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      Pandemic origins and a One Health approach to preparedness and prevention: Solutions based on SARS-CoV-2 and other RNA viruses

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          Abstract

          COVID-19 is the latest zoonotic RNA virus epidemic of concern. Learning how it began and spread will help to determine how to reduce the risk of future events. We review major RNA virus outbreaks since 1967 to identify common features and opportunities to prevent emergence, including ancestral viral origins in birds, bats, and other mammals; animal reservoirs and intermediate hosts; and pathways for zoonotic spillover and community spread, leading to local, regional, or international outbreaks. The increasing scientific evidence concerning the origins of Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) is most consistent with a zoonotic origin and a spillover pathway from wildlife to people via wildlife farming and the wildlife trade. We apply what we know about these outbreaks to identify relevant, feasible, and implementable interventions. We identify three primary targets for pandemic prevention and preparedness: first, smart surveillance coupled with epidemiological risk assessment across wildlife–livestock–human (One Health) spillover interfaces; second, research to enhance pandemic preparedness and expedite development of vaccines and therapeutics; and third, strategies to reduce underlying drivers of spillover risk and spread and reduce the influence of misinformation. For all three, continued efforts to improve and integrate biosafety and biosecurity with the implementation of a One Health approach are essential. We discuss new models to address the challenges of creating an inclusive and effective governance structure, with the necessary stable funding for cross-disciplinary collaborative research. Finally, we offer recommendations for feasible actions to close the knowledge gaps across the One Health continuum and improve preparedness and response in the future.

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          Most cited references68

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          Global trends in emerging infectious diseases

          The next new disease Emerging infectious diseases are a major threat to health: AIDS, SARS, drug-resistant bacteria and Ebola virus are among the more recent examples. By identifying emerging disease 'hotspots', the thinking goes, it should be possible to spot health risks at an early stage and prepare containment strategies. An analysis of over 300 examples of disease emerging between 1940 and 2004 suggests that these hotspots can be accurately mapped based on socio-economic, environmental and ecological factors. The data show that the surveillance effort, and much current research spending, is concentrated in developed economies, yet the risk maps point to developing countries as the more likely source of new diseases. Supplementary information The online version of this article (doi:10.1038/nature06536) contains supplementary material, which is available to authorized users.
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            Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans

            Two-way transmission on mink farms Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a zoonotic virus—one that spilled over from another species to infect and transmit among humans. We know that humans can infect other animals with SARS-CoV-2, such as domestic cats and even tigers in zoos. Oude Munnink et al. used whole-genome sequencing to show that SARS-CoV-2 infections were rife among mink farms in the southeastern Netherlands, all of which are destined to be closed by March 2021 (see the Perspective by Zhou and Shi). Toward the end of June 2020, 68% of mink farm workers tested positive for the virus or had antibodies to SARS-CoV-2. These large clusters of infection were initiated by human COVID-19 cases with viruses that bear the D614G mutation. Sequencing has subsequently shown that mink-to-human transmission also occurred. More work must be done to understand whether there is a risk that mustelids may become a reservoir for SARS-CoV-2. Science, this issue p. 172; see also p. 120
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              Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor

              The 2002–3 pandemic caused by severe acute respiratory syndrome coronavirus (SARS-CoV) was one of the most significant public health events in recent history 1 . An ongoing outbreak of Middle East respiratory syndrome coronavirus (MERS-CoV) 2 suggests that this group of viruses remains a major threat and that their distribution is wider than previously recognized. Although bats have been suggested as the natural reservoirs of both viruses 3–5 , attempts to isolate the progenitor virus of SARS-CoV from bats have been unsuccessful. Diverse SARS-like coronaviruses (SL-CoVs) have now been reported from bats in China, Europe and Africa 5–8 , but none are considered a direct progenitor of SARS-CoV because of their phylogenetic disparity from this virus and the inability of their spike proteins (S) to use the SARS-CoV cellular receptor molecule, the human angiotensin converting enzyme II (ACE2) 9,10 . Here, we report whole genome sequences of two novel bat CoVs from Chinese horseshoe bats (Family: Rhinolophidae) in Yunnan, China; RsSHC014 and Rs3367. These viruses are far more closely related to SARS-CoV than any previously identified bat CoVs, particularly in the receptor binding domain (RDB) of the S protein. Most importantly, we report the first recorded isolation of a live SL-CoV (bat SL-CoV-WIV1) from bat fecal samples in Vero E6 cells, which has typical coronavirus morphology, 99.9% sequence identity to Rs3367 and uses the ACE2s from human, civet and Chinese horseshoe bat for cell entry. Preliminary in vitro testing indicates that WIV1 also has a broad species tropism. Our results provide the strongest evidence to date that Chinese horseshoe bats are natural reservoirs of SARS-CoV, and that intermediate hosts may not be necessary for direct human infection by some bat SL-CoVs. They also highlight the importance of pathogen discovery programs targeting high-risk wildlife groups in emerging disease hotspots as a strategy for pandemic preparedness.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                10 October 2022
                18 October 2022
                10 October 2022
                : 119
                : 42
                : e2202871119
                Affiliations
                [1] aDepartment of Medicine, Section of Infectious Diseases, National Emerging Infectious Diseases Laboratories, Center for Emerging Infectious Diseases Policy and Research, Boston University , Boston, MA 02215;
                [2] bSchool of Public Health, Department of Global Health, Kwame Nkrumah University of Science and Technology (KNUST) , PMB UPO, Kumasi 00000 Ghana;
                [3] cGlobal Health and Infectious Diseases Research Group, Kumasi Centre for Collaborative Research in Tropical Medicine , Kumasi, Ghana;
                [4] dBernhard Nocht Institute of Tropical Medicine, 20359 Hamburg, Germany;
                [5] eVictorian Infectious Diseases Reference Laboratory, The Peter Doherty Institute for Infection and Immunity, University of Melbourne , Melbourne, VIC, 3000 Australia;
                [6] fEcoHealth Alliance , New York, NY 10018;
                [7] gGeneva Centre for Emerging Viral Diseases, Laboratory of Virology, Division of Infectious Diseases, University Hospital of Geneva , CH-1205 Geneva, Switzerland;
                [8] hDepartment of Molecular Medicine and Microbiology Faculty of Medicine, University of Geneva , 1205 Geneva, Switzerland;
                [9] iSchool of Veterinary Science, The University of Queensland , Brisbane, Queensland 4072, Australia;
                [10] jDepartment of Viroscience and Pandemic and Disaster Preparedness Centre, Erasmus Medical Center , CA 3000 Rotterdam, Netherlands;
                [11] kUniversity of Malaya , 50603 Kuala Lumpur, Malaysia;
                [12] lNorwegian Veterinary Institute , 1433 Ås, Norway;
                [13] mFaculty of Health Sciences, UiT – The Arctic University of Norway , Langnes, N-9037 Tromsø, Norway;
                [14] nSchool of Public Health, The University of Hong Kong , 999077 Hong Kong SAR, China;
                [15] oDepartment of Microbiology and Immunology, Department of Pediatrics, University of Iowa , Iowa City, IA 52242;
                [16] pThai Red Cross Emerging Infectious Diseases Clinical Center, King Chulalongkorn Memorial Hospital and Chulalongkorn University , Bangkok 10330, Thailand;
                [17] qCenter for Food Animal Health (CFAH), Ohio Agricultural Research and Development Center, Animal Sciences Department, College of Food, Agricultural and Environmental Sciences, Veterinary Preventive Medicine Department, College of Veterinary Medicine, The Ohio State University , Wooster, OH 44691
                Author notes
                1To whom correspondence may be addressed. Email: keusch@ 123456bu.edu or saif.2@ 123456osu.edu .

                Edited by Xiang-Jin Meng, Virginia Polytechnic Institute and State University, Blacksburg, VA; received June 14, 2022; accepted August 18, 2022

                Author contributions: G.T.K., J.H.A., D.E.A., P.D., I.E., H.F., M.K., S.K.L., C.G.D.N., M.P., S.P., S.W., S.Y., and L.S. wrote the paper.

                Author information
                https://orcid.org/0000-0003-4791-5024
                https://orcid.org/0000-0002-2046-5695
                https://orcid.org/0000-0002-4671-7002
                https://orcid.org/0000-0002-8611-7845
                https://orcid.org/0000-0003-0348-4808
                https://orcid.org/0000-0001-8217-5995
                https://orcid.org/0000-0003-4213-2354
                https://orcid.org/0000-0001-7636-1900
                https://orcid.org/0000-0003-0447-2083
                https://orcid.org/0000-0002-3224-9009
                Article
                202202871
                10.1073/pnas.2202871119
                9586299
                36215506
                8349582b-1d9d-4ef4-bb76-041d538109f5
                Copyright © 2022 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 11
                Categories
                403
                447
                535
                Perspective
                Biological Sciences
                Applied Biological Sciences

                pandemic preparedness,covid-19 origins and spread,drivers of emerging infectious diseases,spillover and spillback,one health solutions

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