Cited by 6,661SARS-CoV-2 and COVID-19 ResearchCOVID-19 Clinical Research StudiesSARS-CoV-2 detection and testing

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Virological assessment of hospitalized patients with COVID-2019

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Wölfel, Roman, Corman, Victor M., Guggemos, Wolfgang, Seilmaier, Michael, Zange, Sabine, Müller, Marcel A., Niemeyer, Daniela, Jones, Terry C., Vollmar, Patrick, Rothe, Camilla, Hoelscher, Michael, Bleicker, Tobias, Brünink, Sebastian, Schneider, Julia, Ehmann, Rosina, Zwirglmaier, Katrin, Drosten, Christian, Wendtner, Clemens·2020·Nature

DOI 10.1038/s41586-020-2196-x

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Abstract

Coronavirus disease 2019 (COVID-19) is an acute infection of the respiratory tract that emerged in late 2019 1,2. Initial outbreaks in China involved 13.8% of cases with severe courses, and 6.1% of cases with critical courses 3. This severe presentation may result from the virus using a virus receptor that is expressed predominantly in the lung 2,4; the same receptor tropism is thought to have determined the pathogenicity-but also aided in the control-of severe acute respiratory syndrome (SARS) in 2003 5. However, there are reports of cases of COVID-19 in which the patient shows mild upper respiratory tract symptoms, which suggests the potential for pre- or oligosymptomatic transmission 6-8. There is an urgent need for information on virus replication, immunity and infectivity in specific sites of the body. Here we report a detailed virological analysis of nine cases of COVID-19 that provides proof of active virus replication in tissues of the upper respiratory tract. Pharyngeal virus shedding was very high during the first week of symptoms, with a peak at 7.11 × 10 8 RNA copies per throat swab on day 4. Infectious virus was readily isolated from samples derived from the throat or lung, but not from stool samples-in spite of high concentrations of virus RNA. Blood and urine samples never yielded virus. Active replication in the throat was confirmed by the presence of viral replicative RNA intermediates in the throat samples. We consistently detected sequence-distinct virus populations in throat and lung samples from one patient, proving independent replication. The shedding of viral RNA from sputum outlasted the end of symptoms. Seroconversion occurred after 7 days in 50% of patients (and by day 14 in all patients), but was not followed by a rapid decline in viral load. COVID-19 can present as a mild illness of the upper respiratory tract. The confirmation of active virus replication in the upper respiratory tract has implications for the containment of COVID-19.

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Review on the contamination of wastewater by COVID-19 virus: Impact and treatment
Lahrich, S., Laghrib, F., Farahi, A., Bakasse, M., Saqrane, S., & Mhammedi, M. A. E. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.142325 · Cited by 116
High levels of SARS-CoV-2–specific T cells with restricted functionality in severe courses of COVID-19
Schub, D., Klemis, V., Schneitler, S., Mihm, J., Lepper, P. M., Wilkens, H., Bals, R., Eichler, H., Gärtner, B. C., Becker, S. L., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.142167 · Cited by 115
Detection of SARS-CoV-2 RNA in hospital wastewater from a low COVID-19 disease prevalence area
Gonçalves, J., Koritnik, T., Mioč, V., Trkov, M., Bolješić, M., Berginc, N., Prosenc, K., Kotar, T., & Paragi, M. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.143226 · Cited by 116
Digital CRISPR-based method for the rapid detection and absolute quantification of nucleic acids
Wu, X., Tay, J. K., Goh, C. K., Chan, C. S. C., Lee, Y. H., Springs, S. L., Wang, D. Y., Loh, K. S., Lu, T. K., & Yu, H. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120876 · Cited by 116
SARS-CoV-2 infections in children: Understanding diverse outcomes
Brodin, P. (2022) · Immunity · doi:10.1016/j.immuni.2022.01.014 · Cited by 118
Serologic responses to SARS-CoV-2 infection among hospital staff with mild disease in eastern France
Fafi-Kremer, S., Bruel, T., Madec, Y., Grant, R., Tondeur, L., Grzelak, L., Staropoli, I., Anna, F., Souque, P., Fernandes-Pellerin, S., et al. (2020) · eBioMedicine · doi:10.1016/j.ebiom.2020.102915 · Cited by 108
SARS‐CoV‐2: A comprehensive review from pathogenicity of the virus to clinical consequences
Lotfi, M., & Rezaei, N. (2020) · Journal of Medical Virology · doi:10.1002/jmv.26123 · Cited by 118
Predicting the number of reported and unreported cases for the COVID-19 epidemics in China, South Korea, Italy, France, Germany and United Kingdom
Liu, Z.-H., Magal, P., & Webb, G. I. (2020) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2020.110501 · Cited by 123
Single‐cell analyses reveal SARS‐CoV‐2 interference with intrinsic immune response in the human gut
Triana, S., Metz‐Zumaran, C., Ramírez, C. D., Kee, C., Doldan, P., Shahraz, M., Schraivogel, D., Gschwind, A. R., Sharma, A. K., Steinmetz, L. M., et al. (2021) · Molecular Systems Biology · doi:10.15252/msb.202110232 · Cited by 111
Insights into pathogenesis of fatal COVID‐19 pneumonia from histopathology with immunohistochemical and viral RNA studies
Sauter, J. L., Baine, M. K., Butnor, K. J., Buonocore, D. J., Chang, J. C., Jungbluth, A. A., Szabolcs, M. J., Morjaria, S., Mount, S. L., Rekhtman, N., et al. (2020) · Histopathology · doi:10.1111/his.14201 · Cited by 104
Hunting coronavirus by transmission electron microscopy – a guide to SARS‐CoV‐2‐associated ultrastructural pathology in COVID‐19 tissues
Hopfer, H., Herzig, M. C., Gosert, R., Menter, T., Hench, J., Tzankov, A., Hirsch, H. H., & Miller, S. (2020) · Histopathology · doi:10.1111/his.14264 · Cited by 113
Neutralisation of SARS-CoV-2 lineage P.1 by antibodies elicited through natural SARS-CoV-2 infection or vaccination with an inactivated SARS-CoV-2 vaccine: an immunological study
de Souza, W. M., Amorim, M. R., Sesti‐Costa, R., Coimbra, L. D., Brunetti, N. S., de Toledo-Teixeira, D. A., de Souza, G. F., Muraro, S. P., Parise, P. L., Barbosa, P. P., et al. (2021) · The Lancet Microbe · doi:10.1016/s2666-5247(21)00129-4 · Cited by 115
Suramin Inhibits SARS-CoV-2 Infection in Cell Culture by Interfering with Early Steps of the Replication Cycle
Salgado‐Benvindo, C., Thaler, M., Taş, A., Ogando, N. S., Bredenbeek, P. J., Ninaber, D. K., Wang, Y., Hiemstra, P. S., Snijder, E. J., & van Hemert, M. J. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00900-20 · Cited by 114
Prolonged viral shedding of SARS-CoV-2 in an immunocompromised patient
Nakajima, Y., Ogai, A., Furukawa, K., Arai, R., Anan, R., Nakano, Y., Kurihara, Y., Shimizu, H., Misaki, T., & Okabe, N. (2020) · Journal of Infection and Chemotherapy · doi:10.1016/j.jiac.2020.12.001 · Cited by 113
“388 was not isolated from such stool samples [3].”
Wastewater-Based Epidemiology (WBE) and Viral Detection in Polluted Surface Water: A Valuable Tool for COVID-19 Surveillance—A Brief Review
Oliveira, M. D. L. A., Campos, A. A. S., Matos, A. D. R., Rigotto, C., Sotero-Martins, A., Teixeira, P. F. P., & Siqueira, M. M. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17249251 · Cited by 113
“On the other hand, other groups were not successful in viral isolation, despite the high viral RNA concentration in those clinical samples [21].”
Background
Can the detection dog alert on COVID-19 positive persons by sniffing axillary sweat samples? A proof-of-concept study
Grandjean, D., Sarkis, R., Tourtier, J.-P., Julien, C., Benard, A., Roger, V., Bernes-Luciani, E., Bernes-Luciani, E., Maestracci, B., Morvan, P., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0243122 · Cited by 120
Duration of SARS-CoV-2 viral shedding in faeces as a parameter for wastewater-based epidemiology: Re-analysis of patient data using a shedding dynamics model
Miura, F., Kitajima, M., & Omori, R. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.144549 · Cited by 113
Evolution of spray and aerosol from respiratory releases: theoretical estimates for insight on viral transmission
de Oliveira, P. M., Mesquita, L. C. C., Gkantonas, S., Giusti, A., & Mastorakos, E. (2021) · Proceedings of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rspa.2020.0584 · Cited by 114
Droplet digital RT-PCR to detect SARS-CoV-2 signature mutations of variants of concern in wastewater
Heijnen, L., Elsinga, G., de Graaf, M., Molenkamp, R., Koopmans, M., & Medema, G. J. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.149456 · Cited by 109
“…of 30–60% of infected the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). individuals (Jones et al., 2020; Wang et al., 2020; Wölfel et al., 2020; Xiao et al., 2020), sparked the idea that wastewater could be used to monitor the circulation of SARS-CoV-2 at community level.”
Influential
Estimate False-Negative RT-PCR Rates for SARS-CoV-2: A Systematic Review and Meta-Analysis
Pecoraro, V., Negro, A., Pirotti, T., & Trenti, T. (2021) · European Journal of Clinical Investigation · doi:10.1111/eci.13706 · Cited by 117
The timing of COVID-19 transmission
Ferretti, L., Ledda, A., Wymant, C., Zhao, L., Ledda, V., Abeler-Dörner, L., Kendall, M., Nurtay, A., Cheng, H.-Y., Ng, T.-C., et al. (2020) · doi:10.1101/2020.09.04.20188516 · Cited by 112
SARS-CoV-2 pandemic: An overview
Martellucci, C. A., Flacco, M. E., Cappadona, R., Bravi, F., Mantovani, L. G., & Manzoli, L. (2020) · Advances in Biological Regulation · doi:10.1016/j.jbior.2020.100736 · Cited by 116
Designing a novel mRNA vaccine against SARS-CoV-2: An immunoinformatics approach
Ahammad, I., & Lira, S. S. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.06.213 · Cited by 112
The unique features of SARS‐CoV‐2 transmission: Comparison with SARS‐CoV, MERS‐CoV and 2009 H1N1 pandemic influenza virus
Wu, Z., Harrich, D., Li, Z., Hu, D., & Li, D. (2020) · Reviews in Medical Virology · doi:10.1002/rmv.2171 · Cited by 114
Clinical Evaluation of Roche SD Biosensor Rapid Antigen Test for SARS-CoV-2 in Municipal Health Service Testing Site, the Netherlands
Iglὁi, Z., Velzing, J., van Beek, J., van de Vijver, D. A. M. C., Aron, G. I., Ensing, R., Benschop, K., Han, W. G. H., Boelsums, T. L., Koopmans, M., et al. (2021) · Emerging infectious diseases · doi:10.3201/eid2705.204688 · Cited by 112
“As expected, the sensitivity of the tests is lower than that of RT-PCR, but in patients in the early phase of illness who have high viral load, performance meets World Health Organization–set criteria of >80% sensitivity and >97% specifi city compared with nucleic acid detection methods (8).”
Endothelial cell infection and dysfunction, immune activation in severe COVID-19
Qin, Z., Liu, F., Blair, R. V., Wang, C., Yang, H., Mudd, J. C., Currey, J. M., Iwanaga, N., He, J., Mi, R., et al. (2021) · Theranostics · doi:10.7150/thno.61810 · Cited by 116
“To examine SARS-CoV-2 infection in tissues of K18 mice, we used qRT-PCR to quantify the nucleocapsid (N) sub-genomic viral RNA, a correlate of active virus replication [33, 34], in organs daily until 6 DPI (Figure S4).”
Method
Contribution of SARS-CoV-2 RNA shedding routes to RNA loads in wastewater
Crank, K. C., Chen, W., Bivins, A. W., Lowry, S. A., & Bibby, K. J. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.150376 · Cited by 112
“For SARS-CoV-2 RNA concentrations in bodily excreta, we fit distributions to data reported in recent papers (Han et al., 2020; Jeong et al., 2020; Kashi et al., 2020; Lescure et al., 2020; Pan et al., 2020; Roshandel et al., 2020; Wölfel et al., 2020; Wyllie et al., 2020; Yoon et al., 2020; Zheng et al., 2020).”
Chest Computed Tomography and Clinical Follow-Up of Discharged Patients with COVID-19 in Wenzhou City, Zhejiang, China
Liu, C., Ye, L., Xia, R., Zheng, X., Yuan, C., Wang, Z., Lin, R., Shi, D., Gao, Y., Yao, J., et al. (2020) · Annals of the American Thoracic Society · doi:10.1513/annalsats.202004-324oc · Cited by 111
First detection of SARS-CoV-2 genetic material in the vicinity of COVID-19 isolation Centre in Bangladesh: Variation along the sewer network
Ahmed, F., Islam, M. T., Kumar, M., Hossain, M., Bhattacharya, P., Islam, M. T., Hossen, F., Islam, M. T., Islam, M. T., Islam, M. T., et al. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.145724 · Cited by 111
The environmental dangers of employing single-use face masks as part of a COVID-19 exit strategyPreprint
Allison, A. L., Ambrose-Dempster, E., Doménech, T., Bawn, M., Arredondo, M. C., Chau, C., Chandler, K. L., Dobrijevic, D., Hailes, H. C., Lettieri, P., et al. (2020) · doi:10.14324/111.444/000031.v1 · Cited by 111
Fighting COVID-19: A quick review of diagnoses, therapies, and vaccines
Shih, H., Wu, C.-J., Tu, Y., & Chi, C. (2020) · Biomedical Journal · doi:10.1016/j.bj.2020.05.021 · Cited by 109
Assessing a novel, lab-free, point-of-care test for SARS-CoV-2 (CovidNudge): a diagnostic accuracy study
Gibani, M. M., Toumazou, C., Sohbati, M., Sahoo, R., Karvela, M., Hon, T.-K., de Mateo, S., Burdett, A. J., Leung, K. Y. F., Barnett, J., et al. (2020) · The Lancet Microbe · doi:10.1016/s2666-5247(20)30121-x · Cited by 110
Comparison of Subgenomic and Total RNA in SARS-CoV-2-Challenged Rhesus Macaques
Dagotto, G., Mercado, N. B., Martinez, D. R., Hou, Y. J., Nkolola, J. P., Carnahan, R. H., Crowe, J. E., Baric, R. S., & Barouch, D. H. (2021) · Journal of Virology · doi:10.1128/jvi.02370-20 · Cited by 103
“The subgenomic E (sgE) gene was used to measure sgRNA levels in this work (17).”
BackgroundMethodInfluential
Dynamics of COVID-19 under social distancing measures are driven by transmission network structure
Nande, A., Adlam, B., Sheen, J. K., Levy, M. Z., & Hill, A. L. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1008684 · Cited by 118
Resuming professional football (soccer) during the COVID-19 pandemic in a country with high infection rates: a prospective cohort study
Schumacher, Y. O., Tabben, M., Hassoun, K., Marwani, A. A., Hussein, I. A., Coyle, P. V., Abbassi, A. K., Ballan, H. T., Al-Kuwari, A. J., Chamari, K., et al. (2021) · British Journal of Sports Medicine · doi:10.1136/bjsports-2020-103724 · Cited by 106
Controlling Epidemic Spread: Reducing Economic Losses with Targeted Closures
Birge, J. R., Candogan, O., & Feng, Y. (2020) · Management Science · doi:10.1287/mnsc.2022.4318 · Cited by 109
Disparate temperature-dependent virus–host dynamics for SARS-CoV-2 and SARS-CoV in the human respiratory epithelium
V’kovski, P., Gultom, M. L., Kelly, J. N., Steiner, S., Russeil, J., Mangeat, B., Cora, E., Pezoldt, J., Holwerda, M., Kratzel, A., et al. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001158 · Cited by 132
A population-based analysis of the longevity of SARS-CoV-2 antibody seropositivity in the United States
Alfego, D., Sullivan, A., Poirier, B., Williams, J., Grover, A., Gillim, L., Adcock, D. M., & Letovsky, S. I. (2021) · EClinicalMedicine · doi:10.1016/j.eclinm.2021.100902 · Cited by 104
Developing RT-LAMP assays for rapid diagnosis of SARS-CoV-2 in saliva
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“38 (cid:1) 40 Our RT-LAMP assays were fast as most reactions were completed within 30-50 min.”
Using influenza surveillance networks to estimate state-specific prevalence of SARS-CoV-2 in the United States
Silverman, J. D., Hupert, N., & Washburne, A. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.abc1126 · Cited by 115
Post-mortem viral dynamics and tropism in COVID-19 patients in correlation with organ damage
Skok, K., Stelzl, E., Trauner, M., Kessler, H. H., & Lax, S. (2020) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-020-02903-8 · Cited by 111
Population-scale longitudinal mapping of COVID-19 symptoms, behaviour and testing
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A prospective clinical pilot study on the effects of a hydrogen peroxide mouthrinse on the intraoral viral load of SARS-CoV-2
Gottsauner, J. M., Michaelides, I., Schmidt, B., Scholz, K. J., Buchalla, W., Widbiller, M., Hitzenbichler, F., Ettl, T., Reichert, T. E., Bohr, C., et al. (2020) · Clinical Oral Investigations · doi:10.1007/s00784-020-03549-1 · Cited by 108

Authors: Wölfel, R., Corman, V. M., Guggemos, W., Seilmaier, M., Zange, S., Müller, M. A., Niemeyer, D., Jones, T. C., Vollmar, P., Rothe, C., Hoelscher, M., Bleicker, T., Brünink, S., Schneider, J., Ehmann, R., Zwirglmaier, K., Drosten, C., & Wendtner, C.
Affiliations: Institut für Mikrobiologie der Bundeswehr (DE)
Charité – Universitätsmedizin Berlin (DE)
München Klinik Schwabing (DE)
University of Cambridge (GB)
LMU Klinikum (DE)
Corresponding author: Drosten, Christian
Wendtner, Clemens
ORCID: Wölfel, Roman
Corman, Victor M.
Seilmaier, Michael
Zange, Sabine
Müller, Marcel A.
Niemeyer, Daniela
Jones, Terry C.
Bleicker, Tobias
Schneider, Julia
Ehmann, Rosina
Zwirglmaier, Katrin
Drosten, Christian
Wendtner, Clemens
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2020-04-01
Volume: 581
Issue: 7809
Pages: 465-469
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-020-2196-x
OpenAlex: W3013893137
Cited by: 6,661
References: 37
Citations by year: 2026: 92 · 2025: 165 · 2024: 328 · 2023: 526 · 2022: 1091 · 2021: 2228 · 2020: 2219
FWCI: 199.03
Type: journal article
Language: en
Update notices: correction (2020-12-11)
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
medRxiv (acceptedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: European Commission (602525)
Topics: Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 detection and testing
Keywords: COVID-19 pandemic, SARS-CoV-2, upper respiratory tract, viral replication, seroconversion, viral load, hospitalized patients
MeSH terms: Seroconversion, Betacoronavirus, COVID-19, SARS-CoV-2, COVID-19 Testing, Coronavirus Envelope Proteins, Antibodies, Viral, Base Sequence, Blood, Feces, Hospitalization, Humans, Immunoglobulin G, Immunoglobulin M, Lung, Pharynx, Pneumonia, Viral, RNA, Viral, Sputum, Urine, Viral Envelope Proteins, Virus Replication, Virus Shedding, Coronavirus Infections, Clinical Laboratory Techniques, Viral Load, Polymorphism, Single Nucleotide, Pandemics

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