Correction APPLIED BIOLOGICAL SCIENCES Correction for “Ranking the risk of animal-to-human spillover for newly discovered viruses,” by Zoë L. Grange, Tracey Goldstein, Christine K. Johnson, Simon Anthony, Kirsten Gilardi, Peter Daszak, Kevin J. Olival, Tammie O’Rourke, Suzan Murray, Sarah H. Olson, Eri Togami, Gema Vidal, Expert Panel, PREDICT Consortium, and Jonna A. K. Mazet, which published April 5, 2021; 10.1073/pnas.2002324118 (Proc. Natl. Acad. Sci. U.S.A. 118, e2002324118). The authors note that on page 6, left column, third full paragraph, line 3, “Betacoronavirus” should instead appear as “Alphacoronavirus.” The online version has been corrected. The authors also note that the list of members of the PREDICT Consortium group was inadvertently truncated. The SI Appendix has been corrected online to include the correct full list of names for this author group. Published under the PNAS license. Published September 20, 2021. CORRECTION www.pnas.org/cgi/doi/10.1073/pnas.2115409118 PNAS 2021 Vol. 118 No. 39 e2115409118 https://doi.org/10.1073/pnas.2115409118 | 1of1 Downloaded by guest on September 30, 2021 Ranking the risk of animal-to-human spillover for newly discovered viruses Zoë L. Grangea,1, Tracey Goldsteina,2, Christine K. Johnsona,2, Simon Anthonya,b,c,d, Kirsten Gilardia, Peter Daszakb, Kevin J. Olivalb, Tammie O’Rourkee, Suzan Murrayf, Sarah H. Olsong, Eri Togamia, Gema Vidala, Expert Panel3, PREDICT Consortium3, and Jonna A. K. Mazeta,1 aOne Health Institute and Karen C. Drayer Wildlife Health Center, School of Veterinary Medicine, University of California, Davis, CA 95616; bEcoHealth Alliance, New York, NY 1001; cCenter for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, NY 10032; dDepartment of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY 10032; eMetabiota, Inc., Nanaimo, BC V9S 1G5, Canada; fGlobal Health, Smithsonian Conservation Biology Institute, Washington, DC 20008; and gWildlife Conservation Society, New York, NY 10460 Edited by Jonathan Dushoff, McMaster University, Hamilton, ON, Canada, and accepted by Editorial Board Member Simon A. Levin February 8, 2021 (received for review February 12, 2020) The death toll and economic loss resulting from the severe acute disease in people (4). While these viruses are of ongoing concern respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic are to human health, as repeated Ebola epidemics demonstrate, the stark reminders that we are vulnerable to zoonotic viral threats. yet to be identified viruses pose an equal if not more serious threat Strategies are needed to identify and characterize animal viruses to humanity. Approximately 1.67 million undescribed viruses are that pose the greatest risk of spillover and spread in humans and thought to exist in mammals and birds, up to half of which are inform public health interventions. Using expert opinion and sci- estimated to have the potential to spill over into humans (5). entific evidence, we identified host, viral, and environmental risk Virus discovery efforts have initiated the process of investi- factors contributing to zoonotic virus spillover and spread in hu- gating potential viral threats. Our team sampled wildlife at high- mans. We then developed a risk ranking framework and interac- risk human disease transmission interfaces in over 30 countries tive web tool, SpillOver, that estimates a risk score for wildlife- (6), resulting in the discovery of hundreds of previously undetected origin viruses, creating a comparative risk assessment of viruses viruses (SI Appendix). Although interesting, virus discovery creates a with uncharacterized zoonotic spillover potential alongside those plethora of data without direction on where to focus efforts to pre- already known to be zoonotic. Using data from testing 509,721 vent viral spillovers that could lead to future epidemics and pan- APPLIED BIOLOGICAL SCIENCES samples from 74,635 animals as part of a virus discovery project demics. A strategy is needed to evaluate viruses and identify those and public records of virus detections around the world, we that are most important for further investigation and surveillance. ranked the spillover potential of 887 wildlife viruses. Validating The risk each virus poses to human health is not equal. Two the risk assessment, the top 12 were known zoonotic viruses, in- viruses may be nearly identical, one zoonotic and the other not. cluding SARS-CoV-2. Several newly detected wildlife viruses ranked higher than known zoonotic viruses. Using a scientifically informed process, we capitalized on the recent wealth of virus discovery data Significance to systematically identify and prioritize targets for investigation. The publicly accessible SpillOver platform can be used by policy The recent emergence and spread of zoonotic viruses, includ- makers and health scientists to inform research and public health ing Ebola virus and severe acute respiratory syndrome coro- interventions for prevention and rapid control of disease outbreaks. navirus 2, demonstrate that animal-sourced viruses are a very SpillOver is a living, interactive database that can be refined over real threat to global public health. Virus discovery efforts have time to continue to improve the quality and public availability of detected hundreds of new animal viruses with unknown zoo- information on viral threats to human health. notic risk. We developed an open-source risk assessment to systematically evaluate novel wildlife-origin viruses in terms of emerging infectious disease | wildlife | zoonotic virus | their zoonotic spillover and spread potential. Our tool will disease ecology | public health help scientists and governments assess and communicate risk, informing national disease prioritization, prevention, and control actions. The resulting watchlist of potential pathogens e now live in an era in which threats posed by viral pan- will identify targets for new virus countermeasure initiatives, demics are a daily reality. A single lethal virus can emerge W which can reduce the economic and health impacts of emerging suddenly and spread rapidly to every household and every diseases. community without regard to national borders or to social and economic standing. Recognizing the importance of emerging in- Author contributions: Z.L.G., T.G., C.K.J., S.A., K.G., P.D., K.J.O., T.O., S.M., S.H.O., P.C., and fectious diseases (EIDs), the World Health Organization (WHO) J.A.K.M. designed research; Z.L.G., E.T., G.V., E.P., P.C., and J.A.K.M. performed research; highlighted Disease X, a currently unknown pathogen capable of Z.L.G. and J.A.K.M. analyzed data; and Z.L.G., T.G., C.K.J., S.A., K.G., P.D., K.J.O., T.O., S.M., causing a serious human epidemic, as a target for research and S.H.O., E.T., G.V., and J.A.K.M. wrote the paper. development in their 2018 Blueprint of Priority Diseases (1). The authors declare no competing interest. However, despite increased investment in pandemic prevention This article is a PNAS Direct Submission. J.D. is a guest editor invited by the Editorial Board. and knowledge gained from previous EID outbreaks, such as This open access article is distributed under Creative Commons Attribution-NonCommercial- severe acute respiratory syndrome coronavirus (SARS-CoV), NoDerivatives License 4.0 (CC BY-NC-ND). Ebola virus (Zaire ebolavirus), and Zika virus, we were unpre- See online for related content such as Commentaries. pared for the severe acute respiratory syndrome coronavirus 2 1To whom correspondence may be addressed. Email: [email protected] or zlgrange@ (SARS-CoV-2) (2) that emerged and rapidly spread around the ucdavis.edu. world in 2019 to 2020 with a devastating death toll and an esti- 2T.G. and C.K.J. contributed equally to this work. mated global economic loss of ∼28 trillion (3). 3The complete lists of Expert Panel and PREDICT Consortium can be found in SI Appendix. SARS-CoV-2 is one of many potential viral threats to humans. This article contains supporting information online at https://www.pnas.org/lookup/suppl/ There are just over 250 known zoonotic viruses—viruses that doi:10.1073/pnas.2002324118/-/DCSupplemental. have previously spilled over from animals to humans and caused Published April 5, 2021. PNAS 2021 Vol. 118 No. 15 e2002324118 https://doi.org/10.1073/pnas.2002324118 | 1of8 However, several factors about the virus, host (the organism in lenders, account for variances among risk factors in order to de- which a virus can live and multiply), environment (the location and termine a comparative risk score. Previous studies and tools using ecology where the host lives), and related human behavior influence this approach for viruses have been insightful but limited in scope by the likelihood that a virus will become zoonotic and spread within focusing on narrow groups of viruses or few risk factors (7–9). Here, human populations (7, 8). Risk assessments, such as those used by we present an innovative relative risk assessment and interactive Fig. 1. Expert opinion (n = 65) of the level of risk each factor included in the risk ranking assessment (n = 42) plays in the risk of a new virus spillover from animals to humans. 2of8 | PNAS Grange et al. https://doi.org/10.1073/pnas.2002324118 Ranking the risk of animal-to-human spillover for newly discovered viruses web application to systematically evaluate viruses of wildlife origin then created a risk ranking framework and web tool called in terms of their potential for zoonotic spillover and spread in SpillOver: Viral Risk Ranking (https://spillover.global) that uses people (henceforth, “spillover risk”). data for these risk factors to calculate a comparative “risk score” Using literature reviews and input from experts, we identified for each virus, much like a credit report. We used SpillOver to risk factors that are most likely to contribute to spillover risk. We rank viruses detected during our viral discovery efforts and APPLIED BIOLOGICAL SCIENCES Fig.