From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo

被引:288
作者
McAloose, Denise [1 ]
Laverack, Melissa [2 ]
Wang, Leyi [3 ]
Killian, Mary Lea [4 ]
Caserta, Leonardo C. [2 ]
Yuan, Fangfeng [5 ]
Mitchell, Patrick K. [2 ]
Queen, Krista [6 ]
Mauldin, Matthew R. [6 ]
Cronk, Brittany D. [2 ]
Bartlett, Susan L. [1 ]
Sykes, John M. [1 ]
Zec, Stephanie [1 ,11 ]
Stokol, Tracy [2 ]
Ingerman, Karen [1 ]
Delaney, Martha A. [7 ]
Fredrickson, Richard [3 ]
Ivancic, Marina [8 ,12 ]
Jenkins-Moore, Melinda [4 ]
Mozingo, Katie [4 ]
Franzen, Kerrie [4 ]
Bergeson, Nichole Hines [4 ]
Goodman, Laura [2 ]
Wang, Haibin [6 ]
Fang, Ying [5 ]
Olmstead, Colleen [3 ]
McCann, Colleen [1 ]
Thomas, Patrick [1 ]
Goodrich, Erin [2 ]
Elvinger, Francois [2 ]
Smith, David C. [9 ]
Tong, Suxiang [6 ]
Slavinski, Sally [10 ]
Calle, Paul P. [1 ]
Terio, Karen [7 ]
Torchetti, Mia Kim [4 ]
Diel, Diego G. [2 ]
机构
[1] Bronx Zoo, Wildlife Conservat Soc, Bronx, NY 10460 USA
[2] Cornell Univ, Coll Vet Med, Dept Populat Med & Diagnost Sci, Anim Hlth Diagnost Ctr, Ithaca, NY 14853 USA
[3] Univ Illinois, Coll Vet Med, Vet Diagnost Lab, Urbana, IL 61801 USA
[4] USDA, Natl Vet Serv Labs, Anim & Plant Hlth Inspect Serv APHIS, Ames, IA 50010 USA
[5] Univ Illinois, Coll Vet Med, Dept Pathobiol, Urbana, IL 61801 USA
[6] Ctr Dis Control & Prevent, Atlanta, GA USA
[7] Univ Illinois, Coll Vet Med, Zool Pathol Program, Brookfield, IL USA
[8] Chicago Zool Soc, Chicago, IL USA
[9] New York State Dept Agr & Markets, Albany, NY USA
[10] New York City Dept Hlth & Mental Hyg, New York, NY USA
[11] Dickerson Pk Zoo, Springfield, MO USA
[12] ZooRedOne, Chicago, IL USA
关键词
One Health; Panthera leo; Panthera tigris; SARS-CoV-2; in situ hybridization; lion; rRT-PCR; tiger; virus isolation; whole-genome sequencing; zoo; zoonotic infection; NUCLEOCAPSID PROTEIN; HOST-RANGE; PERFORMANCE; PCR;
D O I
10.1128/mBio.02220-20
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
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.
引用
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页码:1 / 13
页数:13
相关论文
共 42 条
[1]   The proximal origin of SARS-CoV-2 [J].
Andersen, Kristian G. ;
Rambaut, Andrew ;
Lipkin, W. Ian ;
Holmes, Edward C. ;
Garry, Robert F. .
NATURE MEDICINE, 2020, 26 (04) :450-452
[2]   Median-joining networks for inferring intraspecific phylogenies [J].
Bandelt, HJ ;
Forster, P ;
Röhl, A .
MOLECULAR BIOLOGY AND EVOLUTION, 1999, 16 (01) :37-48
[3]   Real-time PCR for detection and differentiation of Streptococcus equi subsp equi and Streptococcus equi subsp zooepidemicus [J].
Baverud, V. ;
Johansson, S. K. ;
Aspan, A. .
VETERINARY MICROBIOLOGY, 2007, 124 (3-4) :219-229
[4]   Evolutionary origins of the SARS-CoV-2 sarbecovirus lineage responsible for the COVID-19 pandemic [J].
Boni, Maciej F. ;
Lemey, Philippe ;
Jiang, Xiaowei ;
Lam, Tommy Tsan-Yuk ;
Perry, Blair W. ;
Castoe, Todd A. ;
Rambaut, Andrew ;
Robertson, David L. .
NATURE MICROBIOLOGY, 2020, 5 (11) :1408-+
[5]   The emergence of SARS, MERS and novel SARS-2 coronaviruses in the 21st century [J].
da Costa, Vivaldo Gomes ;
Moreli, Marcos Lazaro ;
Saivish, Marielena Vogel .
ARCHIVES OF VIROLOGY, 2020, 165 (07) :1517-1526
[6]   Sustainable development must account for pandemic risk [J].
Di Marco, Moreno ;
Baker, Michelle L. ;
Daszak, Peter ;
De Barro, Paul ;
Eskew, Evan A. ;
Godde, Cecile M. ;
Harwood, Tom D. ;
Herrero, Mario ;
Hoskins, Andrew J. ;
Johnson, Erica ;
Karesh, William B. ;
Machalaba, Catherine ;
Garcia, Javier Navarro ;
Paini, Dean ;
Pirzl, Rebecca ;
Smith, Mark Stafford ;
Zambrana-Torrelio, Carlos ;
Ferrier, Simon .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2020, 117 (08) :3888-3892
[7]  
Fang Y, 2006, ADV EXP MED BIOL, V581, P153
[8]   Introductions and early spread of SARS-CoV-2 in the New York City area [J].
Gonzalez-Reiche, Ana S. ;
Hernandez, Matthew M. ;
Sullivan, Mitchell J. ;
Ciferri, Brianne ;
Alshammary, Hala ;
Obla, Ajay ;
Fabre, Shelcie ;
Kleiner, Giulio ;
Polanco, Jose ;
Khan, Zenab ;
Alburquerque, Bremy ;
van de Guchte, Adriana ;
Dutta, Jayeeta ;
Francoeur, Nancy ;
Melo, Betsaida Salom ;
Oussenko, Irina ;
Deikus, Gintaras ;
Soto, Juan ;
Sridhar, Shwetha Hara ;
Wang, Ying-Chih ;
Twyman, Kathryn ;
Kasarskis, Andrew ;
Altman, Deena R. ;
Smith, Melissa ;
Sebra, Robert ;
Aberg, Judith ;
Krammer, Florian ;
Garcia-Sastre, Adolfo ;
Luksza, Marta ;
Patel, Gopi ;
Paniz-Mondolfi, Alberto ;
Gitman, Melissa ;
Sordillo, Emilia Mia ;
Simon, Viviana ;
van Bakel, Harm .
SCIENCE, 2020, 369 (6501) :297-+
[9]   The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2 [J].
Gorbalenya, Alexander E. ;
Baker, Susan C. ;
Baric, Ralph S. ;
de Groot, Raoul J. ;
Drosten, Christian ;
Gulyaeva, Anastasia A. ;
Haagmans, Bart L. ;
Lauber, Chris ;
Leontovich, Andrey M. ;
Neuman, Benjamin W. ;
Penzar, Dmitry ;
Perlman, Stanley ;
Poon, Leo L. M. ;
Samborskiy, Dmitry V. ;
Sidorov, Igor A. ;
Sola, Isabel ;
Ziebuhr, John .
NATURE MICROBIOLOGY, 2020, 5 (04) :536-544
[10]   Factors associated with upper respiratory tract disease caused by feline herpesvirus, feline calicivirus, Chlamydophila felis and Bordetella bronchiseptica in cats:: experience from 218 European catteries [J].
Helps, CR ;
Lait, P ;
Damhuis, A ;
Björnehammar, U ;
Bolta, D ;
Brovida, C ;
Chabanne, L ;
Egberink, H ;
Ferrand, G ;
Fontbonne, A ;
Pennisi, MG ;
Gruffydd-Jones, I ;
Gunn-Moore, D ;
Hartmann, K ;
Lutz, H ;
Malandain, E ;
Möstl, K ;
Stengel, C ;
Harbour, DA ;
Graat, EAM .
VETERINARY RECORD, 2005, 156 (21) :669-673