SARS-CoV-2 Infection And Longitudinal Fecal Screening In Malayan Tigers (Panthera tigris jacksoni), Amur Tigers (Panthera tigris altaica), And African Lions (Panthera leo krugeri) At The Bronx Zoo, New York, USA

Abstract

Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) emerged as the cause of a global pandemic in 2019-2020. In March 2020 New York City became the USA epicenter for the pandemic. On March 27, 2020 a Malayan tiger (Panthera tigris jacksoni) at the Bronx Zoo in New York City developed a cough and wheezing with subsequent inappetence. Over the next week, an additional Malayan tiger and two Amur tigers (P. t. altaica) in the same building and three lions (Panthera leo krugeri) in a separate building also became ill. The index case was immobilized, and physical examination and bloodwork results were unremarkable. Thoracic radiography and ultrasonography revealed peribronchial cuffing with bronchiectasis, and mild lung consolidation with alveolar-interstitial syndrome, respectively. SARS-CoV-2 RNA was identified by real-time, reverse transcriptase PCR (rRT-PCR) on oropharyngeal and nasal swabs and tracheal wash fluid. Cytologic examination of tracheal wash fluid revealed necrosis, and viral RNA was detected in necrotic cells by in situ hybridization, confirming virus-associated tissue damage. SARS-CoV-2 was isolated from the tracheal wash fluid of the index case, as well as the feces from one Amur tiger and one lion. Fecal viral RNA shedding was confirmed in all seven clinical cases and an asymptomatic Amur tiger. Respiratory signs abated within 1-5 days for most animals, though persisted intermittently for 16 days in the index case. Fecal RNA shedding persisted for as long as 35 days beyond cessation of respiratory signs. This case series describes the clinical presentation, diagnostic evaluation, and management of tigers and lions infected with SARS-CoV-2, and describes the duration of viral RNA fecal shedding in these cases. This report documents the first known natural transmission of SARS-CoV-2 from humans to animals in the USA, and is the first report of SARS-CoV-2 in non-domestic felids.

Susceptibility of livestock and companion animals to COVID‐19

“…A longitudinal fecal screening also revealed fecal shedding in lion and tigers. This was the first natural infection of SARS‐CoV‐2 in nondomestic cats, possibly by reverse zoonosis 27 . Further, minks were also naturally infected from their caretaker, in two mink farms located in the southern Noord Brabant province of the Netherlands where COVID‐19 has stricken hard 28,29 .…”

“…Reverse zoonosis of SARS‐CoV‐2 was not only reported in domestic cats, but also in large cats. In the United States, four Malayan tigersand three lions in Bronx zoo, New York showed respiratory distress, mainly cough, and their fecal samples tested positive for SARS‐CoV‐2 indicating viral shedding and involvement of the respiratory and digestive system as seen in humans 27 . Thoracic radiography of the tiger revealed alveolar interstitial syndrome characterized by mild lung consolidation, peribronchial cuffing similar to the human lung in SARS‐CoV‐2 infections.…”

Assessing the Risks of SARS-CoV-2 in Wildlife

“…Observations from experimental and natural SARS-CoV-2 infections in animals clearly suggest relatively high susceptibility amongst felids (Felidae family). Both wild and domestic felids are amongst the most epidemiologically relevant animal hosts of SARS-CoV-2 because human-to-feline transmission has been sporadically recorded both in pet cats [40,42,65] and captive wild animals such as tigers and lions [41,66]. Moreover, there is experimental evidence for transmission amongst cats both via direct contact [67] and from airborne virus [32].…”

“…However, rare and endangered species could be at risk of exposure to infected people involved in research and conservation programmes. Domestic cats naturally infected with SARS-CoV-2 have often been reported as asymptomatic or showing only mild clinical signs, although some instances of more serious disease have also been reported [40,65,67], whereas only mild respiratory signs accompanied infection in captive tigers and lions [41,66]. It is therefore unclear whether infection could have notable impacts on wild felid populations.…”

Susceptibility of well-differentiated airway epithelial cell cultures from domestic and wildlife animals to SARS-CoV-2

“…Although humans are currently seen as the main hosts, the zoonotic origin, as well as the intermediate and potential spillback host reservoirs of SARS-CoV-2 is unknown. Interestingly, several reports indicate that SARS-CoV-2 spillover events from human to other animal species can occur [5][6][7][8][9] . These events are likely driven by close human-animal interactions and the conservation of crucial receptor binding motif (RBM) residues in the angiotensin-converting enzyme 2 (ACE2) orthologues, potentially facilitating SARS-CoV-2 entry 10,11 .…”