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Volume 26, Number 12—December 2020
Research Letter

Lack of Susceptibility to SARS-CoV-2 and MERS-CoV in Poultry

David L. Suarez, Mary J. Pantin-Jackwood, David E. Swayne, Scott A. Lee, Suzanne M. DeBlois, and Erica SpackmanComments to Author 
Author affiliation: US Department of Agriculture, Athens, Georgia, USA

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Abstract

We challenged chickens, turkeys, ducks, quail, and geese with severe acute respiratory syndrome coronavirus 2 or Middle East respiratory syndrome coronavirus. We observed no disease and detected no virus replication and no serum antibodies. We concluded that poultry are unlikely to serve a role in maintenance of either virus.

Coronaviruses of animals periodically transmit to humans (1), as recently occurred with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). SARS-CoV-2 was recognized in December 2019 in cases of atypical pneumonia in hospitalized patients in Wuhan, China. The virus is a novel betacoronavirus, related to the now-eradicated severe acute respiratory syndrome coronavirus (SARS-CoV) from 2003, with which SARS-CoV-2 has 82% identity across the genome (2). SARS-CoV-2 is highly transmissible among humans and particularly virulent for elderly persons and those with certain underlying health conditions. Multiple studies have examined the susceptibility of domestic animals to SARS-CoV-2 to establish the risk for zoonotic transmission; 2 studies have shown chickens and Pekin ducks were not susceptible to infection (3,4).

Middle East respiratory syndrome coronavirus (MERS-CoV), another coronavirus of high concern associated with zoonotic infection, was first detected in patients with severe acute lower respiratory tract disease in Saudi Arabia in 2012. MERS-CoV causes lower respiratory disease, similar to the SARS-CoVs (5). Unlike SARS-CoV-2, MERS-CoV transmits poorly to humans and does not exhibit sustained human-to-human transmission; however, it has a high case fatality rate of »30%. Although the MERS-CoV case count is low, human cases continue to be reported, therefore there is a possibility for the virus to adapt to humans.

Based on sequence similarity, the closest relatives of SARS-CoV-2 and MERS-CoV are believed to be bat betacoronaviruses (6); the sequence difference between human and bat isolates suggests the existence of an intermediary host. For MERS-CoV, dromedary camels appear to be the primary natural reservoir of infection to humans, but other domestic animals seem to be susceptible to infection (7,8). Hemida et al. looked for MERS-CoV antibodies in chickens; all samples were negative (9).

Because poultry are so widespread and have close and extended contact with humans and other mammals in many production systems, including live animal markets, we conducted susceptibility studies with SARS-CoV-2 and MERS-CoV in 5 common poultry species. Embryonating chicken eggs (ECE) have been used for virus isolation culture, including use in vaccine production, for diverse avian and mammalian viruses; therefore, we tested ECE for their ability to support the replication of both viruses.

We examined 5 poultry species: chickens (Gallus gallus domesticus), turkeys (Meleagris gallopavo), Pekin ducks (Anas platyrhinchos domesticus), Japanese quail (Coturnix japonica), and white Chinese geese (Anser cygnoides). The US National Poultry Research Center Institutional Animal Care and Use Committee reviewed and approved all procedures involving animals; the Institutional Biosafety Committee approved the use of the viruses.

To evaluate their susceptibility to these viruses, 10 birds of each species were challenged with a virus isolate obtained from the Biodefense and Emerging Infections Research Resources Repository (BEI Resources; National Institute of Allergy and Infectious Diseases, National Institutes of Health). We used either the USA-WA1/2020 isolate of SARS-CoV-2 (BEI NR-58221) or the Florida/USA-2_SaudiArabia_2014 isolate of MERS-CoV (BEI NR-50415) (Appendix).

We collected oropharyngeal and cloacal swabs from all birds at 2, 4, and 7 days postchallenge (dpc) and tested them for virus by real-time reverse transcription PCR. At 14 dpc we collected serum specimens from the birds and tested for antibody to the challenge virus by microneutralization. No clinical signs were observed at any time in any species, and virus was not detected in any swab material (Table). Antibodies were not detected in serum from any birds at 14 dpc. These results suggest that neither virus replicated in any of the avian species evaluated or that they replicated at a level that was too low to be detected.

We tested ECE for their ability to support SARS-CoV-2 or MERS-CoV replication after inoculation with any of the 3 most common routes: yolk sac, chorioallantoic sac, or chorioallantoic membrane (Appendix). We collected yolk, allantoic fluid (albumin), and embryo tissues from inoculated eggs; we tested for viral replication by attempting virus isolation in Vero cells from the egg material after each of 2 ECE passages. We did not recover either virus in Vero cells from the inoculated ECEs, nor did we observe lesions in any of the embryos inoculated with SARS-CoV-2 or MERS-CoV. The ECE results with SARS-CoV-2 are consistent with the results reported by Barr et al. (10).

Identifying potential reservoir hosts of the novel coronaviruses is critical to controlling exposure and subsequent infection, as well as to preserving a safe and consistent food supply. None of the avian species nor the ECE appeared to support replication of either virus. Our findings demonstrate that poultry are unlikely to serve a role in the maintenance or transmission of either SARS-CoV-2 or MERS-CoV, and furthermore that ECE are not a viable laboratory host system.

Dr. Suarez is the research leader for the Exotic and Emerging Avian Viral Disease Research Unit of the Agricultural Research Service, USDA. His primary research interests are in the understanding and control of avian influenza and Newcastle disease viruses in poultry and other emerging viral diseases that threaten the poultry industry.

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Acknowledgments

We thank Jesse Gallagher, Melinda Vonkungthong, Anne Hurley-Bacon, Jasmina Luczo, James Doster, and Charles Foley for technical assistance with this work.

Severe acute respiratory syndrome coronavirus 2, isolate USA-WA1/2020, NR-52281 was deposited by the Centers for Disease Control and Prevention and obtained through BEI Resources, NIAID, NIH. Middle East respiratory syndrome coronavirus, Florida/USA-2_Saudi Arabia_2014, NR-50415 was obtained through BEI Resources, NIAID, NIH. Vero African green monkey kidney cells (ATCC CCL-81), FR-243, were obtained through the International Reagent Resource, Influenza Division, WHO Collaborating Center for Surveillance, Epidemiology and Control of Influenza, Centers for Disease Control and Prevention, Atlanta, GA, USA.

This work was supported by USDA-Agricultural Research Service (project no. 6040-32000-066-00-D).

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References

  1. Corman  VM, Muth  D, Niemeyer  D, Drosten  C. Hosts and sources of endemic human coronaviruses. Adv Virus Res. 2018;100:16388.DOIPubMed
  2. Chan  JF, Kok  KH, Zhu  Z, Chu  H, To  KK, Yuan  S, et al. Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg Microbes Infect. 2020;9:22136.DOIPubMed
  3. Schlottau  K, Rissmann  M, Graaf  A, Schön  J, Sehl  J, Wylezich  C, et al. SARS-CoV-2 in fruit bats, ferrets, pigs, and chickens: an experimental transmission study. Lancet Microbe. 2020;1:e21825. DOIPubMed
  4. Shi  J, Wen  Z, Zhong  G, Yang  H, Wang  C, Huang  B, et al. Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2. Science. 2020;368:101620. DOIPubMed
  5. The Lancet. MERS-CoV: a global challenge. Lancet. 2013;381:1960. DOIPubMed
  6. Hui  DS, Azhar  EI, Memish  ZA, Zumla  A. Human coronavirus infections—severe acute respiratory syndrome (SARS), Middle East respiratory syndrome (MERS), and SARS-CoV-2. Reference Module in Biomedical Sciences. 2020 [cited 2020 Sep 23].
  7. Ferguson  NM, Van Kerkhove  MD. Identification of MERS-CoV in dromedary camels. Lancet Infect Dis. 2014;14:934. DOIPubMed
  8. Kandeil  A, Gomaa  M, Shehata  M, El-Taweel  A, Kayed  AE, Abiadh  A, et al. Middle East respiratory syndrome coronavirus infection in non-camelid domestic mammals. Emerg Microbes Infect. 2019;8:1038. DOIPubMed
  9. Hemida  MG, Perera  RA, Wang  P, Alhammadi  MA, Siu  LY, Li  M, et al. Middle East Respiratory Syndrome (MERS) coronavirus seroprevalence in domestic livestock in Saudi Arabia, 2010 to 2013. Euro Surveill. 2013;18:20659. DOIPubMed
  10. Barr  IG, Rynehart  C, Whitney  P, Druce  J. SARS-CoV-2 does not replicate in embryonated hen’s eggs or in MDCK cell lines. Euro Surveill. 2020;25. DOIPubMed

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Table

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Cite This Article

DOI: 10.3201/eid2612.202989

Original Publication Date: November 16, 2020

Table of Contents – Volume 26, Number 12—December 2020

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Erica Spackman, US National Poultry Research Center, USDA Agricultural Research Service, 934 Station Rd, Athens, GA 30605, USA

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Page created: September 22, 2020
Page updated: November 23, 2020
Page reviewed: November 23, 2020
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
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