Detection and Characterization of Influenza A Virus Endemic Circulation in Suckling and Nursery Pigs Originating from Vaccinated Farms in the Same Production System

Dias, Alessandra Silva; Vincent Baker, Amy L.; Baker, Rodney B.; Zhang, Jianqiang; Zeller, Michael A.; Kitikoon, Pravina; Gauger, Phillip C.

doi:10.3390/v16040626

Title: Detection and Characterization of Influenza A Virus Endemic Circulation in Suckling and Nursery Pigs Originating from Vaccinated Farms in the Same Production System

Journal Article · 18 April 2024 · Viruses

DOI: https://doi.org/10.3390/v16040626 · OSTI ID:2471229

^[1]; Vincent Baker, Amy L. ^[2]; Baker, Rodney B. ^[3];

^[3];

^[3]; Kitikoon, Pravina ^[4];

^[3]

Minas Gerais State University, Belo Horizonte, MG (Brazil)
US Department of Agriculture (USDA), Ames, IA (United States)
Iowa State University, Ames, IA (United States)
US Department of Agriculture (USDA), Ames, IA (United States); Ceva Animal Health, Lenexa, KS (United States)

Inactivated influenza A virus (IAV) vaccines help reduce clinical disease in suckling piglets, although endemic infections still exist. The objective of this study was to evaluate the detection of IAV in suckling and nursery piglets from IAV-vaccinated sows from farms with endemic IAV infections. Eight nasal swab collections were obtained from 135 two-week-old suckling piglets from four farms every other week from March to September 2013. Oral fluid samples were collected from the same group of nursery piglets. IAV RNA was detected in 1.64% and 31.01% of individual nasal swabs and oral fluids, respectively. H1N2 was detected most often, with sporadic detection of H1N1 and H3N2. Whole-genome sequences of IAV isolated from suckling piglets revealed an H1 hemagglutinin (HA) from the 1B.2.2.2 clade and N2 neuraminidase (NA) from the 2002A clade. The internal gene constellation of the endemic H1N2 was TTTTPT with a pandemic lineage matrix. The HA gene had 97.59% and 97.52% nucleotide and amino acid identities, respectively, to the H1 1B.2.2.2 used in the farm-specific vaccine. A similar H1 1B.2.2.2 was detected in the downstream nursery. These data demonstrate the low frequency of IAV detection in suckling piglets and downstream nurseries from farms with endemic infections in spite of using farm-specific IAV vaccines in sows.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC); USDA

Grant/Contract Number:: SC0014664; AC05-06OR23100

OSTI ID:: 2471229

Journal Information:: Viruses, Journal Name: Viruses Journal Issue: 4 Vol. 16; ISSN 1999-4915

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (55)

A Brief Introduction to Influenza A Virus in Swine Vincent, Amy L.; Anderson, Tavis K.; Lager, Kelly M. Methods in Molecular Biology https://doi.org/10.1007/978-1-0716-0346-8_18	book	January 2020
Characterization of a newly emerged genetic cluster of H1N1 and H1N2 swine influenza virus in the United States Vincent, Amy L.; Ma, Wenjun; Lager, Kelly M. Virus Genes, Vol. 39, Issue 2 https://doi.org/10.1007/s11262-009-0386-6	journal	July 2009
Effect of maternally derived antibodies on the clinical signs and immune response in pigs after primary and secondary infection with an influenza H1N1 virus Loeffen, W. L. A.; Heinen, P. P.; Bianchi, A. T. J. Veterinary Immunology and Immunopathology, Vol. 92, Issue 1-2 https://doi.org/10.1016/S0165-2427(03)00019-9	journal	March 2003
The epidemiology and evolution of influenza viruses in pigs Brown, Ian H. Veterinary Microbiology, Vol. 74, Issue 1-2 https://doi.org/10.1016/S0378-1135(00)00164-4	journal	May 2000
Porcine reproductive and respiratory syndrome virus: routes of excretion Wills, Robert W.; Zimmerman, Jeff J.; Yoon, Kyoung-Jin Veterinary Microbiology, Vol. 57, Issue 1 https://doi.org/10.1016/S0378-1135(97)00079-5	journal	June 1997
Influenza A virus in swine breeding herds: Combination of vaccination and biosecurity practices can reduce likelihood of endemic piglet reservoir White, L. A.; Torremorell, M.; Craft, M. E. Preventive Veterinary Medicine, Vol. 138 https://doi.org/10.1016/j.prevetmed.2016.12.013	journal	March 2017
Breed-to-wean farm factors associated with influenza A virus infection in piglets at weaning Chamba Pardo, Fabian Orlando; Schelkopf, Adam; Allerson, Matthew Preventive Veterinary Medicine, Vol. 161 https://doi.org/10.1016/j.prevetmed.2018.10.008	journal	December 2018
Finding PRRSV in sow herds: Family oral fluids vs. serum samples from due-to-wean pigs Almeida, M. N.; Zhang, M.; Zimmerman, J. J. Preventive Veterinary Medicine, Vol. 193 https://doi.org/10.1016/j.prevetmed.2021.105397	journal	August 2021
Reverse zoonosis of influenza to swine: new perspectives on the human–animal interface Nelson, Martha I.; Vincent, Amy L. Trends in Microbiology, Vol. 23, Issue 3 https://doi.org/10.1016/j.tim.2014.12.002	journal	March 2015
Safety, immunogenicity, and efficacy of an alphavirus replicon-based swine influenza virus hemagglutinin vaccine Vander Veen, Ryan L.; Loynachan, Alan T.; Mogler, Mark A. Vaccine, Vol. 30, Issue 11 https://doi.org/10.1016/j.vaccine.2012.01.030	journal	March 2012
The impact of maternally derived immunity on influenza A virus transmission in neonatal pig populations Allerson, Matt; Deen, John; Detmer, Susan E. Vaccine, Vol. 31, Issue 3 https://doi.org/10.1016/j.vaccine.2012.11.023	journal	January 2013
Bivalent hemagglutinin and neuraminidase influenza replicon particle vaccines protect pigs against influenza a virus without causing vaccine associated enhanced respiratory disease Wymore Brand, Meghan; Anderson, Tavis K.; Kitikoon, Pravina Vaccine, Vol. 40, Issue 38 https://doi.org/10.1016/j.vaccine.2022.07.042	journal	September 2022
The immune response and maternal antibody interference to a heterologous H1N1 swine influenza virus infection following vaccination Kitikoon, Pravina; Nilubol, Dachrit; Erickson, Barbara J. Veterinary Immunology and Immunopathology, Vol. 112, Issue 3-4 https://doi.org/10.1016/j.vetimm.2006.02.008	journal	August 2006
Porcine circovirus-2 and concurrent infections in the field Ellis, J. Veterinary Microbiology, Vol. 98, Issue 2 https://doi.org/10.1016/j.vetmic.2003.10.008	journal	February 2004
Influenza A virus vaccines for swine Vincent, Amy L.; Perez, Daniel R.; Rajao, Daniela Veterinary Microbiology, Vol. 206 https://doi.org/10.1016/j.vetmic.2016.11.026	journal	July 2017
Heterologous challenge in the presence of maternally-derived antibodies results in vaccine-associated enhanced respiratory disease in weaned piglets Rajao, Daniela S.; Sandbulte, Matthew R.; Gauger, Phillip C. Virology, Vol. 491 https://doi.org/10.1016/j.virol.2016.01.015	journal	April 2016
The development of oral fluid-based diagnostics and applications in veterinary medicine Prickett, John R.; Zimmerman, Jeffrey J. Animal Health Research Reviews, Vol. 11, Issue 2 https://doi.org/10.1017/S1466252310000010	journal	March 2010
Alphavirus replicon vaccines Vander Veen, Ryan L.; Harris, D. L. Hank; Kamrud, Kurt I. Animal Health Research Reviews, Vol. 13, Issue 1 https://doi.org/10.1017/S1466252312000011	journal	March 2012
Molecular evidence for interspecies transmission of H3N2pM/H3N2v influenza A viruses at an Ohio agricultural fair, July 2012 Bowman, Andrew S.; Sreevatsan, Srinand; Killian, Mary L. Emerging Microbes & Infections, Vol. 1, Issue 1 https://doi.org/10.1038/emi.2012.33	journal	July 2012
An integrated semiconductor device enabling non-optical genome sequencing Rothberg, Jonathan M.; Hinz, Wolfgang; Rearick, Todd M. Nature, Vol. 475, Issue 7356 https://doi.org/10.1038/nature10242	journal	July 2011
Global migration of influenza A viruses in swine Nelson, Martha I.; Viboud, Cécile; Vincent, Amy L. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7696	journal	March 2015
Human Infections With Influenza A(H3N2) Variant Virus in the United States, 2011-2012 Epperson, S.; Jhung, M.; Richards, S. Clinical Infectious Diseases, Vol. 57, Issue suppl 1 https://doi.org/10.1093/cid/cit272	journal	June 2013
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
High turnover drives prolonged persistence of influenza in managed pig herds Pitzer, Virginia E.; Aguas, Ricardo; Riley, Steven Journal of The Royal Society Interface, Vol. 13, Issue 119 https://doi.org/10.1098/rsif.2016.0138	journal	June 2016
The genomic evolution of H1 influenza A viruses from swine detected in the United States between 2009 and 2016 Gao, Shibo; Anderson, Tavis K.; Walia, Rasna R. Journal of General Virology, Vol. 98, Issue 8 https://doi.org/10.1099/jgv.0.000885	journal	August 2017
Global transmission of influenza viruses from humans to swine Nelson, Martha I.; Gramer, Marie R.; Vincent, Amy L. Journal of General Virology, Vol. 93, Issue 10 https://doi.org/10.1099/vir.0.044974-0	journal	October 2012
Genotype patterns of contemporary reassorted H3N2 virus in US swine Kitikoon, Pravina; Nelson, Martha I.; Killian, Mary Lea Journal of General Virology, Vol. 94, Issue 6 https://doi.org/10.1099/vir.0.051839-0	journal	June 2013
Swine Influenza A Viruses and the Tangled Relationship with Humans Anderson, Tavis K.; Chang, Jennifer; Arendsee, Zebulun W. Cold Spring Harbor Perspectives in Medicine, Vol. 11, Issue 3 https://doi.org/10.1101/cshperspect.a038737	journal	January 2020
Population dynamics of cocirculating swine influenza A viruses in the United States from 2009 to 2012 Anderson, Tavis K.; Nelson, Martha I.; Kitikoon, Pravina Influenza and Other Respiratory Viruses, Vol. 7 https://doi.org/10.1111/irv.12193	journal	November 2013
Regional patterns of genetic diversity in swine influenza A viruses in the United States from 2010 to 2016 Walia, Rasna R.; Anderson, Tavis K.; Vincent, Amy L. Influenza and Other Respiratory Viruses, Vol. 13, Issue 3 https://doi.org/10.1111/irv.12559	journal	January 2019
A matrix gene–based multiplex real‐time RT‐PCR for detection and differentiation of 2009 pandemic H1N1 and other influenza A viruses in North America Harmon, Karen; Bower, Leslie; Kim, Won‐Il Influenza and Other Respiratory Viruses, Vol. 4, Issue 6 https://doi.org/10.1111/j.1750-2659.2010.00153.x	journal	October 2010
Characterization of Influenza A Outbreaks in Minnesota Swine Herds and Measures Taken to Reduce the Risk of Zoonotic Transmission Beaudoin, A.; Johnson, S.; Davies, P. Zoonoses and Public Health, Vol. 59, Issue 2 https://doi.org/10.1111/j.1863-2378.2011.01423.x	journal	July 2011
Infection Dynamics of Pandemic 2009 H1N1 Influenza Virus in a Two-Site Swine Herd Allerson, M. W.; Davies, P. R.; Gramer, M. R. Transboundary and Emerging Diseases, Vol. 61, Issue 6 https://doi.org/10.1111/tbed.12053	journal	January 2013
Effect of influenza A virus sow vaccination on infection in pigs at weaning: A prospective longitudinal study Chamba Pardo, Fabian O.; Allerson, Matthew; Culhane, Marie Transboundary and Emerging Diseases, Vol. 68, Issue 1 https://doi.org/10.1111/tbed.13688	journal	July 2020
Pathogenic and Antigenic Properties of Phylogenetically Distinct Reassortant H3N2 Swine Influenza Viruses Cocirculating in the United States Richt, J. A.; Lager, K. M.; Janke, B. H. Journal of Clinical Microbiology, Vol. 41, Issue 7 https://doi.org/10.1128/JCM.41.7.3198-3205.2003	journal	July 2003
Complete Genome Sequencing of Influenza A Viruses within Swine Farrow-to-Wean Farms Reveals the Emergence, Persistence, and Subsidence of Diverse Viral Genotypes Diaz, Andres; Marthaler, Douglas; Culhane, Marie Journal of Virology, Vol. 91, Issue 18 https://doi.org/10.1128/JVI.00745-17	journal	September 2017
Genetic Reassortment of Avian, Swine, and Human Influenza A Viruses in American Pigs Zhou, Nan Nan; Senne, Dennis A.; Landgraf, John S. Journal of Virology, Vol. 73, Issue 10 https://doi.org/10.1128/JVI.73.10.8851-8856.1999	journal	October 1999
Haemagglutinin and nucleoprotein replicon particle vaccination of swine protects against the pandemic H1N1 2009 virus Vander Veen, R. L.; Mogler, M. A.; Russell, B. J. Veterinary Record, Vol. 173, Issue 14 https://doi.org/10.1136/vr.101741	journal	October 2013
Detection of Influenza a Virus in Porcine Oral Fluid Samples Detmer, Susan E.; Patnayak, Devi P.; Jiang, Yin Journal of Veterinary Diagnostic Investigation, Vol. 23, Issue 2 https://doi.org/10.1177/104063871102300207	journal	March 2011
Swine influenza virus infection dynamics in two pig farms; results of a longitudinal assessment Simon-Grifé, Meritxell; Martín-Valls, Gerard E.; Vilar, María J. Veterinary Research, Vol. 43, Issue 1 https://doi.org/10.1186/1297-9716-43-24	journal	January 2012
Dynamics of influenza A virus infections in permanently infected pig farms: evidence of recurrent infections, circulation of several swine influenza viruses and reassortment events Rose, Nicolas; Hervé, Séverine; Eveno, Eric Veterinary Research, Vol. 44, Issue 1 https://doi.org/10.1186/1297-9716-44-72	journal	January 2013
Comparison of individual, group and environmental sampling strategies to conduct influenza surveillance in pigs Garrido-Mantilla, Jorge; Alvarez, Julio; Culhane, Marie BMC Veterinary Research, Vol. 15, Issue 1 https://doi.org/10.1186/s12917-019-1805-0	journal	February 2019
Farm management practices associated with influenza A virus contamination of people working in Midwestern United States swine farms Lopez-Moreno, Gustavo; Culhane, Marie R.; Davies, Peter Porcine Health Management, Vol. 9, Issue 1 https://doi.org/10.1186/s40813-023-00304-2	journal	May 2023
Rapid Development of an Efficacious Swine Vaccine for Novel H1N1 Vander Veen, Ryan; Kamrud, Kurt; Mogler, Mark PLoS Currents, Vol. 1 https://doi.org/10.1371/currents.RRN1123	journal	October 2009
Airborne Detection and Quantification of Swine Influenza A Virus in Air Samples Collected Inside, Outside and Downwind from Swine Barns Corzo, Cesar A.; Culhane, Marie; Dee, Scott PLoS ONE, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pone.0071444	journal	August 2013
Mathematical Modeling of Influenza A Virus Dynamics within Swine Farms and the Effects of Vaccination Reynolds, Jennifer J. H.; Torremorell, Montserrat; Craft, Meggan E. PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0106177	journal	August 2014
Association between Influenza A Virus Infection and Pigs Subpopulations in Endemically Infected Breeding Herds Diaz, Andres; Perez, Andres; Sreevatsan, Srinand PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0129213	journal	June 2015
Effect of strain-specific maternally-derived antibodies on influenza A virus infection dynamics in nursery pigs Chamba Pardo, Fabian Orlando; Wayne, Spencer; Culhane, Marie Rene PLOS ONE, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pone.0210700	journal	January 2019
Outbreak of Influenza A(H3N2) Variant Virus Infections Among Persons Attending Agricultural Fairs Housing Infected Swine — Michigan and Ohio, July–August 2016 Schicker, Rebekah S.; Rossow, John; Eckel, Seth MMWR. Morbidity and Mortality Weekly Report, Vol. 65, Issue 42 https://doi.org/10.15585/mmwr.mm6542a1	journal	October 2016
Field study on swine influenza virus (SIV) infection in weaner pigs and sows Meiners, C.; Loesken, S.; Doehring, S. Tierärztliche Praxis Ausgabe G: Großtiere / Nutztiere, Vol. 42, Issue 06 https://doi.org/10.15653/TPG-131130	journal	January 2014
Recent zoonoses caused by influenza A viruses Alexander, D. J.; Brown, I. H. Revue Scientifique et Technique de l'OIE, Vol. 19, Issue 1 https://doi.org/10.20506/rst.19.1.1220	journal	April 2000
Multiple Reassortment between Pandemic (H1N1) 2009 and Endemic Influenza Viruses in Pigs, United States Ducatez, Mariette F.; Hause, Ben; Stigger-Rosser, Evelyn Emerging Infectious Diseases, Vol. 17, Issue 9 https://doi.org/10.3201/1709.110338	journal	September 2011
Adaptation of Human Influenza Viruses to Swine Rajao, Daniela S.; Vincent, Amy L.; Perez, Daniel R. Frontiers in Veterinary Science, Vol. 5 https://doi.org/10.3389/fvets.2018.00347	journal	January 2019
Optimal Use of Vaccines for Control of Influenza A Virus in Swine Sandbulte, Matthew; Spickler, Anna; Zaabel, Pamela Vaccines, Vol. 3, Issue 1 https://doi.org/10.3390/vaccines3010022	journal	January 2015

Similar Records

Interspecies Transmission from Pigs to Ferrets of Antigenically Distinct Swine H1 Influenza A Viruses with Reduced Reactivity to Candidate Vaccine Virus Antisera as Measures of Relative Zoonotic Risk

Journal Article · 2022 · Viruses · OSTI ID:2424092

Kimble, J. Brian; Souza, Carine K.; Anderson, Tavis K.; +7 more

Regional patterns of genetic diversity in swine influenza A viruses in the United States from 2010 to 2016

Journal Article · 2019 · Influenza and Other Respiratory Viruses · OSTI ID:1625884

Walia, Rasna R.; Anderson, Tavis K.; Vincent, Amy L.

Antigenic Characterization and Pandemic Risk Assessment of North American H1 Influenza A Viruses Circulating in Swine

Journal Article · 2022 · Microbiology Spectrum · OSTI ID:2424086

Venkatesh, Divya; Anderson, Tavis K.; Kimble, J. Brian; +9 more

Related Subjects

60 APPLIED LIFE SCIENCES
endemic infection
influenza A virus
sucking piglets
swine
vaccine
virology

Title: Detection and Characterization of Influenza A Virus Endemic Circulation in Suckling and Nursery Pigs Originating from Vaccinated Farms in the Same Production System

Citation Formats

References (55)

Similar Records

Related Subjects