SARS-CoV-2 Isolation From Ocular Secretions of a Patient With COVID-19 in Italy With Prolonged Viral RNA Detection
Authors: Francesca Colavita, Daniele Lapa, Fabrizio Carletti, Eleonora Lalle, Licia Bordi, Patrizia Marsella, Emanuele Nicastri, Nazario Bevilacqua, Maria Letizia Giancola, Angela Corpolongo, Giuseppe Ippolito, Maria Rosaria Capobianchi, Concetta Castilletti
Journal: Annals of Internal Medicine (2020)

Letters17 April 2020SARS-CoV-2 Isolation From Ocular Secretions of a Patient With COVID-19 in Italy With Prolonged Viral RNA DetectionFREEFrancesca Colavita, PhD, Daniele Lapa, PhD, Fabrizio Carletti, PhD, Eleonora Lalle, PhD, Licia Bordi, PhD, Patrizia Marsella, PhD, Emanuele Nicastri, MD, Nazario Bevilacqua, MD, Maria Letizia Giancola, MD, Angela Corpolongo, MD, Giuseppe Ippolito, MD, Maria Rosaria Capobianchi, PhD, and Concetta Castilletti, PhDFrancesca Colavita, PhDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Daniele Lapa, PhDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Fabrizio Carletti, PhDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Eleonora Lalle, PhDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Licia Bordi, PhDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Patrizia Marsella, PhDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Emanuele Nicastri, MDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Nazario Bevilacqua, MDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Maria Letizia Giancola, MDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Angela Corpolongo, MDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Giuseppe Ippolito, MDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), Maria Rosaria Capobianchi, PhDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.), and Concetta Castilletti, PhDNational Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.)Author, Article, and Disclosure Informationhttps://doi.org/10.7326/M20-1176 SectionsAboutVisual AbstractPDF ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinkedInRedditEmail Background: Coronavirus disease 2019 (COVID-19), the disease caused by the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that originated in China in December 2019, was recently recognized as pandemic threat by the World Health Organization, with the potential of rapidly overloading health care systems and causing substantial mortality worldwide (www.who.int/dg/speeches/detail/who-director-general-s-opening-remarks-at-the-media-briefing-on-covid-19---11-march-2020). Human-to-human transmission occurs mainly through respiratory droplets, but other routes are under investigation, because SARS-CoV-2 has been detected in several body fluids (1). So far, few data are available on ocular samples from patients with COVID-19, although conjunctivitis has been occasionally reported among COVID-19 symptoms, similar to infections caused by other human coronaviruses (2, 3). During the SARS epidemic, eye exposure to infectious fluids was associated with an increased risk for SARS-CoV transmission to health care workers (3, 4). Although SARS-CoV RNA was occasionally found in ocular specimens during the early phase of illness, its infectivity is unknown (2, 3).With regard to COVID-19, unprotected ocular exposure was thought to be responsible for infections that occurred in the Wuhan Fever Clinic in January 2020 (3, 4); in addition, SARS-CoV-2 RNA was detected in conjunctival secretions collected from the only patient with conjunctivitis out of 30 patients with COVID-19 from a hospital in China (5). However, further studies are needed to evaluate the infectious potential of the SARS-CoV-2 RNA detected in the ocular specimens and to determine whether transmission may occur through ocular secretions (3, 4).Objective: To present the early detection of infectious SARS-CoV-2 in ocular fluids from a patient with the first confirmed case of COVID-19 in Italy, who had been hospitalized at the National Institute for Infectious Diseases “L. Spallanzani” (INMI) in Rome.Methods and Findings: The patient, a 65-year-old woman, travelled from Wuhan, China, to Italy on 23 January 2020 and was admitted on 29 January 2020, 1 day after symptom onset. At admission to the high isolation unit at INMI, she presented with nonproductive cough, sore throat, coryza, and bilateral conjunctivitis. She had no fever until day 4, when fever (38 °C), nausea, and vomiting began. Infection with SARS-CoV-2 was confirmed by performing real-time reverse transcription polymerase chain reaction (RT-PCR) assay on sputum samples (cycle threshold value [Ct], 16.1) on the admission day, followed by viral M gene sequencing (GenBank accession number MT008022), and virus isolation on Vero E6 cell line (2019-nCoV/Italy-INMI1). The full genome sequence was obtained from either clinical sample or culture isolate (GISAID accession numbers EPI_ISL_410545 and EPI_ISL_410546). At admission, no other respiratory infections were detected (QIAstat-Dx Respiratory Panel; Qiagen).On day 3 after hospital admission, owing to the persistence of conjunctivitis, an ocular swab was collected and viral RNA was detected (Ct, 21.6). Subsequent ocular samples collected with almost daily frequency resulted positive up to day 21, with declining virus concentration (increased Ct values). Conjunctivitis greatly improved at day 15 and apparently resolved at day 20.Five days after it became undetectable, SARS-CoV-2 RNA was detected again (Ct, 36.25) in the ocular swab sample collected at day 27 (Table). SARS-CoV-2 RNA was detected in ocular swabs days after it was undetectable in nasal swabs (Table). In addition, the Ct values detected in the late ocular samples were lower than those observed in the nasal swabs (Table), suggesting sustained replication in conjunctiva. With the aim of demonstrating that viral genomes detected in ocular swabs represented infectious virus, the first RNA-positive ocular sample was inoculated in Vero E6 cells, and cytopathic effect was observed 5 days postinoculum. Viral replication was confirmed by real-time RT-PCR on RNA purified from spent cell growth medium.Table. Viral Load in Ocular and Nasal Swabs From the First SARS-CoV-2 Infection Detected in Italy*Discussion: We found that ocular fluids from SARS-CoV-2–infected patients may contain infectious virus, and hence may be a potential source of infection. These findings highlight the importance of control measures, such as avoiding touching the nose, mouth, and eyes and frequent hand washing. A related implication is the importance of appropriate use of personal protective equipment for ophthalmologists during clinical examination, because ocular mucosa may be not only a site of virus entry but also a source of contagion. Furthermore, we observed that ocular involvement of SARS-CoV-2 may occur early in the COVID-19 course, suggesting that measures to prevent transmission via this route must be implemented as early as possible.Future studies are needed to define the human ocular cell types capable of supporting viral replication and the mechanisms underlying ocular tropism of SARS-CoV-2.Appendix: INMI COVID-19 Study GroupMaria Alessandra Abbonizio, Chiara Agrati, Fabrizio Albarello, Gioia Amadei, Alessandra Amendola, Mario Antonini, Raffaella Barbaro, Barbara Bartolini, Martina Benigni, Nazario Bevilacqua, Licia Bordi, Veronica Bordoni, Marta Branca, Paolo Campioni, Maria Rosaria Capobianchi, Cinzia Caporale, Ilaria Caravella, Fabrizio Carletti, Concetta Castilletti, Roberta Chiappini, Carmine Ciaralli, Francesca Colavita, Angela Corpolongo, Massimo Cristofaro, Salvatore Curiale, Alessandra D'Abramo, Cristina Dantimi, Alessia De Angelis, Giada De Angelis, Rachele Di Lorenzo, Federica Di Stefano, Federica Ferraro, Lorena Fiorentini, Andrea Frustaci, Paola Gallì, Gabriele Garotto, Maria Letizia Giancola, Filippo Giansante, Emanuela Giombini, Maria Cristina Greci, Giuseppe Ippolito, Eleonora Lalle, Simone Lanini, Daniele Lapa, Luciana Lepore, Andrea Lucia, Franco Lufrani, Manuela Macchione, Alessandra Marani, Luisa Marchioni, Andrea Mariano, Maria Cristina Marini, Micaela Maritti, Giulia Matusali, Silvia Meschi, Francesco Messina, Chiara Montaldo, Silvia Murachelli, Emanuele Nicastri, Roberto Noto, Claudia Palazzolo, Emanuele Pallini, Virgilio Passeri, Federico Pelliccioni, Antonella Petrecchia, Ada Petrone, Nicola Petrosillo, Elisa Pianura, Maria Pisciotta, Silvia Pittalis, Costanza Proietti, Vincenzo Puro, Gabriele Rinonapoli, Martina Rueca, Alessandra Sacchi, Francesco Sanasi, Carmen Santagata, Silvana Scarcia, Vincenzo Schininà, Paola Scognamiglio, Laura Scorzolini, Giulia Stazi, Francesco Vaia, Francesco Vairo, Maria Beatrice Valli.References1. Wang W, Xu Y, Gao R, et al. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA. 2020 Mar 11 [Epub ahead of print]. [PMID: 32159775] doi:10.1001/jama.2020.3786 CrossrefMedlineGoogle Scholar2. Li JO, Lam DS, Chen Y, Ting DS. Novel coronavirus disease 2019 (COVID-19): The importance of recognising possible early ocular manifestation and using protective eyewear [Editorial]. Br J Ophthalmol. 2020;104:297-8. [PMID: 32086236] doi:10.1136/bjophthalmol-2020-315994 CrossrefMedlineGoogle Scholar3. Seah I, Agrawal R. Can the coronavirus disease 2019 (COVID-19) affect the eyes? A review of coronaviruses and ocular implications in humans and animals. Ocul Immunol Inflamm. 2020;28:391-5. [PMID: 32175797] doi:10.1080/09273948.2020.1738501 CrossrefMedlineGoogle Scholar4. Lu CW, Liu XF, Jia ZF. 2019-nCoV transmission through the ocular surface must not be ignored [Letter]. Lancet. 2020;395:e39. [PMID: 32035510] doi:10.1016/S0140-6736(20)30313-5 CrossrefMedlineGoogle Scholar5. 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 Feb 26. [Epub ahead of print]. [PMID: 32100876] doi:10.1002/jmv.25725 CrossrefMedlineGoogle Scholar Comments 0 Comments Sign In to Submit A Comment Lorenzo Loffredo, Giulia Tiscione and Francesco VioliDepartment of Clinical, Internal Medicine, Anesthesiology and Cardiovascular Sciences, Sapienza University of Rome, Italy.27 April 2020 Conjunctivitis and COVID-19: true or casual association? The coronavirus disease 2019 (COVID‐19) represents a worldwide pandemic characterized by potentially severe complications(1). In a recent brief report, Colavita et al. described the case of a 65-year-old woman admitted to the hospital with COVID-19, and bilateral conjunctivitis with the virus in the tears(2). The Authors hypothesized that the viral ocular involvement may occur early in the COVID-19 course, that the virus may replicate in the conjunctiva and represent a potential source of infection(2). This could be plausible but other possibilities must be considered.Conjunctivitis may not be the first sign of infection but the consequence of a systemic viral manifestation. To support this possibility, Chen et al. reported that acute conjunctivitis can occur also in the middle phase of COVID-19; in particular, these authors reported the case of conjunctivitis in a patient with SARS-CoV-2 infection arising 13 days after onset(3). Experimental studies in feline and mouse infected by Coronavirus showed conjunctivitis and virus isolates from conjunctival swabs after infection onset, suggesting that this eye manifestation could be related to inflammation and vasculitis(4). Furthermore, considering that the nasolacrimal duct links the lacrimal sac of the eye to the nasal cavity, the COVID-19 could enter from respiratory tract and infect the eye later(5). This could be favoured by the higher expression of angiotensin-converting enzyme 2, that represent the receptor used by the virus to enter in the human cells, in epithelial cells of the respiratory surface compared to the conjunctiva(5).In conclusion, future studies are necessary to better understand the role of conjunctiva in COVID-19.References:1. Lipsitch M, Swerdlow DL, Finelli L. Defining the Epidemiology of Covid-19 - Studies Needed. N Engl J Med. 2020;382(13):1194-6.2. Colavita F, Lapa D, Carletti F, Lalle E, Bordi L, Marsella P, 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. 2020.3. 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. 2020.4. Seah I, Agrawal R. Can the Coronavirus Disease 2019 (COVID-19) Affect the Eyes? A Review of Coronaviruses and Ocular Implications in Humans and Animals. Ocul Immunol Inflamm. 2020;28(3):391-5.5. Guo D, Xia J, Shen Y, Tong J. SARS-CoV-2 may be related to conjunctivitis but not necessarily spread through the conjunctiva SARS-CoV-2 and conjunctiva. J Med Virol. 2020. Disclosures: No conflict of interest exist. Author, Article, and Disclosure InformationAuthors: Francesca Colavita, PhD; Daniele Lapa, PhD; Fabrizio Carletti, PhD; Eleonora Lalle, PhD; Licia Bordi, PhD; Patrizia Marsella, PhD; Emanuele Nicastri, MD; Nazario Bevilacqua, MD; Maria Letizia Giancola, MD; Angela Corpolongo, MD; Giuseppe Ippolito, MD; Maria Rosaria Capobianchi, PhD; Concetta Castilletti, PhDAffiliations: National Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS, Rome, Italy (F.C., D.L., F.C., E.L., L.B., P.M., E.N., N.B., M.L.G., A.C., G.I., M.R.C., C.C.)Note: Drs. Colavita and Lapa contributed equally.Acknowledgment: The authors thank the Collaborators Members of the INMI COVID-19 Study Group (Appendix).Financial Support: By funds to the National Institute for Infectious Diseases “Lazzaro Spallanzani” IRCCS from Ministero della Salute, Ricerca Corrente, linea1, and European Commission Horizon 2020 (EU project 101003544, CoNVat; EU project 101003551, EXSCALATE4CoV).Disclosures: Authors have disclosed no conflicts of interest. Forms can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M20-1176.Reproducible Research Statement: Study protocol and data set: Available from Dr. Castilletti (e-mail, concetta.castilletti@inmi.it) through written agreement with the authors.Corresponding Author: Concetta Castilletti, PhD, Laboratory of Virology, National Institute for Infectious Diseases “Lazzaro Spallanzani”, Via Portuense 292, 00149 Rome, Italy; e-mail, concetta.castilletti@inmi.it.This article was published at Annals.org on 17 April 2020. 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From the Entry to the EffectsOphthalmic manifestations of coronavirus disease 2019 and ocular side effects of investigational pharmacologic agentsOcular Findings in COVID-19 Patients: A Review of Direct Manifestations and Indirect Effects on the EyeCOVID-19 Infection Among Healthcare Workers: Serological Findings Supporting Routine TestingOcular Features and Associated Systemic Findings in SARS-CoV-2 InfectionThe COVID-19 pandemicA Review of COVID-19 Clinical PresentationEffect of COVID-19 on the OrgansSpatial and temporal dynamics of SARS-CoV-2 in COVID-19 patients: A systematic review and meta-analysisReview of maternal COVID-19 infection: considerations for the pediatric ophthalmologistA Panel of Broad-Spectrum Antivirals in Topical Ophthalmic Medications from the Drug Repurposing Approach during and after the Coronavirus Disease 2019 EraSARS-CoV-2 pandemic: An overviewCorneal transplantation in the aftermath of the COVID-19 pandemic: an international perspectiveCOVID-19 and the Ocular Surface: A Review of Transmission and ManifestationsPathogenesis of SARS-CoV-2 in Transgenic Mice Expressing Human Angiotensin-Converting Enzyme 2The Ocular Manifestations and Transmission of COVID-19: Recommendations for PreventionCOVID-19: Specific and Non-Specific Clinical Manifestations and Symptoms: The Current State of KnowledgeThe Ocular Surface and the Coronavirus Disease 2019: Does a Dual ‘Ocular Route’ Exist?Comparing The Viral Load of Severe Acute Respiratory Syndrome Coronavirus 2 in Different Human SpecimensOphthalmic complaints in face-mask wearing: prevalence, treatment, and prevention with a potential protective effect against SARS-CoV-2Detection of SARS-CoV-2 RNA in conjunctival swab of a COVID-19 patient: The first report from BangladeshIs the use of a powered dermatome an aerosol-generating procedure (AGP)? Implications for personal protection against COVID-19 virus Awareness, Perceptions, and Attitude Regarding Coronavirus Disease 2019 (COVID-19) Among Ophthalmologists in Jordan: Cross-Sectional Online Survey Preserving Vision in the COVID-19 Pandemic: Focus on Health Equity Assessment of Coronavirus in the Conjunctival Tears and Secretions in Patients with SARS-CoV-2 Infection in Sohag Province, Egypt Emerging challenges and possible strategies in maxillo-facial and oral surgery during the COVID-19 pandemicCharacteristics of Ocular Manifestations of Patients with Coronavirus Disease 2019 in Daegu Province, KoreaConsideraciones para la donación y trasplante de tejido ocular en México durante la pandemia de COVID-19 4 August 2020Volume 173, Issue 3 Page: 242-243 Keywords Conjunctivitis COVID-19 Fevers Infectious diseases Reverse transcriptase polymerase chain reaction RNA SARS coronavirus Viral replication Virology Vomiting ePublished: 17 April 2020 Issue Published: 4 August 2020 Copyright & PermissionsCopyright © 2020 by American College of Physicians. 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