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From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo.
mBio. 2020 10 13; 11(5)MBIO

Abstract

Despite numerous barriers to transmission, zoonoses are the major cause of emerging infectious diseases in humans. Among these, severe acute respiratory syndrome (SARS), Middle East respiratory syndrome (MERS), and ebolaviruses have killed thousands; the human immunodeficiency virus (HIV) has killed millions. Zoonoses and human-to-animal cross-species transmission are driven by human actions and have important management, conservation, and public health implications. The current SARS-CoV-2 pandemic, which presumably originated from an animal reservoir, has killed more than half a million people around the world and cases continue to rise. In March 2020, New York City was a global epicenter for SARS-CoV-2 infections. During this time, four tigers and three lions at the Bronx Zoo, NY, developed mild, abnormal respiratory signs. We detected SARS-CoV-2 RNA in respiratory secretions and/or feces from all seven animals, live virus in three, and colocalized viral RNA with cellular damage in one. We produced nine whole SARS-CoV-2 genomes from the animals and keepers and identified different SARS-CoV-2 genotypes in the tigers and lions. Epidemiologic and genomic data indicated human-to-tiger transmission. These were the first confirmed cases of natural SARS-CoV-2 animal infections in the United States and the first in nondomestic species in the world. We highlight disease transmission at a nontraditional interface and provide information that contributes to understanding SARS-CoV-2 transmission across species.IMPORTANCE The human-animal-environment interface of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is an important aspect of the coronavirus disease 2019 (COVID-19) pandemic that requires robust One Health-based investigations. Despite this, few reports describe natural infections in animals or directly link them to human infections using genomic data. In the present study, we describe the first cases of natural SARS-CoV-2 infection in tigers and lions in the United States and provide epidemiological and genetic evidence for human-to-animal transmission of the virus. Our data show that tigers and lions were infected with different genotypes of SARS-CoV-2, indicating two independent transmission events to the animals. Importantly, infected animals shed infectious virus in respiratory secretions and feces. A better understanding of the susceptibility of animal species to SARS-CoV-2 may help to elucidate transmission mechanisms and identify potential reservoirs and sources of infection that are important in both animal and human health.

Authors+Show Affiliations

Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA dmcaloose@wcs.org dgdiel@cornell.edu.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA.National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.Centers for Disease Control and Prevention, Atlanta, Georgia, USA.Centers for Disease Control and Prevention, Atlanta, Georgia, USA.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA.Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA.Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA.Zoological Pathology Program, College of Veterinary Medicine, University of Illinois, Brookfield, Illinois, USA.Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA.Chicago Zoological Society, Chicago, Illinois, USA.National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA.National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA.National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA.National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.Centers for Disease Control and Prevention, Atlanta, Georgia, USA.Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA.Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA.Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA.Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.New York State Department of Agriculture and Markets, Albany, New York, USA.Centers for Disease Control and Prevention, Atlanta, Georgia, USA.New York City Department of Health and Mental Hygiene, Queens, New York, USA.Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA.Zoological Pathology Program, College of Veterinary Medicine, University of Illinois, Brookfield, Illinois, USA.National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA.Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA dmcaloose@wcs.org dgdiel@cornell.edu.

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

33051368

Citation

McAloose, Denise, et al. "From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo." MBio, vol. 11, no. 5, 2020.
McAloose D, Laverack M, Wang L, et al. From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo. mBio. 2020;11(5).
McAloose, D., Laverack, M., Wang, L., Killian, M. L., Caserta, L. C., Yuan, F., Mitchell, P. K., Queen, K., Mauldin, M. R., Cronk, B. D., Bartlett, S. L., Sykes, J. M., Zec, S., Stokol, T., Ingerman, K., Delaney, M. A., Fredrickson, R., Ivančić, M., Jenkins-Moore, M., ... Diel, D. G. (2020). From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo. MBio, 11(5). https://doi.org/10.1128/mBio.02220-20
McAloose D, et al. From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo. mBio. 2020 10 13;11(5) PubMed PMID: 33051368.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo. AU - McAloose,Denise, AU - Laverack,Melissa, AU - Wang,Leyi, AU - Killian,Mary Lea, AU - Caserta,Leonardo C, AU - Yuan,Fangfeng, AU - Mitchell,Patrick K, AU - Queen,Krista, AU - Mauldin,Matthew R, AU - Cronk,Brittany D, AU - Bartlett,Susan L, AU - Sykes,John M, AU - Zec,Stephanie, AU - Stokol,Tracy, AU - Ingerman,Karen, AU - Delaney,Martha A, AU - Fredrickson,Richard, AU - Ivančić,Marina, AU - Jenkins-Moore,Melinda, AU - Mozingo,Katie, AU - Franzen,Kerrie, AU - Bergeson,Nichole Hines, AU - Goodman,Laura, AU - Wang,Haibin, AU - Fang,Ying, AU - Olmstead,Colleen, AU - McCann,Colleen, AU - Thomas,Patrick, AU - Goodrich,Erin, AU - Elvinger,François, AU - Smith,David C, AU - Tong,Suxiang, AU - Slavinski,Sally, AU - Calle,Paul P, AU - Terio,Karen, AU - Torchetti,Mia Kim, AU - Diel,Diego G, Y1 - 2020/10/13/ PY - 2020/10/14/entrez PY - 2020/10/15/pubmed PY - 2020/11/5/medline KW - One Health KW - Panthera leo KW - Panthera tigris KW - SARS-CoV-2 KW - in situ hybridization KW - lion KW - rRT-PCR KW - tiger KW - virus isolation KW - whole-genome sequencing KW - zoo KW - zoonotic infection JF - mBio JO - mBio VL - 11 IS - 5 N2 - Despite numerous barriers to transmission, zoonoses are the major cause of emerging infectious diseases in humans. Among these, severe acute respiratory syndrome (SARS), Middle East respiratory syndrome (MERS), and ebolaviruses have killed thousands; the human immunodeficiency virus (HIV) has killed millions. Zoonoses and human-to-animal cross-species transmission are driven by human actions and have important management, conservation, and public health implications. The current SARS-CoV-2 pandemic, which presumably originated from an animal reservoir, has killed more than half a million people around the world and cases continue to rise. In March 2020, New York City was a global epicenter for SARS-CoV-2 infections. During this time, four tigers and three lions at the Bronx Zoo, NY, developed mild, abnormal respiratory signs. We detected SARS-CoV-2 RNA in respiratory secretions and/or feces from all seven animals, live virus in three, and colocalized viral RNA with cellular damage in one. We produced nine whole SARS-CoV-2 genomes from the animals and keepers and identified different SARS-CoV-2 genotypes in the tigers and lions. Epidemiologic and genomic data indicated human-to-tiger transmission. These were the first confirmed cases of natural SARS-CoV-2 animal infections in the United States and the first in nondomestic species in the world. We highlight disease transmission at a nontraditional interface and provide information that contributes to understanding SARS-CoV-2 transmission across species.IMPORTANCE The human-animal-environment interface of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is an important aspect of the coronavirus disease 2019 (COVID-19) pandemic that requires robust One Health-based investigations. Despite this, few reports describe natural infections in animals or directly link them to human infections using genomic data. In the present study, we describe the first cases of natural SARS-CoV-2 infection in tigers and lions in the United States and provide epidemiological and genetic evidence for human-to-animal transmission of the virus. Our data show that tigers and lions were infected with different genotypes of SARS-CoV-2, indicating two independent transmission events to the animals. Importantly, infected animals shed infectious virus in respiratory secretions and feces. A better understanding of the susceptibility of animal species to SARS-CoV-2 may help to elucidate transmission mechanisms and identify potential reservoirs and sources of infection that are important in both animal and human health. SN - 2150-7511 UR - https://www.unboundmedicine.com/medline/citation/33051368/From_People_to_Panthera:_Natural_SARS_CoV_2_Infection_in_Tigers_and_Lions_at_the_Bronx_Zoo_ L2 - http://mbio.asm.org/cgi/pmidlookup?view=long&pmid=33051368 DB - PRIME DP - Unbound Medicine ER -