Evolution of influenza A virus in intensive and free-range swine farms in Spain.

Paloma Encinas1 Gustavo Del Real1 Jayeeta Dutta2 Zenab Khan2 Harm van Bakel2 M Ángeles Martín Del Burgo1 Adolfo García-Sastre3 Martha I Nelson4
Affiliations 4 institutions
  1. Department of Biotechnology, National Institute of Agricultural and Food Research and Technology (INIA, CSIC), Ctra. de La Coruña Km 7.5, Madrid 28040, Spain.
  2. Genetics and Genomic Sciences, Hess Center for Science and Medicine, Icahn School of Medicine at Mount Sinai, 1470 Madison Avenue, New York, NY 10029, USA.
  3. Department of Microbiology, Icahn School of Medicine at Mount Sinai, 1 Gustave L. Levy Place, New York, NY 10029, USA.
  4. Laboratory of Parasitic Diseases, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 50 South Drive, Bethesda, MD 20892, USA.

Abstract

Swine harbor genetically diverse influenza A viruses (IAVs) with the capacity to host-switch to humans, causing global pandemics. Spain is the largest swine producer in Europe and has a mixed production system that includes 'white coat' pigs raised intensively in modern buildings and free-range Iberian pigs that interface differently with humans, wildlife, and other swine. Through active longitudinal IAV surveillance in nine Spanish provinces during 2015-9, we generated forty-seven complete or near-complete genome sequences from IAVs collected from swine in both systems. Genetically diverse IAVs were identified in intensively raised white pigs and free-range Iberian pigs, including new H3N1 reassortants. Both systems are dynamic environments for IAV evolution, but driven by different processes. IAVs in white pigs were genetically related to viruses found in swine raised intensively in other European countries, reflecting high rates of viral introduction following European trade routes. In contrast, IAVs in Iberian pigs have a genetic makeup shaped by frequent introductions of human IAVs, reflecting rearing practices with high rates of human contact. Transmission between white and Iberian pigs also occurred. In conclusion, Iberian swine with high rates of human contact harbor genetically diverse IAVs and potentially serve as intermediary hosts between white pigs and humans, presenting an understudied zoonotic risk that requires further investigation.

Supporting text Virus Host Location
ecology 17 evolution 62 genomic reassortment 2 influenza A virus 227 pandemic 15 reverse zoonosis 38

Evidence records

6 total
Zoonotic Surveillance
2 records · 2 evidence types
Evidence type
1 records
OVE5543
Key finding

Influenza A viruses were detected and sequenced from swine in both intensive and free-range systems across nine Spanish provinces between 2015 and 2019.

Virus
Host
Location
Supporting text

Through active longitudinal IAV surveillance in nine Spanish provinces during 2015-9, we generated forty-seven complete or near-complete genome sequences from IAVs collected from swine in both systems.

Method
active longitudinal surveillance | genome sequencing
Sample type
swine specimens
Geographic raw
nine Spanish provinces | Spain
Country inferred
ESP
Evidence type
1 records
OVE5548
Key finding

Free-range Iberian swine in Spain with frequent human contact harbor genetically diverse influenza A viruses and may act as intermediary hosts between white pigs and humans.

Virus
Host
Location
Supporting text

Spain is the largest swine producer in Europe and has a mixed production system that includes 'white coat' pigs raised intensively in modern buildings and free-range Iberian pigs that interface differently with humans, wildlife, and other swine. In conclusion, Iberian swine with high rates of human contact harbor genetically diverse IAVs and potentially serve as intermediary hosts between white pigs and humans, presenting an understudied zoonotic risk that requires further investigation.

Method
longitudinal influenza A virus surveillance | genomic sequencing
Sample type
swine samples
Geographic raw
Spain
Country inferred
ESP
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE5547
Key finding

Influenza A viruses were transmitted between white pigs and Iberian pigs in Spain.

Virus
Host
Location
Supporting text

Through active longitudinal IAV surveillance in nine Spanish provinces during 2015-9, we generated forty-seven complete or near-complete genome sequences from IAVs collected from swine in both systems. Transmission between white and Iberian pigs also occurred.

Method
genomic sequencing | phylogenetic analysis
Geographic raw
Spain
Genomic Evolution
3 records · 2 evidence types
Evidence type
1 records
OVE5544
Key finding

New H3N1 reassortant influenza A viruses were identified in intensively raised white pigs and free-range Iberian pigs in Spain.

Virus
Host
Not specified
Location
Not specified
Supporting text

Genetically diverse IAVs were identified in intensively raised white pigs and free-range Iberian pigs, including new H3N1 reassortants.

Event type
reassortment
Evidence type
2 records
OVE5545
Key finding

Phylogenetic analysis showed that influenza A viruses (IAVs) in white pigs were closely related to swine viruses from other European countries, indicating viral introduction through European trade routes.

Virus
Host
Location
Not specified
Supporting text

IAVs in white pigs were genetically related to viruses found in swine raised intensively in other European countries, reflecting high rates of viral introduction following European trade routes.

Analysis methods
phylogenetic analysis | genomic comparison
OVE5546
Key finding

Phylogenetic evidence indicated that IAVs in Iberian pigs have genetic composition derived from repeated introductions of human influenza A viruses due to frequent human contact.

Virus
Host
Location
Not specified
Supporting text

In contrast, IAVs in Iberian pigs have a genetic makeup shaped by frequent introductions of human IAVs, reflecting rearing practices with high rates of human contact.

Analysis methods
phylogenetic analysis | genomic comparison