OmniVira

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

Denise McAloose1 Melissa Laverack2 Leyi Wang3 Mary Lea Killian4 Leonardo C Caserta2 Fangfeng Yuan5 Patrick K Mitchell2 Krista Queen6 Matthew R Mauldin6 Brittany D Cronk2 Susan L Bartlett7 John M Sykes7 Stephanie Zec7 Tracy Stokol2 Karen Ingerman7 Martha A Delaney8 Richard Fredrickson3 Marina Ivančić9 Melinda Jenkins-Moore4 Katie Mozingo4 Kerrie Franzen4 Nichole Hines Bergeson4 Laura Goodman2 Haibin Wang6 Ying Fang5 Colleen Olmstead3 Colleen McCann7 Patrick Thomas7 Erin Goodrich2 François Elvinger2 David C Smith10 Suxiang Tong6 Sally Slavinski11 Paul P Calle7 Karen Terio8 Mia Kim Torchetti4 Diego G Diel12
Affiliations 12 institutions
  1. Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA [email protected] [email protected].
  2. Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.
  3. Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA.
  4. National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA.
  5. Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA.
  6. Centers for Disease Control and Prevention, Atlanta, Georgia, USA.
  7. Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA.
  8. Zoological Pathology Program, College of Veterinary Medicine, University of Illinois, Brookfield, Illinois, USA.
  9. Chicago Zoological Society, Chicago, Illinois, USA.
  10. New York State Department of Agriculture and Markets, Albany, New York, USA.
  11. New York City Department of Health and Mental Hygiene, Queens, New York, USA.
  12. Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA [email protected] [email protected].
PMID33051368 DOI10.1128/mBio.02220-20 Year2020 Journal mBio Languageeng Statusepublish

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.

Supporting text Virus Host Location
in situ hybridization 3 lion 4 One Health 98 Panthera leo 2 Panthera tigris 1 rRT-PCR 1 SARS-CoV-2 550 tiger 3 virus isolation 7 whole-genome sequencing 9 zoo 3 zoonotic infection 9 Animals 1948 Animals, Zoo 18 Betacoronavirus 78 Coronavirus Infections 171 COVID-19 425 Genome, Viral 317 Haplotypes 2 Humans 1440 New York City 3 One Health 14 Pandemics 108 Panthera 5

Evidence records

3 total
Zoonotic Surveillance
2 records · 2 evidence types
Evidence type Virus Isolation
1 records
Evidence type Viral Detection
1 records
OVE4207 Viral Detection
Key finding

SARS-CoV-2 RNA was detected in respiratory secretions and feces from tigers and lions at the Bronx Zoo.

Virus
Severe acute respiratory syndrome coronavirus 2
Host
tiger Panthera tigris Natural host lion Panthera leo Natural host
Location
United States
Supporting text

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.

Method
RNA detection
Sample type
respiratory secretions | feces
Geographic raw
Bronx Zoo, NY
Country inferred
USA
Transmission Evidence
1 records · 1 evidence types
Evidence type Cross-species Transmission
1 records
OVE4209 Cross-species Transmission
Key finding

Epidemiologic and genomic evidence demonstrated human-to-tiger transmission of SARS-CoV-2 at the Bronx Zoo.

Virus
Severe acute respiratory syndrome coronavirus 2
Host
tiger Panthera tigris Natural host human Homo sapiens Natural host
Location
United States
Supporting text

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 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.

Method
epidemiologic data | genomic sequencing
Study design
natural infection investigation combining epidemiologic and genomic evidence
Transmission direction
human-to-animal
Geographic raw
Bronx Zoo, NY