Ophthalmological aspects of coronavirus infections
https://doi.org/10.21516/2072-0076-2021-14-1-7-14
Abstract
The novel coronavirus infection (COVID-19) caused by SARS-CоV-2 virus, may lead to ocular diseases besides affecting the respiratory system. Cororonavirus infection may be transmitted not only through the respiratory system but also through the conjunctiva. The review article summarizes the data on the origin and variants of coronaviruses that infect humans, as well as on SARS-CоV-2 structures. Literature data on prospects of molecular diagnostics of the disease, coronavirus type detection methods, clinical sample types and duration of the disease before it is diagnosed are discussed. The data on the relationship between the coronavirus infection and conjunctivitis are given. Molecular tests of the tear and conjunctival swabs were used to diagnose the coronavirus infection independently of whether symptoms of ocular disorders were present. The real-time reverse-transcription of RNA polymerase chain reaction (PCR) was the most informative method for diagnosis of SARS-CоV-2 in the early stage of COVID-19 (until the 9th day). The presence of SARS-CоV-2 in the tear fluid and conjunctival swabs indicates the need for safety measures to prevent virus transmission through the ocular surface, including protective goggles to be worn by healthcare workers. Since side effects in the eye may appear, COVID-19 patients with visual impairment who received etiotropic or pathogenetic treatment are advised to consult an ophthalmologist.
About the Authors
V. V. NeroevRussian Federation
Vladimir V. Neroev — Academician of the Russian Academy of Sciences, Dr. of Med. Sci., professor, director1 , head of chair of ophthalmology.
14/19, Sadovaya-Chernogryazskaya st., Moscow, 105062; 20/1, Delegatskaya st., Moscow, 127473
T. N. Kiseleva
Russian Federation
Tatiana N. Kiseleva — Dr. of Med. Sci., professor, head of the ultrasound department.
14/19, Sadovaya-Chernogryazskaya st., Moscow, 105062
E. K. Eliseeva
Russian Federation
Elena K. Eliseeva — Cand. of Med. Sci., researcher, ultrasound department.
14/19, Sadovaya-Chernogryazskaya st., Moscow, 105062
References
1. Prilutskii A.S. Coronavirus disease 2019. Part 1: coronavirus characteristic, epidemiological features. Vestnik of hygiene and epidemiology. 2020; 24 (1): 77–86 (in Russian).
2. Kojevoda S., Canovic S., Pastar Z., et al. Ophthalmic manifestations of novel coronaviruses: precautionary measures and diagnostic possibilities. Journal of global health. 2020; 10 (1): 1–4. https://doi.org/10.7189/jogh.10.010340
3. Shamsheva O.V. New koronavirus COVID-19 (SARS-CoV-2). Detskiye infektsii. 2020; (1): 5–6 (in Russian).
4. Akhmetshin R.F., Rizvanov A.A., Bulgar S.N., et al. Coronavirus infection and ophthalmology. Kazan medical journal. 2020; 101 (3): 371–80 (in Russian). http://dx.doi.org/10.17816/kmj2020-371
5. Gusev E.I., Martynov M.Y., Boyko A.N., et al. Novel coronavirus infection (COVID-19) and nervous system involvement: pathogenesis, clinical manifestations, organization of neurological care. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova. 2020; 120 (6): 7 (in Russian). http://dx.doi.org/10.17116/jnevro20201200617
6. Guan Y., Zheng B.J., He Y.Q., et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science. 2003; 302 (5643): 276–8. https://doi.org/10.1126/science.1087139
7. Hoffmann M., Kleine-Weber H., Schroeder S., et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020; 181 (2): 271–80.e8. https://doi.org/10.1016/j.cell.2020.02.052
8. Cui L., Wang H., Ji Y., et al. The nucleocapsid protein of coronaviruses acts as a viral suppressor of RNA silencing in mammalian cells. Journal of Virology. 2015; 89 (17): 9029–43. https://doi.org/10.1128/JVI.01331-15
9. Ji W., Wang W., Zhao X., et al. Homologous recombination within the spike glycoprotein of the newly identified coronavirus may boost cross-species transmission from snake to human. J. Med. Virol. 2020; 92 (4): 433–40. doi: 10.1002/jmv.25682
10. Chen X., Yu H., Mei T., et al. SARS-CoV-2 on the ocular surface: is it truly a novel transmission route? Br. J. Ophthalmol. 2020: 1–6. https://doi.org/10.1136/bjophthalmol-2020-316263
11. Cui W., Geriletu, Gao W., Liu W. Comparative study on specific antibody in tear and blood of SARS patients. Inner Mongolia Med. J. 2004; 36: 577–8.
12. Loon S.C., Teoh S.C., Oon L.L., et al. The severe acute respiratory syndrome coronavirus in tears. Br. J. Ophthalmol. 2004; 88 (7): 861–3. http://dx.doi.org/10.1136/bjo.2004.054130
13. Bermingham A., Heinen P., Iturriza-Gomara M., et al. Laboratory diagnosis of SARS. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2004; 359: 1083–9. https://doi.org/10.1098/rstb.2004.1493
14. Corman V.M., Landt O., Kaiser M., et al. Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR. Euro Surveill. 2020 Jan 23; 25 (3): 2000045. doi:10.2807/1560-7917.ES.2020.25.3.2000045
15. Zhou Y., Zeng Y., Tong Y., et al. Ophthalmologic evidence against the interpersonal transmission of 2019 novel coronavirus through conjunctiva. MedRxiv. 2020; 2. https://doi.org/10.1101/2020.02.11.20021956
16. Holshue M.L., DeBolt C., Lindquist S., et al. First case of 2019 novel coronavirus in the United States. New Engl. J. Med. 2020; 382: 929–36. https://doi.org/10.1056/nejmoa2001191
17. Chen L., Liu M., Zhang Z., et al. Ocular manifestations of a hospitalised patient with confirmed 2019 novel coronavirus disease. Br. J. Ophthalmol. 2020; 104: 748–51. https://doi.org/10.1136/bjophthalmol-2020-316304
18. Chan W.M., Yuen K.S., Fan D.S., et al. Tears and conjunctival scrapings for coronavirus in patients with SARS. Br. J. Ophthalmol. 2004; 88: 968–9. https://doi.org/10.1136/bjo2003.035931
19. Huang W.E., Lim B., Hsu C.C., et al. RT-LAMP for rapid diagnosis of coronavirus SARS-CoV-2. Microb Biotechnol. 2020; 13: 950–6. https://doi.org/10.1111/1751-7915.13586
20. Chen Y., Liu Q., Guo D. Emerging coronaviruses: Genome structure, replication, and pathogenesis. J. Med.Virol. 2020; 92: 418–23. https://doi.org/10.1002/jmv.25681
21. Robbins S.G., Detrick B., Hooks J.J. Retinopathy following intravitreal injection of mice with MHV strain JHM. Adv. Exp. Med. Biol. 1990; 276: 519–24. https://doi.org/10.1007/978-1-4684-5823-7_72
22. Hooks J.J., Percopo C., Wang Y., Detrick B. Retina and retinal pigment epithelial cell autoantibodies are produced during murine coronavirus retinopathy. J. Immunol. 1993; 151: 3381–9.
23. Shindler K.S., Kenyon L.C., Dutt M., et al. Experimental optic neuritis induced by a demyelinating strain of mouse hepatitis virus. J. Virol. 2008; 82 (17): 8882–6. https://doi.org/10.1128/JVI.00920-08
24. Guan W.J., Ni Z.Y., Hu Y., et al. Clinical characteristics of coronavirus disease 2019 in China. N. Engl. J. Med. 2020; 382 (18): 1708–20. https://doi.org/10.1056/NEJMoa2002032
25. Xia J., Tong J., Liu M., Shen Y., Guo D. Evaluation of coronavirus in tears and conjunctival secretions of patients with SARSCoV-2 infection. J. Med. Virol. 2020; 92 (6): 589–94. https://doi.org/10.1002/jmv.25725
26. Zhang X., Chen X., Chen L., et al. The infection evidence of SARS-COV-2 in ocular surface: a single center cross-sectional study. MedRxiv. 2020. https://doi.org/10.1101/2020.02.26.20027938
27. Wu P., Duan F., Luo C., et al. Characteristics of ocular findings of patients with coronavirus disease 2019 (COVID-19) in Hubei Province, China. JAMA Ophthalmol. 2020; 138 (5): 575. https://doi.org/10.1001/jamaophthalmol
28. Cheema M., Aghazadeh H., Nazarali S., et al. Keratoconjunctivitis as the initial medical presentation of the novel coronavirus disease 2019 (COVID-19). Canadian journal of ophthalmology. 2020; 55 (4): 125–9. https://doi.org/10.1016/j.jcjo.2020.03.003
29. Xie H.T., Jiang S.Y., Xu K.K., et al. SARS-CoV-2 in the ocular surface of COVID-19 patients. Eye and Vision. 2020; 7: 1–3. https://doi.org/10.1186/s40662-020-00189-0
30. Li J.O., Lam D.S.C., Chen Y., Ting D.S.W. Novel coronavirus disease 2019 (COVID-19): The importance of recognising possible early ocular manifestation and using protective eyewear. Br. J. Ophthalmol. 2020; 104 (3): 297–8. https://doi.org/10.1136/bjophthalmol-2020-315994
31. Tong T.R., Lam B.H., Ng T.K., et al. Conjunctiva-upper respiratory tract irrigation for early diagnosis of severe acute respiratory syndrome. J. Clin. Microbiol. 2003; 41: 5352. https://doi.org/10.1128/jcm.41.11.5352.2003
32. Falzarano D., de Wit E., Feldmann F., et al. Infection with MERS-CoV causes lethal pneumonia in the common marmoset. PLoS pathogens. 2014; 10 (9). https://doi.org/10.1371/journal.ppat.1004431
33. Ranjan R., Ranjan S. Ocular pathology: role of emerging viruses in the AsiaPacific region — a review. The Asia-Pacific Journal of Ophthalmology. 2014; 3 (5): 299–307. https://doi.org/10.1097/apo.0000000000000021
34. Jun I.S.Y., Anderson D.E., Kang A.E.Z., et al. Assessing viral shedding and infectivity of tears in coronavirus disease 2019 (COVID-19) patients. Ophthalmology. 2020; 127 (7): 977–9. https://doi.org/10.1016/j.ophtha.2020.03.026
35. Neroev V.V., Krichevskaya G.I., Balatskaya N.V. COVID-19 and problems of ophthalmology. Russian ophthalmological journal. 2020; 13 (4): 99–104 (in Russian). https://doi.org/10.21516/2072-0076-2020-13-4-99-104
36. Interim guidelines: prevention, diagnosis and treatment of new coronavirus infection (COVID-19). Ver. 9 (26.10.20) (in Russian). https://static-0.minzdrav.gov.ru/system/attachments/attaches/000/052/550/original/МР_COVID19_%28v9%29.pdf?1603788097
37. Marmor M.F. COVID-19 and Chloroquine/Hydroxychloroquine: Is there ophthalmological concern? Am. Journ. of Ophthalmol. 2020; 213: А3–А4.https://doi.org/10.1016/j.ajo.2020.03.028
38. Devaux C.A., Rolain J.-M., Colson P., Raoult D. New insights on the antiviral effects of chloroquine against coronavirus: what to expect for COVID-19? Int. J. Antimicrob. Agents 2020; 55 (5): 105938. https://doi.org/10.1016/j.ijantimicag.2020.105938
39. Cambiaggi A. Unusual ocular lesions in a case of systemic lupus erythematosus. AMA. Arch. Ophthalmol. 1957; 57: 451–3. https://doi.org/10.1001/archopht.1957.00930050463019
40. Kazaryan A., Ponomareva E. Ocular manifestations of toxic effects of hydroxychloroquine. Part 1. Russian оphthalmological journal. 2011; 4: 96–100 (in Russian).
41. Marmor M., Kellner U., Lai T.Y., Melles R.B., Mieler W.F. Recommendations on screening for chloroquine and hydroxychloroquine retinopathy. Ophthalmology. 2016; 123 (6): 1386–94. https://doi.org/10.1016/j.ophtha.2016.01.058
42. Ojeda A., Miers Granada G.R. Ocular toxicity of hydroxychloroquine. Revista Paraguaya de Reumatolog a. 2019; 5 (2): 63–9. https://doi.org/10.18004/rpr/2019.05.02.63-69
43. Budzinskaya M.V., Durzhinskaya M.H. Differential diagnosis of hydroxychloroquine-induced retinal damage. Vestnik oftal’mologii. 2020; 136 (4): 265–71 (in Russian). https://doi.org/10.17116/oftalma2020136042265
44. Ahn S.J., Ryu S.J., Joung J.Y., Lee B.R. Choroidal thinning associated with hydroxychloroquine retinopathy. Am. Journ. of Ophthalmol. 2017; 183: 56–64. https://doi.org/10.1016/j.ajo.2017.08.02233
45. Duncker G., Schmiederer M., Bredehorn T. Chloroquine induced lipidosis in the rat retina: a functional and morphological study. Ophthalmologica. 1995; 209 (2): 79–83. https://doi.org/10.1159/000310585
46. Shroyer N.F., Lewis R.A., Lupski J.R. Analysis of the ABCR(ABCA4) gene in 4-aminoquinoline retinopathy: is retinal toxicity by chloroquine and hydroxychloroquine related to Stargardt disease? Am. J. Opthalmol. 2001; 131 (6): 761–6. https://doi.org/10.1016/s0002-9394(01)00838-8
47. Mouraviev V.Yu., Turgieva E.P. Therapy by antimalaria (aminoquinoline) drugs and of ocular safety. Rheumatology Science and Practice. 2002; 40 (2): 3 (in Russian). https://doi.org/10.14412/1995-4484-2002-70
48. Chen E., Brown D.M., Benz M.S., et al. Spectral domain optical coherence tomography as an effective screening test for hydroxychloroquine retinopathy (the “flying saucer” sign). Clinical Ophthalmology. 2010; 4: 1151–8. https://doi.org/10.2147/OPTH.S14257
49. Hecquet S., Rabie, M. B., Lepelley M., et al. FRI0153 ophthalmological adverse events under JAK inhibitors in patients with rheumatoid arthritis: case analysis of the European pharmacovigilance database. Annals of the Rheumatic Diseases. 2019; 78: 748. http://dx.doi.org/10.1136/annrheumdis-2019-eular.3811
50. Nasonov E.L., Mazurov V.I., Usacheva Yu.V., et al. Developments of Russian original biological agents for the treatment of immune inflammatory rheumatic diseases. Rheumatology Science and Practice. 2017; 55 (2): 201–10 (in Russian). https://doi.org/10.14412/1995-4484-2017-201-210
51. Fernández-Ferreiro A., Santiago-Varela M., Gil-Martínez M., et al. Ocular safety comparison of non-steroidal anti-inflammatory eye drops used in pseudophakic cystoid macular edema prevention. Intern. Journal of Pharmaceutics. 2015; 495 (2): 680–91. https://doi.org/10.1016/j.ijpharm.2015.09.058
52. Morozov V.V., Yakovlev A.A. Pharmacotherapy of eye diseases. Moscow: Medpress-inform. 2009 (in Russian).
53. Krasnova T.V., Kanyukov I.V. Retinopathic accessory drug-induced action and measures of prevention. Bulletin of the Orenburg state University. 2004; 38: 202–5 (in Russian).
54. Максименя Г.Г. Офтальмотоксические эффекты лекарственных препаратов. Офтальмология. Восточная Европа. 2012 (1): 77–86. [Maksimenya G.G. Ophthalmotoxic effects of medicinal preparations. Ophthalmology. Eastern Europe. 2012; (1): 77–86 (in Russian)].
55. Lindsey A.E., Townes-Anderson E. Antibiotics reduce retinal cell survival in vitro. Neurotoxicity research. 2018; 33 (4): 781–9. https://doi.org/10.1007/s12640-017-9826-6
56. Maychuk D.Yu., Atlas S.N., Loshkareva A.O. Ocular manifestations of coronavirus infection COVID-19 (clinical observation). Vestnik oftal’mologii. 2020; 136 (4): 118–23 (in Russian). https://doi.org/10.17116/oftalma2020136041118]
Review
For citations:
Neroev V.V., Kiseleva T.N., Eliseeva E.K. Ophthalmological aspects of coronavirus infections. Russian Ophthalmological Journal. 2021;14(1):7-14. (In Russ.) https://doi.org/10.21516/2072-0076-2021-14-1-7-14