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Home / Equine Research Bank / Emerg Infect Dis / Human Immunity and Susceptibility to Influenza A(H3) Viruses...
Emerging infectious diseases2022; 29(1); 98-109; doi: 10.3201/eid2901.220943

Human Immunity and Susceptibility to Influenza A(H3) Viruses of Avian, Equine, and Swine Origin.

Abstract: Influenza A viruses (IAVs) of subtype H3 that infect humans are antigenically divergent from those of birds, horses, and swine. Human immunity against these viruses might be limited, implying potential pandemic risk. To determine human risk, we selected 4 avian, 1 equine, and 3 swine IAVs representing major H3 lineages. We tested serum collected during 2017-2018 from 286 persons in Belgium for hemagglutination inhibiting antibodies and virus neutralizing antibodies against those animal-origin IAVs and tested replication in human airway epithelia. Seroprevalence rates for circulating IAVs from swine in North America were >51%, swine in Europe 7%-37%, and birds and equids ≤12%. Replication was efficient for cluster IV-A IAVs from swine in North America and IAVs from swine in Europe, intermediate for IAVs from horses and poultry, and absent for IAVs from wild birds and a novel human-like swine IAV in North America. Public health risk may be highest for swine H3 IAVs.
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Publication Date: 2022-12-28 PubMed ID: 36573615PubMed Central: PMC9796212DOI: 10.3201/eid2901.220943Google Scholar: Lookup
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  • Journal Article
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  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research focuses on understanding human immunity against Influenza A viruses (IAVs) of the H3 subtype originating from birds, horses, and pigs, which are dissimilar to those infecting humans, suggesting limited immunity and potential pandemic risks.

Research Methodology & Sample Selection

  • The researchers selected seven representative IAVs of the H3 subtype from various animal lineages (four from birds, one from horses, and three from pigs).
  • They collected serum samples from a cohort of 286 individuals in Belgium during 2017-2018.
  • The selected IAVs and serum samples served as the basis for analyzing human immunity against animal-origin IAVs.

Testing for Immunity

  • The scientists tested the serum samples for hemagglutination inhibiting antibodies and virus neutralizing antibodies against the chosen animal-origin IAVs.
  • The levels of these antibodies in the serum samples provided insight into the human immune response to these IAVs.

Evaluating Virus Replication in Human Cells

  • The researchers also tested the replication of selected IAVs in human airway epithelia, an essential step in the viral infection process.
  • The efficiency of virus replication in human cells helps determine the potential infectivity of the virus strains.

Results

  • The research unveiled relatively high seroprevalence rates for IAVs from pigs in North America (>51%), indicating a substantial exposure of the Belgian population to these viruses.
  • Lower prevalence rates were observed for IAVs from pigs in Europe (7%-37%) and from birds and horses (≤12%).
  • The replication efficiency was found to be high for some IAVs from pigs (both in North America and Europe) but was intermediate for IAVs from horses and poultry, and absent for IAVs from wild birds and a new human-like pig IAV in North America.

Implications

  • The study results underscore that the public health risk from the H3 subtype of IAVs may be highest for those originating from pigs.
  • This information is valuable in estimating potential pandemic risks and prioritizing disease prevention strategies.

Cite This Article

APA
Vandoorn E, Stadejek W, Leroux-Roels I, Leroux-Roels G, Parys A, Van Reeth K. (2022). Human Immunity and Susceptibility to Influenza A(H3) Viruses of Avian, Equine, and Swine Origin. Emerg Infect Dis, 29(1), 98-109. https://doi.org/10.3201/eid2901.220943

Publication

Emerging infectious diseases
ISSN: 1080-6059
NlmUniqueID: 9508155
Country: United States
Language: English
Volume: 29
Issue: 1
Pages: 98-109

Researcher Affiliations

Vandoorn, Elien
    Stadejek, Wojciech
      Leroux-Roels, Isabel
        Leroux-Roels, Geert
          Parys, Anna
            Van Reeth, Kristien

              MeSH Terms

              • Animals
              • Humans
              • Horses
              • Swine
              • Influenza A virus
              • Influenza, Human / epidemiology
              • Orthomyxoviridae Infections / epidemiology
              • Orthomyxoviridae Infections / veterinary
              • Seroepidemiologic Studies
              • Birds
              • Swine Diseases / epidemiology

              References

              This article includes 49 references
              1. Fang R, Min Jou W, Huylebroeck D, Devos R, Fiers W. Complete structure of A/duck/Ukraine/63 influenza hemagglutinin gene: animal virus as progenitor of human H3 Hong Kong 1968 influenza hemagglutinin.. Cell 1981 Aug;25(2):315-23.
                pubmed: 6169439doi: 10.1016/0092-8674(81)90049-0google scholar: lookup
              2. Bailey E, Long LP, Zhao N, Hall JS, Baroch JA, Nolting J, Senter L, Cunningham FL, Pharr GT, Hanson L, Slemons R, DeLiberto TJ, Wan XF. Antigenic Characterization of H3 Subtypes of Avian Influenza A Viruses from North America.. Avian Dis 2016 May;60(1 Suppl):346-53.
                pmc: PMC4911812pubmed: 27309078doi: 10.1637/11086-041015-regrgoogle scholar: lookup
              3. Pu J, Liu QF, Xia YJ, Fan YL, Brown EG, Tian FL, Liu JH. Genetic analysis of H3 subtype influenza viruses isolated from domestic ducks in northern China during 2004-2005.. Virus Genes 2009 Feb;38(1):136-42.
                pubmed: 19067150doi: 10.1007/s11262-008-0300-7google scholar: lookup
              4. Woodward A, Rash AS, Medcalf E, Bryant NA, Elton DM. Using epidemics to map H3 equine influenza virus determinants of antigenicity.. Virology 2015 Jul;481:187-98.
                pubmed: 25797606doi: 10.1016/j.virol.2015.02.027google scholar: lookup
              5. World Organisation for Animal Health. OIE expert surveillance panel on equine influenza vaccine composition. 2020. Apr 16 [cited 2021 Aug 27]. https://oiebulletin.fr/?officiel=08-4-2-2020-1-panel
              6. Anderson TK, Chang J, Arendsee ZW, Venkatesh D, Souza CK, Kimble JB, Lewis NS, Davis CT, Vincent AL. Swine Influenza A Viruses and the Tangled Relationship with Humans.. Cold Spring Harb Perspect Med 2021 Mar 1;11(3).
                pmc: PMC7919397pubmed: 31988203doi: 10.1101/cshperspect.a038737google scholar: lookup
              7. Qiu Y, Muller CP, Van Reeth K. Lower seroreactivity to European than to North American H3N2 swine influenza viruses in humans, Luxembourg, 2010.. Euro Surveill 2015 Apr 2;20(13):25-33.
                pubmed: 25860393doi: 10.2807/1560-7917.es2015.20.13.21078google scholar: lookup
              8. Lorbach JN, Fitzgerald T, Nolan C, Nolting JM, Treanor JJ, Topham DJ, Bowman AS. Gaps in Serologic Immunity against Contemporary Swine-Origin Influenza A Viruses among Healthy Individuals in the United States.. Viruses 2021 Jan 18;13(1).
                pmc: PMC7830885pubmed: 33477472doi: 10.3390/v13010127google scholar: lookup
              9. Krumbholz A, Lange J, Dürrwald R, Walther M, Müller TH, Kühnel D, Wutzler P, Sauerbrei A, Zell R. Prevalence of antibodies to European porcine influenza viruses in humans living in high pig density areas of Germany.. Med Microbiol Immunol 2014 Feb;203(1):13-24.
                pubmed: 24013183doi: 10.1007/s00430-013-0309-ygoogle scholar: lookup
              10. Hoschler K, Thompson C, Casas I, Ellis J, Galiano M, Andrews N, Zambon M. Population susceptibility to North American and Eurasian swine influenza viruses in England, at three time points between 2004 and 2011.. Euro Surveill 2013 Sep 5;18(36):pii=20578.
                pubmed: 24079379doi: 10.2807/1560-7917.es2013.18.36.20578google scholar: lookup
              11. US Centers for Disease Control and Prevention. Novel influenza A virus infections [cited 2021 Nov 21]. https://gis.cdc.gov/grasp/fluview/Novel_Influenza.html
              12. Freidl GS, Meijer A, de Bruin E, de Nardi M, Munoz O, Capua I, Breed AC, Harris K, Hill A, Kosmider R, Banks J, von Dobschuetz S, Stark K, Wieland B, Stevens K, van der Werf S, Enouf V, van der Meulen K, Van Reeth K, Dauphin G, Koopmans M. Influenza at the animal-human interface: a review of the literature for virological evidence of human infection with swine or avian influenza viruses other than A(H5N1).. Euro Surveill 2014 May 8;19(18).
                pubmed: 24832117doi: 10.2807/1560-7917.es2014.19.18.20793google scholar: lookup
              13. Piralla A, Moreno A, Orlandi ME, Percivalle E, Chiapponi C, Vezzoli F, Baldanti F. Swine Influenza A(H3N2) Virus Infection in Immunocompromised Man, Italy, 2014.. Emerg Infect Dis 2015 Jul;21(7):1189-91.
                pmc: PMC4480377pubmed: 26079745doi: 10.3201/eid2107.140981google scholar: lookup
              14. Xie T, Anderson BD, Daramragchaa U, Chuluunbaatar M, Gray GC. A Review of Evidence that Equine Influenza Viruses Are Zoonotic.. Pathogens 2016 Jul 12;5(3).
                pmc: PMC5039430pubmed: 27420100doi: 10.3390/pathogens5030050google scholar: lookup
              15. Baz M, Paskel M, Matsuoka Y, Zengel J, Cheng X, Jin H, Subbarao K. Replication and immunogenicity of swine, equine, and avian h3 subtype influenza viruses in mice and ferrets.. J Virol 2013 Jun;87(12):6901-10.
                pmc: PMC3676140pubmed: 23576512doi: 10.1128/jvi.03520-12google scholar: lookup
              16. Steensels M, Gelaude P, Van Borm S, Van Den Berg T, Cargnel M, Roupie V, Rauw F, Lambrecht B. Atypical Pathogenicity of Avian Influenza (H3N1) Virus Involved in Outbreak, Belgium, 2019.. Emerg Infect Dis 2020 Aug;26(8):1899-1903.
                pmc: PMC7392414pubmed: 32687049doi: 10.3201/eid2608.191338google scholar: lookup
              17. Tan X, Yan X, Liu Y, Wu Y, Liu JY, Mu M, Zhao J, Wang X, Li JQ, Wen L, Guo P, Zhou ZG, Li XB, Bao PT. A case of human infection by H3N8 influenza virus.. Emerg Microbes Infect 2022 Dec;11(1):2214-2217.
                pmc: PMC9542523pubmed: 36000153doi: 10.1080/22221751.2022.2117097google scholar: lookup
              18. World Health Organization. Tool for Influenza Pandemic Risk Assessment (TIPRA) version 1. 2016 May.
              19. Fragaszy E, Ishola DA, Brown IH, Enstone J, Nguyen-Van-Tam JS, Simons R, Tucker AW, Wieland B, Williamson SM, Hayward AC, Wood JL. Increased risk of A(H1N1)pdm09 influenza infection in UK pig industry workers compared to a general population cohort.. Influenza Other Respir Viruses 2016 Jul;10(4):291-300.
                pmc: PMC4910179pubmed: 26611769doi: 10.1111/irv.12364google scholar: lookup
              20. Sikkema RS, Freidl GS, de Bruin E, Koopmans M. Weighing serological evidence of human exposure to animal influenza viruses - a literature review.. Euro Surveill 2016 Nov 3;21(44).
                pmc: PMC5114483pubmed: 27874827doi: 10.2807/1560-7917.es.2016.21.44.30388google scholar: lookup
              21. Zhou N, He S, Zhang T, Zou W, Shu L, Sharp GB, Webster RG. Influenza infection in humans and pigs in southeastern China.. Arch Virol 1996;141(3-4):649-61.
                pubmed: 8645101doi: 10.1007/bf01718323google scholar: lookup
              22. Burnell FJ, Holmes MA, Roiko AH, Lowe JB, Heil GL, White SK, Gray GC. Little evidence of human infection with equine influenza during the 2007 epizootic, Queensland, Australia.. J Clin Virol 2014 Feb;59(2):100-3.
                pubmed: 24360918doi: 10.1016/j.jcv.2013.11.011google scholar: lookup
              23. Khurelbaatar N, Krueger WS, Heil GL, Darmaa B, Ulziimaa D, Tserennorov D, Baterdene A, Anderson BD, Gray GC. Little evidence of avian or equine influenza virus infection among a cohort of Mongolian adults with animal exposures, 2010-2011.. PLoS One 2014;9(1):e85616.
                pmc: PMC3897462pubmed: 24465622doi: 10.1371/journal.pone.0085616google scholar: lookup
              24. Larson KR, Heil GL, Chambers TM, Capuano A, White SK, Gray GC. Serological evidence of equine influenza infections among persons with horse exposure, Iowa.. J Clin Virol 2015 Jun;67:78-83.
                pubmed: 25959164doi: 10.1016/j.jcv.2015.04.009google scholar: lookup
              25. Ilyushina NA, Ikizler MR, Kawaoka Y, Rudenko LG, Treanor JJ, Subbarao K, Wright PF. Comparative study of influenza virus replication in MDCK cells and in primary cells derived from adenoids and airway epithelium.. J Virol 2012 Nov;86(21):11725-34.
                pmc: PMC3486302pubmed: 22915797doi: 10.1128/jvi.01477-12google scholar: lookup
              26. Shin DL, Yang W, Peng JY, Sawatsky B, von Messling V, Herrler G, Wu NH. Avian Influenza A Virus Infects Swine Airway Epithelial Cells without Prior Adaptation.. Viruses 2020 May 28;12(6).
                pmc: PMC7374723pubmed: 32481674doi: 10.3390/v12060589google scholar: lookup
              27. Sun X, Pulit-Penaloza JA, Belser JA, Pappas C, Pearce MB, Brock N, Zeng H, Creager HM, Zanders N, Jang Y, Tumpey TM, Davis CT, Maines TR. Pathogenesis and Transmission of Genetically Diverse Swine-Origin H3N2 Variant Influenza A Viruses from Multiple Lineages Isolated in the United States, 2011-2016.. J Virol 2018 Aug 15;92(16).
                pmc: PMC6069210pubmed: 29848587doi: 10.1128/jvi.00665-18google scholar: lookup
              28. Driskell EA, Jones CA, Stallknecht DE, Howerth EW, Tompkins SM. Avian influenza virus isolates from wild birds replicate and cause disease in a mouse model of infection.. Virology 2010 Apr 10;399(2):280-9.
                pubmed: 20123144doi: 10.1016/j.virol.2010.01.005google scholar: lookup
              29. Solórzano A, Foni E, Córdoba L, Baratelli M, Razzuoli E, Bilato D, Martín del Burgo MÁ, Perlin DS, Martínez J, Martínez-Orellana P, Fraile L, Chiapponi C, Amadori M, del Real G, Montoya M. Cross-Species Infectivity of H3N8 Influenza Virus in an Experimental Infection in Swine.. J Virol 2015 Nov;89(22):11190-202.
                pmc: PMC4645675pubmed: 26311894doi: 10.1128/jvi.01509-15google scholar: lookup
              30. Walia RR, Anderson TK, Vincent AL. Regional patterns of genetic diversity in swine influenza A viruses in the United States from 2010 to 2016.. Influenza Other Respir Viruses 2019 May;13(3):262-273.
                pmc: PMC6468071pubmed: 29624873doi: 10.1111/irv.12559google scholar: lookup
              31. Henritzi D, Petric PP, Lewis NS, Graaf A, Pessia A, Starick E, Breithaupt A, Strebelow G, Luttermann C, Parker LMK, Schröder C, Hammerschmidt B, Herrler G, Beilage EG, Stadlbauer D, Simon V, Krammer F, Wacheck S, Pesch S, Schwemmle M, Beer M, Harder TC. Surveillance of European Domestic Pig Populations Identifies an Emerging Reservoir of Potentially Zoonotic Swine Influenza A Viruses.. Cell Host Microbe 2020 Oct 7;28(4):614-627.e6.
                pubmed: 32721380doi: 10.1016/j.chom.2020.07.006google scholar: lookup
              32. Choi JG, Kang HM, Kim MC, Paek MR, Kim HR, Kim BS, Kwon JH, Kim JH, Lee YJ. Genetic relationship of H3 subtype avian influenza viruses isolated from domestic ducks and wild birds in Korea and their pathogenic potential in chickens and ducks.. Vet Microbiol 2012 Mar 23;155(2-4):147-57.
                pubmed: 21955449doi: 10.1016/j.vetmic.2011.08.028google scholar: lookup
              33. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets.. Mol Biol Evol 2016 Jul;33(7):1870-4.
                pmc: PMC8210823pubmed: 27004904doi: 10.1093/molbev/msw054google scholar: lookup
              34. Rajão DS, Gauger PC, Anderson TK, Lewis NS, Abente EJ, Killian ML, Perez DR, Sutton TC, Zhang J, Vincent AL. Novel Reassortant Human-Like H3N2 and H3N1 Influenza A Viruses Detected in Pigs Are Virulent and Antigenically Distinct from Swine Viruses Endemic to the United States.. J Virol 2015 Nov;89(22):11213-22.
                pmc: PMC4645639pubmed: 26311895doi: 10.1128/jvi.01675-15google scholar: lookup
              35. Van Reeth K, Gregory V, Hay A, Pensaert M. Protection against a European H1N2 swine influenza virus in pigs previously infected with H1N1 and/or H3N2 subtypes.. Vaccine 2003 Mar 28;21(13-14):1375-81.
                pubmed: 12615433doi: 10.1016/s0264-410x(02)00688-6google scholar: lookup
              36. Van Poucke SG, Nicholls JM, Nauwynck HJ, Van Reeth K. Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution.. Virol J 2010 Feb 16;7:38.
                pmc: PMC2829537pubmed: 20158900doi: 10.1186/1743-422x-7-38google scholar: lookup
              37. Boda B, Benaoudia S, Huang S, Bonfante R, Wiszniewski L, Tseligka ED, Tapparel C, Constant S. Antiviral drug screening by assessing epithelial functions and innate immune responses in human 3D airway epithelium model.. Antiviral Res 2018 Aug;156:72-79.
                pmc: PMC7113743pubmed: 29890184doi: 10.1016/j.antiviral.2018.06.007google scholar: lookup
              38. Liu F, Levine MZ. Heterologous Antibody Responses Conferred by A(H3N2) Variant and Seasonal Influenza Vaccination Against Newly Emerged 2016-2018 A(H3N2) Variant Viruses in Healthy Persons.. Clin Infect Dis 2020 Dec 15;71(12):3061-3070.
                pmc: PMC8974393pubmed: 31858129doi: 10.1093/cid/ciz1203google scholar: lookup
              39. Ciminski K, Chase GP, Beer M, Schwemmle M. Influenza A Viruses: Understanding Human Host Determinants.. Trends Mol Med 2021 Feb;27(2):104-112.
                pubmed: 33097424doi: 10.1016/j.molmed.2020.09.014google scholar: lookup
              40. Stewart CE, Torr EE, Mohd Jamili NH, Bosquillon C, Sayers I. Evaluation of differentiated human bronchial epithelial cell culture systems for asthma research.. J Allergy (Cairo) 2012;2012:943982.
                pmc: PMC3263641pubmed: 22287976doi: 10.1155/2012/943982google scholar: lookup
              41. Fonville JM, Wilks SH, James SL, Fox A, Ventresca M, Aban M, Xue L, Jones TC, Le NMH, Pham QT, Tran ND, Wong Y, Mosterin A, Katzelnick LC, Labonte D, Le TT, van der Net G, Skepner E, Russell CA, Kaplan TD, Rimmelzwaan GF, Masurel N, de Jong JC, Palache A, Beyer WEP, Le QM, Nguyen TH, Wertheim HFL, Hurt AC, Osterhaus ADME, Barr IG, Fouchier RAM, Horby PW, Smith DJ. Antibody landscapes after influenza virus infection or vaccination.. Science 2014 Nov 21;346(6212):996-1000.
                pmc: PMC4246172pubmed: 25414313doi: 10.1126/science.1256427google scholar: lookup
              42. Guan L, Shi J, Kong X, Ma S, Zhang Y, Yin X, He X, Liu L, Suzuki Y, Li C, Deng G, Chen H. H3N2 avian influenza viruses detected in live poultry markets in China bind to human-type receptors and transmit in guinea pigs and ferrets.. Emerg Microbes Infect 2019;8(1):1280-1290.
                pmc: PMC6746299pubmed: 31495283doi: 10.1080/22221751.2019.1660590google scholar: lookup
              43. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. Mapping the antigenic and genetic evolution of influenza virus.. Science 2004 Jul 16;305(5682):371-6.
                pubmed: 15218094doi: 10.1126/science.1097211google scholar: lookup
              44. de Jong JC, Smith DJ, Lapedes AS, Donatelli I, Campitelli L, Barigazzi G, Van Reeth K, Jones TC, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. Antigenic and genetic evolution of swine influenza A (H3N2) viruses in Europe.. J Virol 2007 Apr;81(8):4315-22.
                pmc: PMC1866135pubmed: 17287258doi: 10.1128/jvi.02458-06google scholar: lookup
              45. Tharakaraman K, Raman R, Stebbins NW, Viswanathan K, Sasisekharan V, Sasisekharan R. Antigenically intact hemagglutinin in circulating avian and swine influenza viruses and potential for H3N2 pandemic.. Sci Rep 2013;3:1822.
                pmc: PMC3650665pubmed: 23661027doi: 10.1038/srep01822google scholar: lookup
              46. Broberg E, Nicoll A, Amato-Gauci A. Seroprevalence to influenza A(H1N1) 2009 virus--where are we?. Clin Vaccine Immunol 2011 Aug;18(8):1205-12.
                pmc: PMC3147351pubmed: 21653743doi: 10.1128/cvi.05072-11google scholar: lookup
              47. Long JS, Mistry B, Haslam SM, Barclay WS. Host and viral determinants of influenza A virus species specificity.. Nat Rev Microbiol 2019 Jan;17(2):67-81.
                pubmed: 30487536doi: 10.1038/s41579-018-0115-zgoogle scholar: lookup
              48. Borkenhagen LK, Salman MD, Ma MJ, Gray GC. Animal influenza virus infections in humans: A commentary.. Int J Infect Dis 2019 Nov;88:113-119.
                pubmed: 31401200doi: 10.1016/j.ijid.2019.08.002google scholar: lookup
              49. Sorrell EM, Schrauwen EJ, Linster M, De Graaf M, Herfst S, Fouchier RA. Predicting 'airborne' influenza viruses: (trans-) mission impossible?. Curr Opin Virol 2011 Dec;1(6):635-42.
                pmc: PMC3311991pubmed: 22440921doi: 10.1016/j.coviro.2011.07.003google scholar: lookup

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