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].

Abstract

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.IMPORTANCE 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 in vivo 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.

Supporting text Virus Host Location
ferrets 79 H3N2 7 human-like 1 influenza 61 swine 267 transmission 55 Aerosols 2 Animals 1948 Cross Reactions 21 Ferrets 79 Hemagglutinin Glycoproteins, Influenza Virus 180 Humans 1440 Influenza A virus 186 Influenza A Virus, H1N1 Subtype 74 Influenza A Virus, H3N2 Subtype 48 Influenza, Human 286 Orthomyxoviridae Infections 228 Swine 258 Swine Diseases 153 United States 46 Zoonoses 397

Evidence records

7 total
Zoonotic Surveillance
1 records · 1 evidence types
Evidence type
1 records
OVE3876
Key finding

A 2010.1 H3N2 influenza A virus isolate (A/swine/Ohio/A01354299/2017 [sw/OH/2017]) was successfully isolated from a pig associated with the 2017 Ohio agricultural fair outbreak.

Virus
Host
Location
Not specified
Supporting text

A 2010.1 H3N2 IAV (A/swine/Ohio/A01354299/2017 [sw/OH/2017]) isolated from a pig in the agricultural fair outbreak.

Sample type
swine sample
Transmission Evidence
2 records · 2 evidence types
Evidence type
1 records
OVE3874
Key finding

Human H3N2v influenza cases occurred at an agricultural fair in Ohio in 2017, linked to concurrent infection of exhibition swine with 2010.1 H3N2 influenza A virus, indicating animal-to-human spillover.

Virus
Host
Location
Supporting text

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.

Method
virus genomic analysis | outbreak surveillance
Study design
epidemiological outbreak association at agricultural fair
Transmission direction
animal-to-human
Geographic raw
Ohio | United States
Country inferred
USA
Evidence type
1 records
OVE3875
Key finding

Genomic investigation of the 2017 Ohio agricultural fair outbreak showed that 2010.1 H3N2 influenza A virus isolates from swine and humans were nearly identical, linking human H3N2v cases to concurrent infections in exhibition pigs.

Virus
Host
Location
Supporting text

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 | case investigation
Transmission direction
animal-to-human
Geographic raw
Ohio
Country inferred
USA
Outbreak setting
agricultural fair
Outbreak time
2017
Outbreak scale
cluster of human H3N2v cases
Experimental Infection
3 records · 2 evidence types
Evidence type
1 records
OVE3877
Key finding

The swine H3N2 virus isolate sw/OH/2017 replicated efficiently in ferret respiratory tracts and produced mild clinical disease characterized by slight fever and moderate weight loss.

Virus
Host
Location
Not specified
Supporting text

sw/OH/2017 displayed robust replication in the ferret respiratory tract, causing slight fever and moderate weight loss.

Method
in vivo infection | clinical observation of fever and weight loss
Experimental system
in vivo ferret infection model
Evidence type
2 records
OVE3878
Key finding

The H3N2 influenza virus sw/OH/2017 efficiently transmitted by respiratory droplets from infected pigs to contact ferrets.

Virus
Host
Location
Not specified
Supporting text

sw/OH/2017 was capable of efficient respiratory droplet transmission from infected pigs to contact ferrets.

Method
in vivo transmission study | respiratory droplet transmission model | aerosol contact ferret exposure
Experimental system
respiratory droplet transmission model from pigs to ferrets
OVE3879
Key finding

An H3.2010.1 H3N2 influenza A virus transmitted from infected pigs to contact ferrets by respiratory droplets.

Virus
Host
Location
Not specified
Supporting text

Further, sw/OH/2017 was capable of efficient respiratory droplet transmission from infected pigs to contact ferrets.

Method
respiratory droplet transmission experiment | viral isolation | genomic analysis
Experimental system
in vivo experimental transmission study
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE3880
Key finding

A human seasonal H3 virus from the 2010-2011 influenza season was introduced into U.S. swine and established the H3.2010.1 lineage.

Virus
Host
Location
Not specified
Supporting text

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.

Analysis methods
genomic analysis | lineage analysis