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.

Highlights

  • Despite numerous barriers to transmission, zoonoses are the major cause of emerging infectious diseases in humans

  • We report natural infection of tigers (Panthera tigris) and lions (Panthera leo) with severe acute respiratory syndrome (SARS)-CoV-2 at the Wildlife Conservation Society’s (WCS’s) Bronx Zoo, New York, NY, and provide a detailed genomic characterization of viruses obtained from infected animals and keepers who had close contact with the SARS-CoV-2-positive animals

  • Our results document susceptibility and natural SARS-CoV-2 infection in tigers and lions. These were the first confirmed animal infections in the United States and the first to be described in a nondomestic species in the world

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Summary

Introduction

Despite numerous barriers to transmission, zoonoses are the major cause of emerging infectious diseases in humans. 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. A recent study suggests the virus may have been circulating in bats for several decades [7], and an early cluster of human COVID-19 cases had an epidemiological link to the Huanan Seafood Wholesale market in Wuhan where a variety of live wild animals were sold [4]. The current SARS-CoV-2 pandemic and outbreaks of severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) before it raise awareness and concerns about zoonotic (animal-tohuman) diseases and cross-species transmission of coronaviruses [8,9,10,11]. Virus shedding and horizontal transmission have been shown in cats and ferrets [15,16,17] following experimental inoculation

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