From People to <italic toggle="yes">Panthera</italic>: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo
Denise McAloose,
Melissa Laverack,
Leyi Wang,
Mary Lea Killian,
Leonardo C. Caserta,
Fangfeng Yuan,
Patrick K. Mitchell,
Krista Queen,
Matthew R. Mauldin,
Brittany D. Cronk,
Susan L. Bartlett,
John M. Sykes,
Stephanie Zec,
Tracy Stokol,
Karen Ingerman,
Martha A. Delaney,
Richard Fredrickson,
Marina Ivančić,
Melinda Jenkins-Moore,
Katie Mozingo,
Kerrie Franzen,
Nichole Hines Bergeson,
Laura Goodman,
Haibin Wang,
Ying Fang,
Colleen Olmstead,
Colleen McCann,
Patrick Thomas,
Erin Goodrich,
François Elvinger,
David C. Smith,
Suxiang Tong,
Sally Slavinski,
Paul P. Calle,
Karen Terio,
Mia Kim Torchetti,
Diego G. Diel
Affiliations
Denise McAloose
Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
Melissa Laverack
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Leyi Wang
Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA
Mary Lea Killian
National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA
Leonardo C. Caserta
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Fangfeng Yuan
Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA
Patrick K. Mitchell
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Krista Queen
Centers for Disease Control and Prevention, Atlanta, Georgia, USA
Matthew R. Mauldin
Centers for Disease Control and Prevention, Atlanta, Georgia, USA
Brittany D. Cronk
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Susan L. Bartlett
Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
John M. Sykes
Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
Stephanie Zec
Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
Tracy Stokol
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Karen Ingerman
Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
Martha A. Delaney
Zoological Pathology Program, College of Veterinary Medicine, University of Illinois, Brookfield, Illinois, USA
Richard Fredrickson
Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA
Marina Ivančić
Chicago Zoological Society, Chicago, Illinois, USA
Melinda Jenkins-Moore
National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA
Katie Mozingo
National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA
Kerrie Franzen
National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA
Nichole Hines Bergeson
National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA
Laura Goodman
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Haibin Wang
Centers for Disease Control and Prevention, Atlanta, Georgia, USA
Ying Fang
Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA
Colleen Olmstead
Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA
Colleen McCann
Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
Patrick Thomas
Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
Erin Goodrich
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
François Elvinger
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
David C. Smith
New York State Department of Agriculture and Markets, Albany, New York, USA
Suxiang Tong
Centers for Disease Control and Prevention, Atlanta, Georgia, USA
Sally Slavinski
New York City Department of Health and Mental Hygiene, Queens, New York, USA
Paul P. Calle
Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
Karen Terio
Zoological Pathology Program, College of Veterinary Medicine, University of Illinois, Brookfield, Illinois, USA
Mia Kim Torchetti
National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA
Diego G. Diel
Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
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.
