Reverse-zoonoses of 2009 H1N1 pandemic influenza A viruses and evolution in United States swine results in viruses with zoonotic potential

Abstract

The 2009 H1N1 pandemic (pdm09) lineage of influenza A virus (IAV) crosses interspecies barriers with frequent human-to-swine spillovers each year. These spillovers reassort and drift within swine populations, leading to genetically and antigenically novel IAV that represent a zoonotic threat. We quantified interspecies transmission of the pdm09 lineage, persistence in swine, and identified how evolution in swine impacted zoonotic risk. Human and swine pdm09 case counts between 2010 and 2020 were correlated and human pdm09 burden and circulation directly impacted the detection of pdm09 in pigs. However, there was a relative absence of pdm09 circulation in humans during the 2020–21 season that was not reflected in swine. During the 2020–21 season, most swine pdm09 detections originated from human-to-swine spillovers from the 2018–19 and 2019–20 seasons that persisted in swine. We identified contemporary swine pdm09 representatives of each persistent spillover and quantified cross-reactivity between human seasonal H1 vaccine strains and the swine strains using a panel of monovalent ferret antisera in hemagglutination inhibition (HI) assays. The swine pdm09s had variable antigenic reactivity to vaccine antisera, but each swine pdm09 clade exhibited significant reduction in cross-reactivity to one or more of the human seasonal vaccine strains. Further supporting zoonotic risk, we showed phylogenetic evidence for 17 swine-to-human transmission events of pdm09 from 2010 to 2021, 11 of which were not previously classified as variants, with each of the zoonotic cases associated with persistent circulation of pdm09 in pigs. These data demonstrate that reverse-zoonoses and evolution of pdm09 in swine results in viruses that are capable of zoonotic transmission and represent a potential pandemic threat.

Document Details

Document Type
Pub Defense Publication
Publication Date
Jul 27, 2023
Source ID
10.1371/journal.ppat.1011476

Entities

People

  • Alexey Markin
  • Amy L. Vincent Baker
  • Giovana Ciacci Zanella
  • Jianqiang Zhang
  • Karen M. Krueger
  • Phillip C Gauger
  • Tavis K Anderson
  • Zebulun Arendsee

Organizations

  • Agricultural Research Service
  • Animal and Plant Health Inspection Service
  • Defense Advanced Research Projects Agency
  • National Center for Immunization and Respiratory Diseases
  • National Institute of Allergy and Infectious Diseases
  • Oak Ridge Institute for Science and Education

Tags

Fields of Study

  • Biology

Readers

  • Infectious Disease/Epidemiology
  • Organizational Psychology.

Technology Areas

  • Biotechnology