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Review

Evidence of SARS-CoV-2 Transmission Through the Ocular Route

, ORCID Icon &
Pages 687-696 | Published online: 18 Feb 2021

References

  • Novel Coronavirus (2019-nCoV) situation report – 22. World Health Organization (WHO). Available from: https://www.who.int/docs/default-source/coronaviruse/situation-reports/20200211-sitrep-22-ncov.pdf?sfvrsn=fb6d49b1_2. Accessed February 11, 2020.
  • Gorbalenya AE, Baker SC, Baric RS, et al. The species severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol. 2020;5(4):536–544.
  • WHO Director-General’s opening remarks at the media briefing on COVID-19-11 March 2020. World Health Organization (WHO). Available from: https://www.who.int/dg/speeches/detail/who-director-general-s-opening-remarks-at-the-media-briefing-on-covid-19—11-march-2020. Accessed March 11, 2020.
  • Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579(7798):270–273. doi:10.1038/s41586-020-2012-7
  • Lu R, Zhao X, Li J, et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet (London, England). 2020;395(10224):565–574. doi:10.1016/S0140-6736(20)30251-8
  • Chan JF, Kok KH, Zhu Z, et al. Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg Microbes Infect. 2020;9(1):221–236. doi:10.1080/22221751.2020.1719902
  • Jin Y, Yang H, Ji W, et al. Virology, epidemiology, pathogenesis, and control of COVID-19. Viruses. 2020;12(4):372. doi:10.3390/v12040372
  • Hossain MG, Javed A, Akter S, Saha S. SARS-CoV-2 host diversity: an update of natural infections and experimental evidence. J Microbiol Immunol Infect. 2020. doi:10.1016/j.jmii.2020.06.006
  • The Chinese Center for Disease Control and Prevention isolated the new coronavirus from the outer packaging of cold chain food. Chinese Center for Disease Control and Prevention (CDC). Available from: http://www.chinacdc.cn/yw_9324/202010/t20201017_222144.html. Accessed October 17, 2020.
  • Tsatsakis A, Calina D, Falzone L, et al. SARS-CoV-2 pathophysiology and its clinical implications: an integrative overview of the pharmacotherapeutic management of COVID-19. Food Chem Toxicol. 2020;146:111769. doi:10.1016/j.fct.2020.111769
  • Khalili M, Chegeni M, Javadi S, Farokhnia M, Sharifi H, Karamouzian M. Therapeutic interventions for COVID-19: a living overview of reviews. Ther Adv Respir Dis. 2020;14:1753466620976021. doi:10.1177/1753466620976021
  • WHO Coronavirus disease (COVID-19) dashboard. World Health Organization (WHO). Available from: https://covid19.who.int/. Accessed January 8, 2021.
  • China’s new coronavirus vaccine is approved for marketing! The State Council of the People’s Republic of China. Available from: http://www.gov.cn/xinwen/2020-12/31/content_5575757.htm. Accessed December 31, 2020.
  • FDA takes key action in fight against COVID-19 by issuing emergency use authorization for first COVID-19 vaccine. The U.S. Food and Drug Administration. Available from: https://www.fda.gov/news-events/press-announcements/fda-takes-key-action-fight-against-covid-19-issuing-emergency-use-authorization-first-covid-19. Accessed December 11, 2020.
  • Lu CW, Liu XF, Jia ZF. 2019-nCoV transmission through the ocular surface must not be ignored. Lancet (London, England). 2020;395(10224):e39. doi:10.1016/S0140-6736(20)30313-5
  • Casalino G, Monaco G, Di Sarro PP, David A, Scialdone A. Coronavirus disease 2019 presenting with conjunctivitis as the first symptom. Eye (London, England). 2020;34(7):1235–1236. doi:10.1038/s41433-020-0909-x
  • Chavis A, Bakken H, Ellenby M, Hasan R. COVID-19 and telehealth: prevention of exposure in a medically complex patient with a mild presentation. Article in press. J Adolesc Health. 2020;67(3):456–458. doi:10.1016/j.jadohealth.2020.06.001
  • Hui KP, Peiris M, Nicholls JM, Chan MC. SARS-CoV-2 infection in conjunctival tissue - authors’ reply. Lancet Respir Med. 2020;8(7):e58. doi:10.1016/S2213-2600(20)30273-3
  • Liu YC, Ang M, Ong HS, Wong TY, Mehta JS. SARS-CoV-2 infection in conjunctival tissue. Lancet Respir Med. 2020;8(7):e57. doi:10.1016/S2213-2600(20)30272-1
  • Machhi J, Herskovitz J, Senan AM, et al. The natural history, pathobiology, and clinical manifestations of SARS-CoV-2 infections. J Neuroimmune Pharmacol. 2020;15:1–28. doi:10.1007/s11481-019-09901-x
  • 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):271–280 e8. doi:10.1016/j.cell.2020.02.052
  • Sungnak W, Huang N, Becavin C, et al. SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Article. Nat Med. 2020;26(5):681–687. doi:10.1038/s41591-020-0868-6
  • Zhou L, Xu Z, Castiglione GM, Soiberman US, Eberhart CG, Duh EJ. ACE2 and TMPRSS2 are expressed on the human ocular surface, suggesting susceptibility to SARS-CoV-2 infection. Ocul Surf. 2020;18(4):537–544. doi:10.1016/j.jtos.2020.06.007
  • Roehrich H, Yuan C, Hou JH. Immunohistochemical study of SARS-CoV-2 viral entry factors in the cornea and ocular surface. Cornea. 2020;39(12):1556–1562. doi:10.1097/ICO.0000000000002509
  • Li S, Li D, Fang J, et al. SARS-CoV-2 receptor ACE2 is expressed in human conjunctival tissue, especially in diseased conjunctival tissue. Ocul Surf. 2020. doi:10.1016/j.jtos.2020.09.010
  • Holappa M, Vapaatalo H, Vaajanen A. Many faces of renin-angiotensin system – focus on eye. Open Ophthalmol J. 2017;11:122–142. doi:10.2174/1874364101711010122
  • Senanayake P, Drazba J, Shadrach K, et al. Angiotensin II and its receptor subtypes in the human retina. Invest Ophthalmol Vis Sci. 2007;48(7):3301–3311. doi:10.1167/iovs.06-1024
  • Luhtala S, Vaajanen A, Oksala O, Valjakka J, Vapaatalo H. Activities of angiotensin-converting enzymes ACE1 and ACE2 and inhibition by bioactive peptides in porcine ocular tissues. J Ocular Pharmacol Therap. 2009;25(1):23–28. doi:10.1089/jop.2008.0081
  • Cavalleri M, Brambati M, Starace V, et al. Ocular features and associated systemic findings in SARS-CoV-2 infection. Ocul Immunol Inflamm. 2020;28(6):916–921. doi:10.1080/09273948.2020.1781198
  • Ordas CM, Villacieros-Alvarez J, Pastor-Vivas AI, Corrales-Benitez A. Concurrent tonic pupil and trochlear nerve palsy in COVID-19. J Neurovirol. 2020;26:970–972. doi:10.1007/s13365-020-00909-1
  • Otaif W, Al Somali AI, Al Habash A. Episcleritis as a possible presenting sign of the novel coronavirus disease: a case report. Am J Ophthalmol. 2020;20:100917. doi:10.1016/j.ajoc.2020.100917
  • Invernizzi A, Pellegrini M, Messenio D, et al. Impending central retinal vein occlusion in a patient with Coronavirus disease 2019 (COVID-19). Ocul Immunol Inflamm. 2020;28(8):1290–1292. doi:10.1080/09273948.2020.1807023
  • Benito-Pascual B, Gegundez JA, Diaz-Valle D, et al. Panuveitis and optic neuritis as a possible initial presentation of the novel Coronavirus disease 2019 (COVID-19). Ocul Immunol Inflamm. 2020;28(6):922–925. doi:10.1080/09273948.2020.1792512
  • Tisdale AK, Chwalisz B. Neuro-ophthalmic manifestations of coronavirus disease 19. Curr Opin Ophthalmol. 2020;Publish Ahead of Print. doi:10.1097/ICU.0000000000000707
  • Li X, Wang M, Dai J, Wang W, Yang Y, Jin W. Novel coronavirus disease with conjunctivitis and conjunctivitis as first symptom: two cases report. Zhonghua Shiyan Yanke Zazhi. 2020;38(4):318–321.
  • Zhang X, Chen X, Chen L, et al. The evidence of SARS-CoV-2 infection on ocular surface. Ocul Surf. 2020;18(3):360–362. doi:10.1016/j.jtos.2020.03.010
  • Ying NY, Idris NS, Muhamad R, Ahmad I. Coronavirus disease 2019 presenting as conjunctivitis. Korean J Fam Med. 2020. doi:10.4082/kjfm.20.0090
  • Daruich A, Martin D, Bremond-Gignac D. Ocular manifestation as first sign of Coronavirus disease 2019 (COVID-19): interest of telemedicine during the pandemic context. J Fr Ophtalmologie. 2020;43(5):389–391. doi:10.1016/j.jfo.2020.04.002
  • Cheema M, Aghazadeh H, Nazarali S, et al. Keratoconjunctivitis as the initial medical presentation of the novel coronavirus disease 2019 (COVID-19). Can J Ophthalmol. 2020;55(4):e125–e129. doi:10.1016/j.jcjo.2020.03.003
  • Salducci M, La Torre G. COVID-19 emergency in the cruise’s ship: a case report of conjunctivitis. Clin Ter. 2020;171(3):e189–e191. doi:10.7417/CT.2020.2212
  • Scalinci SZ, Trovato Battagliola E. Conjunctivitis can be the only presenting sign and symptom of COVID-19. IDCases. 2020;20:e00774. doi:10.1016/j.idcr.2020.e00774
  • Wu P, Liang L, Chen C, Nie S. A child confirmed COVID-19 with only symptoms of conjunctivitis and eyelid dermatitis. Letter. Graefe’s Arch Clin Exp Ophthalmol. 2020;258(7):1565–1566. doi:10.1007/s00417-020-04708-6
  • COVID-19 testing overview. Centers for Disease Control and Prevention. Available from: https://www.cdc.gov/coronavirus/2019-ncov/symptoms-testing/testing.html. Accessed December 7, 2020.
  • Colavita F, Lapa D, Carletti F, et al. SARS-CoV-2 isolation from ocular secretions of a patient with COVID-19 in Italy with prolonged viral RNA detection. Ann Intern Med. 2020;173(3):242–243. doi:10.7326/M20-1176
  • Hui KPY, Cheung MC, Perera R, et al. Tropism, replication competence, and innate immune responses of the coronavirus SARS-CoV-2 in human respiratory tract and conjunctiva: an analysis in ex-vivo and in-vitro cultures. Lancet Respir Med. 2020;8(7):687–695. doi:10.1016/S2213-2600(20)30193-4
  • 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):97. doi:10.1186/s12985-020-01370-6
  • Sindhuja K, Lomi N, Asif MI, Tandon R. Clinical profile and prevalence of conjunctivitis in mild COVID-19 patients in a tertiary care COVID-19 hospital: a retrospective cross-sectional study. Indian J Ophthalmol. 2020;68(8):1546–1550. doi:10.4103/ijo.IJO_1319_20
  • Chen L, Deng C, Chen X, et al. Ocular manifestations and clinical characteristics of 535 cases of COVID-19 in Wuhan, China: a cross-sectional study. Acta Ophthalmol. 2020;98. Doi:10.1111/aos.14472
  • Workman AD, Jafari A, Welling DB, et al. Airborne aerosol generation during endonasal procedures in the era of COVID-19: risks and recommendations. Otolaryngol. Head Neck Surg. 2020;163(3):465–470. doi:10.1177/0194599820931805
  • Jayaweera M, Perera H, Gunawardana B, Manatunge J. Transmission of COVID-19 virus by droplets and aerosols: a critical review on the unresolved dichotomy. Environ Res. 2020;188:109819. doi:10.1016/j.envres.2020.109819
  • Tang S, Mao Y, Jones RM, et al. Aerosol transmission of SARS-CoV-2? Evidence, prevention and control. Environ Int. 2020;144:106039. doi:10.1016/j.envint.2020.106039
  • Liyanage S, Ramasamy P, Elhaddad O, Darcy K, Hudson A, Keller J. Assessing visible aerosol generation during vitrectomy in the era of Covid-19. Eye (London, England). 2020;1–4.
  • Okada M, Sousa DC, Fabinyi DCA, et al. Vitrectomy as an aerosol-generating procedure in the time of COVID-19: the VAPOR study. Ophthalmol Retina. 2020.
  • Khamar P, Shetty R, Balakrishnan N, et al. Quantitative shadowgraphy of aerosol and droplet creation during oscillatory motion of the microkeratome amid COVID-19 and other infectious diseases. Article in Press. J Cataract Refract Surg. 2020;46(10):1416–1421. doi:10.1097/j.jcrs.0000000000000326
  • Darcy K, Elhaddad O, Achiron A, et al. Reducing visible aerosol generation during phacoemulsification in the era of Covid-19. Eye (London, England). 2020;1–6.
  • McGhee CNJ, Dean S, Freundlich SEN, et al. Microdroplet and spatter contamination during phacoemulsification cataract surgery in the era of COVID −19. Clin Experiment Ophthalmol. 2020;48:1168–1174. doi:10.1111/ceo.13861
  • Workman AD, Welling DB, Carter BS, et al. Endonasal instrumentation and aerosolization risk in the era of COVID-19: simulation, literature review, and proposed mitigation strategies. Int Forum Allergy Rhinol. 2020;10(7):798–805. doi:10.1002/alr.22577
  • Chari DA, Workman AD, Chen JX, et al. Aerosol dispersion during mastoidectomy and custom mitigation strategies for otologic surgery in the COVID-19 era. Otolaryngol. Head Neck Surg. 2020;194599820941835.
  • Tang Y, Li C, Chen Y, et al. Effect of Intraocular Pressure on Aerosol Density Generated by Noncontact Tonometer Measurement. J Glaucoma. 2020;29(11):1001–1005. doi:10.1097/IJG.0000000000001669
  • Aytogan H, Ayintap E, Ozkalay Yilmaz N. Detection of Coronavirus disease 2019 viral material on environmental surfaces of an ophthalmology examination room. JAMA Ophthalmol. 2020;138(9):990–993. doi:10.1001/jamaophthalmol.2020.3154
  • Ong SC, Razali MAB, Shaffiee L, et al. Do slit-lamp shields and face masks protect ophthalmologists amidst COVID-19? Ophthalmology. 2020;127(10):1427–1429. doi:10.1016/j.ophtha.2020.06.031
  • Bostanci Ceran B, Karakoc A, Taciroglu E. Airborne pathogen projection during ophthalmic examination. Graefe’s Arch Clin Exp Ophthalmol. 2020;258(10):2275–2282. doi:10.1007/s00417-020-04815-4
  • van Doremalen N, Bushmaker T, Morris DH, et al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N Engl J Med. 2020;382(16):1564–1567. doi:10.1056/NEJMc2004973
  • Deng W, Bao L, Gao H, et al. Ocular conjunctival inoculation of SARS-CoV-2 can cause mild COVID-19 in rhesus macaques. Nat Commun. 2020;11(1):4400. doi:10.1038/s41467-020-18149-6
  • Paulsen F, Thale A, Kohla G, et al. Functional anatomy of human lacrimal duct epithelium. Anat Embryol (Berl). 1998;198(1):1–12. doi:10.1007/s004290050160
  • Hu Y, Chen T, Liu M, et al. Positive detection of SARS-CoV-2 combined HSV1 and HHV6B virus nucleic acid in tear and conjunctival secretions of a non-conjunctivitis COVID-19 patient with obstruction of common lacrimal duct. Acta Ophthalmol. 2020;98:859–863. doi:10.1111/aos.14456
  • Valente P, Iarossi G, Federici M, et al. Ocular manifestations and viral shedding in tears of pediatric patients with coronavirus disease 2019: a preliminary report. J AAPOS. 2020;24(4):212–215. doi:10.1016/j.jaapos.2020.05.002
  • Casagrande M, Fitzek A, Puschel K, et al. Detection of SARS-CoV-2 in human retinal biopsies of deceased COVID-19 patients. Ocul Immunol Inflamm. 2020;28(5):721–725. doi:10.1080/09273948.2020.1770301
  • 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;bjophthalmol-2020-316263. Doi:10.1136/bjophthalmol-2020-316263
  • de Figueiredo CS, Raony Í, Giestal-de-Araujo E. SARS-CoV-2 targeting the retina: host-virus interaction and possible mechanisms of viral tropism. Ocul Immunol Inflamm. 2020;1–4.
  • Coroneo MT. The eye as the discrete but defensible portal of coronavirus infection. review. Ocul Surf. 2020. doi:10.1016/j.jtos.2020.05.011
  • Barnett BP, Wahlin K, Krawczyk M, et al. Potential of ocular transmission of SARS-CoV-2: a review. Vision (Basel, Switzerland). 2020;4(3). doi:10.3390/vision4030040.
  • Güemes-Villahoz N, Burgos-Blasco B, Vidal-Villegas B, et al. Novel insights into the transmission of SARS-CoV-2 through the ocular surface and its detection in tears and conjunctival secretions: a review. Adv Ther. 2020;37(10):4086–4095. doi:10.1007/s12325-020-01442-7
  • Arora R, Goel R, Kumar S, et al. Evaluation of SARS-CoV-2 in tears of patients with moderate to severe COVID-19. Ophthalmology. 2020. doi:10.1016/j.ophtha.2020.08.029
  • Atum M, Boz AAE, Cakir B, et al. Evaluation of conjunctival swab PCR results in patients with SARS-CoV-2 infection. Ocul Immunol Inflamm. 2020;28(5):745–748. doi:10.1080/09273948.2020.1775261
  • Deng C, Yang Y, Chen H, et al. Low risk of SARS-CoV-2 transmission through the ocular surface. Acta Ophthalmol. 2020;98(7):e926–e927. doi:10.1111/aos.14471
  • Guemes-Villahoz N, Burgos-Blasco B, Arribi-Vilela A, et al. Detecting SARS-CoV-2 RNA in conjunctival secretions: is it a valuable diagnostic method of COVID-19? J Med Virol. 2020.
  • Karimi S, Arabi A, Shahraki T, Safi S. Detection of severe acute respiratory syndrome Coronavirus-2 in the tears of patients with Coronavirus disease 2019. Eye (London, England). 2020;34(7):1220–1223. doi:10.1038/s41433-020-0965-2
  • Kaya H, Caliskan A, Okul M, Sari T, Akbudak IH. Detection of SARS-CoV-2 in the tears and conjunctival secretions of Coronavirus disease 2019 patients. Article. J Infect Dev Ctries. 2020;14(9):977–981. doi:10.3855/jidc.13224
  • Kumar K, Prakash AA, Gangasagara SB, et al. Presence of viral RNA of SARS-CoV-2 in conjunctival swab specimens of COVID-19 patients. Indian J Ophthalmol. 2020;68(6):1015–1017. doi:10.4103/ijo.IJO_1287_20
  • Li X, Wang M, Chen C, Yang A, Jin W. Ophthalmologists’ strategy for the prevention and control of coronavirus pneumonia with conjunctivitis or with conjunctivitis as the first symptom. Article. Zhonghua Shiyan Yanke Zazhi. 2020;38(3):276–280.
  • Li X, Chan JF, Li KK, et al. Detection of SARS-CoV-2 in conjunctival secretions from patients without ocular symptoms. Infection. 2020. doi:10.1007/s15010-020-01524-2
  • Liang L, Wu P. There may be virus in conjunctival secretion of patients with COVID-19. Acta Ophthalmol. 2020;98(3):223. doi:10.1111/aos.14413
  • Mahmoud H, Ammar H, El Rashidy A, Ali AH, Hefny HM, Mounir A. Assessment of coronavirus in the conjunctival tears and secretions in patients with SARS-CoV-2 infection in Sohag Province, Egypt. Clin Ophthalmol (Auckland, NZ). 2020;14:2701–2708. doi:10.2147/OPTH.S270006
  • 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):575–578. doi:10.1001/jamaophthalmol.2020.1291
  • Xia J, Tong J, Liu M, Shen Y, Guo D. Evaluation of coronavirus in tears and conjunctival secretions of patients with SARS-CoV-2 infection. J Med Virol. 2020;92(6):589–594. doi:10.1002/jmv.25725
  • Xie HT, Jiang SY, Xu KK, et al. SARS-CoV-2 in the ocular surface of COVID-19 patients. Eye Vision (London, England). 2020;7:23. doi:10.1186/s40662-020-00189-0
  • Zhou Y, Duan C, Zeng Y, et al. Ocular findings and proportion with conjunctival SARS-COV-2 in COVID-19 patients. Ophthalmology. 2020;127(7):982–983. doi:10.1016/j.ophtha.2020.04.028
  • Dutescu RM, Banasik P, Schildgen O, Schrage N, Uthoff D. Detection of Coronavirus in tear samples of hospitalized patients with confirmed SARS-CoV-2 from oropharyngeal swabs. Cornea. 2020;Publish Ahead of Print. doi:10.1097/ICO.0000000000002562
  • Fang Z, Zhang Y, Hang C, Ai J, Li S, Zhang W. Comparisons of viral shedding time of SARS-CoV-2 of different samples in ICU and non-ICU patients. Letter. J Infect. 2020;81(1):147–178. doi:10.1016/j.jinf.2020.03.013
  • Huang Y, Chen S, Yang Z, et al. SARS-CoV-2 viral load in clinical samples from critically ill patients. Am J Respir Crit Care Med. 2020;201(11):1435–1438. doi:10.1164/rccm.202003-0572LE