Reston Virus Causes Severe Respiratory Disease in Young Domestic Pigs

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2021 Jan 14

PMID 33443221

Citations 10

Authors

Elaine Haddock

Greg Saturday

Friederike Feldmann

Patrick W Hanley

Atsushi Okumura

Jamie Lovaglio

Dan Long

Tina Thomas

Dana P Scott

Mikayla Pulliam

Jurgen A Richt

Emmie de Wit

Heinz Feldmann

Affiliations

Soon will be listed here.

Abstract

Reston virus (RESTV), an ebolavirus, causes clinical disease in macaques but has yet only been associated with rare asymptomatic infections in humans. Its 2008 emergence in pigs in the Philippines raised concerns about food safety, pathogenicity, and zoonotic potential, questions that are still unanswered. Until today, the virulence of RESTV for pigs has remained elusive, with unclear pathogenicity in naturally infected animals and only one experimental study demonstrating susceptibility and evidence for shedding but no disease. Here we show that combined oropharyngeal and nasal infection of young (3- to 7-wk-old) Yorkshire cross pigs with RESTV resulted in severe respiratory disease, with most animals reaching humane endpoint within a week. RESTV-infected pigs developed severe cyanosis, tachypnea, and acute interstitial pneumonia, with RESTV shedding from oronasal mucosal membranes. Our studies indicate that RESTV should be considered a livestock pathogen with zoonotic potential.

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References

Yan F, He S, Banadyga L, Zhu W, Zhang H, Rahim M . Characterization of Reston virus infection in ferrets. Antiviral Res. 2019; 165:1-10. DOI: 10.1016/j.antiviral.2019.03.001. View

Fischer K, Jabaty J, Suluku R, Strecker T, Groseth A, Fehling S . Serological Evidence for the Circulation of Ebolaviruses in Pigs From Sierra Leone. J Infect Dis. 2018; 218(suppl_5):S305-S311. DOI: 10.1093/infdis/jiy330. View

Nfon C, Leung A, Smith G, Embury-Hyatt C, Kobinger G, Weingartl H . Immunopathogenesis of severe acute respiratory disease in Zaire ebolavirus-infected pigs. PLoS One. 2013; 8(4):e61904. PMC: 3633953. DOI: 10.1371/journal.pone.0061904. View

de Wit E, Munster V, Metwally S, Feldmann H . Assessment of rodents as animal models for Reston ebolavirus. J Infect Dis. 2011; 204 Suppl 3:S968-72. PMC: 3189989. DOI: 10.1093/infdis/jir330. View

Jahrling P, Geisbert T, Jaax N, Hanes M, Ksiazek T, Peters C . Experimental infection of cynomolgus macaques with Ebola-Reston filoviruses from the 1989-1990 U.S. epizootic. Arch Virol Suppl. 1996; 11:115-34. DOI: 10.1007/978-3-7091-7482-1_11. View

Weingartl H, Nfon C, Kobinger G . Review of Ebola virus infections in domestic animals. Dev Biol (Basel). 2013; 135:211-8. DOI: 10.1159/000178495. View

Kobinger G, Leung A, Neufeld J, Richardson J, Falzarano D, Smith G . Replication, pathogenicity, shedding, and transmission of Zaire ebolavirus in pigs. J Infect Dis. 2011; 204(2):200-8. DOI: 10.1093/infdis/jir077. View

Amman B, Jones M, Sealy T, Uebelhoer L, Schuh A, Bird B . Oral shedding of Marburg virus in experimentally infected Egyptian fruit bats (Rousettus aegyptiacus). J Wildl Dis. 2014; 51(1):113-24. PMC: 5022530. DOI: 10.7589/2014-08-198. View

Pan Y, Zhang W, Cui L, Hua X, Wang M, Zeng Q . Reston virus in domestic pigs in China. Arch Virol. 2012; 159(5):1129-32. DOI: 10.1007/s00705-012-1477-6. View

10.

Jahrling P, Geisbert T, Dalgard D, Johnson E, Ksiazek T, Hall W . Preliminary report: isolation of Ebola virus from monkeys imported to USA. Lancet. 1990; 335(8688):502-5. DOI: 10.1016/0140-6736(90)90737-p. View

11.

Jayme S, Field H, de Jong C, Olival K, Marsh G, Tagtag A . Molecular evidence of Ebola Reston virus infection in Philippine bats. Virol J. 2015; 12:107. PMC: 4504098. DOI: 10.1186/s12985-015-0331-3. View

12.

Urbanowicz R, McClure C, Sakuntabhai A, Sall A, Kobinger G, Muller M . Human Adaptation of Ebola Virus during the West African Outbreak. Cell. 2016; 167(4):1079-1087.e5. PMC: 5101188. DOI: 10.1016/j.cell.2016.10.013. View

13.

Diehl W, Lin A, Grubaugh N, Carvalho L, Kim K, Kyawe P . Ebola Virus Glycoprotein with Increased Infectivity Dominated the 2013-2016 Epidemic. Cell. 2016; 167(4):1088-1098.e6. PMC: 5115602. DOI: 10.1016/j.cell.2016.10.014. View

14.

Spengler J, Saturday G, Lavender K, Martellaro C, Keck J, Nichol S . Severity of Disease in Humanized Mice Infected With Ebola Virus or Reston Virus Is Associated With Magnitude of Early Viral Replication in Liver. J Infect Dis. 2017; 217(1):58-63. PMC: 5853858. DOI: 10.1093/infdis/jix562. View

15.

Cantoni D, Hamlet A, Michaelis M, Wass M, Rossman J . Risks Posed by Reston, the Forgotten Ebolavirus. mSphere. 2017; 1(6). PMC: 5196033. DOI: 10.1128/mSphere.00322-16. View

16.

Schuh A, Amman B, Jones M, Sealy T, Uebelhoer L, Spengler J . Modelling filovirus maintenance in nature by experimental transmission of Marburg virus between Egyptian rousette bats. Nat Commun. 2017; 8:14446. PMC: 5316840. DOI: 10.1038/ncomms14446. View

17.

Marsh G, Haining J, Robinson R, Foord A, Yamada M, Barr J . Ebola Reston virus infection of pigs: clinical significance and transmission potential. J Infect Dis. 2011; 204 Suppl 3:S804-9. DOI: 10.1093/infdis/jir300. View

18.

Miranda M, Miranda N . Reston ebolavirus in humans and animals in the Philippines: a review. J Infect Dis. 2011; 204 Suppl 3:S757-60. DOI: 10.1093/infdis/jir296. View

19.

Barrette R, Metwally S, Rowland J, Xu L, Zaki S, Nichol S . Discovery of swine as a host for the Reston ebolavirus. Science. 2009; 325(5937):204-6. DOI: 10.1126/science.1172705. View

20.

Weingartl H, Embury-Hyatt C, Nfon C, Leung A, Smith G, Kobinger G . Transmission of Ebola virus from pigs to non-human primates. Sci Rep. 2012; 2:811. PMC: 3498927. DOI: 10.1038/srep00811. View