Rodrigues F, Rocha EM, Jorge R, Bollela VR, et al. Ocular findings among patients surviving COVID-19. Sci Rep 2021;11:11085. doi: 10.1038/s41598-021-90482-2.  Back to cited text no. 6
    
7.
Sanjay S, Gowda PB, Rao B, Mutalik D, Mahendradas P, Kawali A, et al. “Old wine in a new bottle”- post COVID-19 infection, central serous chorioretinopathy and the steroids. J Ophthalmic Inflamm Infect 2021;11:14.  Back to cited text no. 7
    
8.
Franklin M, Wagner A, Kapoor K. Psychological stress during COVID-19 and central serous chorioretinopathy (CSCR). Invest Ophthalmol Vis Sci 2021;62:1971.  Back to cited text no. 8
    
9.
Nasiri N, Sharifi H, Bazrafshan A, Noori A, Karamouzian M, Sharifi A. Ocular manifestations of COVID-19: A systematic review and meta-analysis. J Ophthalmic Vis Res 2021;16:103-12.  Back to cited text no. 9
    
10.
Cheema M, Aghazadeh H, Nazarali S, Ting A, Hodges J, McFarlane A, et al. Keratoconjunctivitis as the initial medical presentation of the novel coronavirus disease 2019 (COVID-19). Can J Ophthalmol 2020;55:e125-9.  Back to cited text no. 10
    
11.
Guo D, Xia J, Wang Y, Zhang X, Shen Y, Tong JP. Relapsing viral keratoconjunctivitis in COVID-19: A case report. Virol J 2020;17:1-7.  Back to cited text no. 11
    
12.
Abrishami M, Tohidinezhad F, Daneshvar R, Omidtabrizi A, Amini M, Sedaghat A, et al. Ocular manifestations of hospitalized patients with COVID-19 in Northeast of Iran. Ocul Immunol Inflamm 2020;28:739-44.  Back to cited text no. 12
    
13.
Chen L, Liu M, Zhang Z, Qiao K, Huang T, Chen M, et al. Ocular manifestations of a hospitalised patient with confirmed 2019 novel coronavirus disease. Br J Ophthalmol 2020;104:748-51.  Back to cited text no. 13
    
14.
Nayak B, Poddar C, Panigrahi MK, Tripathy S, Mishra B. Late manifestation of follicular conjunctivitis in ventilated patient following COVID-19 positive severe pneumonia. Indian J Ophthalmol 2020;68:1675-7.  Back to cited text no. 14
[PUBMED]  [Full text]  
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Sen M, Honavar SG, Sharma N, Sachdev MS. COVID-19 and eye. Indian J Ophthalmol 2021;69:488-509.  Back to cited text no. 15
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Sen M, Lahane S, Lahane TP, Parekh R, Honavar SG. Mucor in a viral land: A tale of two pathogens. Indian J Ophthalmol 2021;69:244-52.  Back to cited text no. 16
[PUBMED]  [Full text]  


    Figures

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