Influenza Vaccination of Swine Reduces Public Health Risk at the Swine-Human Interface

Joshua N. Lorbach, Sarah W. Nelson, Sarah E. Lauterbach, Jacqueline M. Nolting, Eben Kenah, Dillon S. McBride, Marie R. Culhane, Christa Goodell, Andrew S. Bowman

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Influenza A viruses (IAV) in swine (IAV-S) pose serious risk to public health through spillover at the human-animal interface. Continued zoonotic transmission increases the likelihood novel IAV-S capable of causing the next influenza pandemic will emerge from this animal reservoir. Because current mitigation strategies are insufficient to prevent IAV zoonosis, we investigated the ability of swine vaccination to decrease IAV-S zoonotic transmission risk. We assessed postchallenge viral shedding in market-age swine vaccinated with either live-attenuated influenza virus (LAIV), killed influenza virus (KV), or sham vaccine (NV). We also assessed postchallenge transmission by exposing naive ferrets to pigs with contact types reflective of those experienced by humans in a field setting. LAIV and KV swine groups exhibited a nearly 100-fold reduction in peak nasal titer (LAIV mean, 4.55 log 50% tissue culture infectious dose [TCID50]/ml; KV mean, 4.53 log TCID50/ml) compared to NV swine (mean, 6.40 log TCID50/ml). Air sampling during the postchallenge period revealed decreased cumulative IAV in LAIV and KV study room air (LAIV, area under the concentration-time curve [AUC] of 57.55; KV, AUC = 24.29) compared to the NV study room (AUC = 86.92). Pairwise survival analysis revealed a significant delay in onset of infection among ferrets exposed to LAIV pigs versus NV pigs (rate ratio, 0.66; P = 0.028). Ferrets exposed to vaccinated pigs had lower cumulative virus titers in nasal wash samples (LAIV versus NV, P, 0.0001; KV versus NV, P= 0.3490) and experienced reduced clinical signs during infection. Our findings support the implementation of preexhibition influenza vaccination of swine to reduce the public health risk posed by IAV-S at agricultural exhibitions. IMPORTANCE Swine exhibited at agricultural fairs in North America have been the source of repeated zoonotic influenza A virus transmission, which creates a pathway for influenza pandemic emergence. We investigated the effect of using either live-attenuated influenza virus or killed influenza virus vaccines as prefair influenza vaccination of swine on zoonotic influenza transmission risk. Ferrets were exposed to the pigs in order to simulate human exposure in a field setting. We observed reductions in influenza A virus shedding in both groups of vaccinated pigs as well as the corresponding ferret exposure groups, indicating vaccination improved outcomes on both sides of the interface. There was also significant delay in onset of infection among ferrets that were exposed to live-attenuated virus-vaccinated pigs, which might be beneficial during longer fairs. Our findings indicate that policies mandating influenza vaccination of swine before fairs, while not currently common, would reduce the public health risk posed by influenza zoonosis.

Original languageEnglish (US)
Article numbere01170-20
JournalmSphere
Volume6
Issue number3
DOIs
StatePublished - May 2021

Bibliographical note

Funding Information:
We thank the CPMPSR at Ohio State for tissue specimen processing and Kara Corps for their guidance during histologic evaluation of tissue specimens. We also extend our gratitude for assistance provided by University Laboratory Animal Resource animal husbandry and veterinary staff at Ohio State. We thank William G. Lindsley (CDC/NIOSH) for providing NIOSH air samplers. Scientific editing was provided by Rhymes with Orange, LLC. Funding for this project was provided by Boehringer Ingelheim Vetmedica, Inc. While C.G. and other BIVI employees participated in the overall study design and manuscript preparation, the collection and analysis of experimental data were performed independently by J.N.L., E.K., S.W.N., S.E.L., J.M.N., D.S.M., and A.S.B. to limit the potential for commercial bias.

Funding Information:
Funding for this project was provided by Boehringer Ingelheim Vetmedica, Inc. While C.G. and other BIVI employees participated in the overall study design and manuscript preparation, the collection and analysis of experimental data were performed independently by J.N.L., E.K., S.W.N., S.E.L., J.M.N., D.S.M., and A.S.B. to limit the potential for commercial bias.

Publisher Copyright:
Copyright © 2021 Lorbach et al.

Keywords

  • Disease transmission
  • Infectious
  • Infectious disease
  • Influenza A virus
  • Preventive medicine
  • Swine
  • Transmission
  • Vaccines
  • Zoonoses

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