Literature detail

Aerosol Transmission from Infected Swine to Ferrets of an H3N2 Virus Collected from an Agricultural Fair and Associated with Human Variant Infections.

Bryan S Kaplan1 J Brian Kimble1 Jennifer Chang1 Tavis K Anderson1 Phillip C Gauger2 Alicia Janas-Martindale3 Mary Lea Killian3 Andrew S Bowman4 Amy L Vincent5
Affiliations 5 institutions
  1. Virus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA.
  2. Department of Veterinary Diagnostic and Production Animal Medicine, Iowa State University, Ames, Iowa, USA.
  3. National Veterinary Services Laboratories, USDA-APHIS, Ames, Iowa, USA.
  4. Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, Ohio, USA.
  5. Virus and Prion Research Unit, National Animal Disease Center, USDA-ARS, Ames, Iowa, USA [email protected].
PMID 32522849 2020 J Virol eng epublish
PubMed DOI Browse context

Article

Publication summary

Influenza A viruses (IAV) sporadically transmit from swine to humans, typically associated with agricultural fairs in the United States. A human seasonal H3 virus from the 2010-2011 IAV season was introduced into the U.S. swine population and termed H3.2010.1 to differentiate it from the previous swine H3 virus. This H3N2 lineage became widespread in the U.S. commercial swine population, subsequently spilling over into exhibition swine, and caused a majority of H3N2 variant (H3N2v) cases in humans in 2016 and 2017. A cluster of human H3N2v cases were reported at an agricultural fair in 2017 in Ohio, where 2010.1 H3N2 IAV was concurrently detected in exhibition swine. Genomic analysis showed that the swine and human isolates were nearly identical. In this study, we evaluated the propensity of a 2010.1 H3N2 IAV (A/swine/Ohio/A01354299/2017 [sw/OH/2017]) isolated from a pig in the agricultural fair outbreak to replicate in ferrets and transmit from swine to ferret. sw/OH/2017 displayed robust replication in the ferret respiratory tract, causing slight fever and moderate weight loss. Further, sw/OH/2017 was capable of efficient respiratory droplet transmission from infected pigs to contact ferrets. These findings establish a model for evaluating the propensity of swine IAV to transmit from pig to ferret as a measure of risk to the human population. The identification of higher-risk swine strains can then be targeted for control measures to limit the dissemination at human-swine interfaces to reduce the risk of zoonotic infections and to inform pandemic planning.<b>IMPORTANCE</b> A recently emerged lineage of human-like H3N2 (H3.2010.1) influenza A virus (IAV) from swine has been frequently detected in commercial and exhibition swine in recent years and has been associated with H3N2 variant cases in humans from 2016 and 2017. To demonstrate a model for characterizing the potential for zoonotic transmission associated with swine IAV, we performed an <i>in vivo</i> study of transmission between pigs infected with an H3.2010.1 H3N2 IAV and aerosol contact ferrets. The efficient interspecies transmission demonstrated for the H3.2010.1 IAV in swine emphasizes the need for further characterization of viruses circulating at the swine-human interface for transmission potential prior to human spillover and the development and implementation of more robust vaccines and control strategies to mitigate human exposure to higher-risk swine strains.

ferrets H3N2 human-like influenza swine transmission Aerosols Animals Cross Reactions Ferrets Hemagglutinin Glycoproteins, Influenza Virus Humans Influenza A virus Influenza A Virus, H1N1 Subtype Influenza A Virus, H3N2 Subtype Influenza, Human Orthomyxoviridae Infections Swine

Structured evidence records

Evidence records

4 total
2 records
Extraction confidence 0.95
Key finding

Human infections with H3N2v virus were directly linked to swine at agricultural fairs, confirmed by genomic similarity.

Virus
Location
Supporting text

Influenza A viruses (IAV) sporadically transmit from swine to humans, typically associated with agricultural fairs in the United States. A human seasonal H3 virus from the 2010-2011 IAV season was introduced into the U.S. swine population and termed H3.2010.1 to differentiate it from the previous swine H3 virus. This H3N2 lineage became widespread in the U.S. commercial swine population, subsequently spilling over into exhibition swine, and caused a majority of H3N2 variant (H3N2v) cases in humans in 2016 and 2017. A cluster of human H3N2v cases were reported at an agricultural fair in 2017 in Ohio, where 2010.1 H3N2 IAV was concurrently detected in exhibition swine. Genomic analysis showed that the swine and human isolates were nearly identical.

Method
genomic analysis
Study design
outbreak investigation
Transmission direction
animal-to-human
Geographic raw
Ohio
Country inferred
United States
Extraction confidence 0.90
Key finding

The H3.2010.1 H3N2 virus from swine efficiently transmitted to ferrets via aerosols, modeling human spillover risk.

Virus
Location
Supporting text

In this study, we evaluated the propensity of a 2010.1 H3N2 IAV (A/swine/Ohio/A01354299/2017 [sw/OH/2017]) isolated from a pig in the agricultural fair outbreak to replicate in ferrets and transmit from swine to ferret. sw/OH/2017 displayed robust replication in the ferret respiratory tract, causing slight fever and moderate weight loss. Further, sw/OH/2017 was capable of efficient respiratory droplet transmission from infected pigs to contact ferrets.

Method
in vivo study; aerosol transmission assay
Study design
animal experiment
Transmission direction
animal-to-human
Geographic raw
Ohio
Country inferred
United States
1 records
Extraction confidence 0.85
Key finding

Genomic analysis revealed that H3N2 influenza A virus isolates from swine and humans associated with a 2017 Ohio agricultural fair were nearly identical, indicating high genetic similarity between animal and human viruses.

Virus
Location
Not specified
Supporting text

Genomic analysis showed that the swine and human isolates were nearly identical.

Genes or proteins
whole genome
Analysis methods
genomic analysis
1 records
Extraction confidence 0.97
Key finding

The swine-origin H3N2 influenza A virus A/swine/Ohio/A01354299/2017 replicated efficiently in ferret respiratory tissue and transmitted via aerosol from infected pigs to ferrets.

Virus
Location
Not specified
Supporting text

In this study, we evaluated the propensity of a 2010.1 H3N2 IAV (A/swine/Ohio/A01354299/2017 [sw/OH/2017]) isolated from a pig in the agricultural fair outbreak to replicate in ferrets and transmit from swine to ferret. sw/OH/2017 displayed robust replication in the ferret respiratory tract ... and was capable of efficient respiratory droplet transmission from infected pigs to contact ferrets.

Method
experimental infection; transmission assay; replication assay
Sample type
respiratory tract
Experimental system
in vivo animal experiment