, Volume 30, Issue 3, pp 433–440 | Cite as

Clinical evaluation, serological response and lesions generated by the A/Mexico/La Gloria-3/2009/H1N1 and A/swine/New Jersey/11/1976/H1N1 influenza viruses in colostrated and non-colostrated pigs

  • Mireya Juárez-Ramírez
  • Iván Sánchez-BetancourtEmail author
  • María Elena Trujillo-Ortega
  • Susana Mendoza-Elvira
  • Rosalba Carreón-Nápoles
  • Benjamín Fuente-Martínez
  • Francisco J. Trigo-TaveraEmail author
Original Article


Influenza A viruses cause respiratory disease in piglets, and maternal immunity plays an important role in protecting against Influenza virus infection. Nevertheless, in the presence of high levels of maternal antibodies against influenza, an adequate immune response is not developed. In this study, the effect of maternal antibodies against the swine influenza A/swine/New Jersey/11/1976/H1N1 virus (swH1N1) on clinical presentation, serological response, and lesions produced in colostrated and non-colostrated pigs was evaluated in pigs infected with the human influenza A/Mexico/La Gloria-3/2009/ H1N1 (pH1N1) and swH1N1 viruses. Our results indicated that between 2 and 4 days post-challenge, sneezing and mild nasal discharge were observed in all pigs. Body temperature in pigs from all treatment groups ranged between 39.2 and 39.3 °C. Pigs inoculated with the pH1N1 virus (421 g) exhibited a significantly lower daily weight gain than those inoculated with the swH1N1 virus (524 g). HI antibody titers against the pH1N1 virus were significantly different between colostrated (1.62) and non-colostrated (0.43) pigs. Significant differences in antibody titers were detected between pigs inoculated with the pH1N1 (1.28) or the swH1N1 virus (0.77) (P < 0.05). The highest percentage of pulmonary lesions was observed in non-colostrated/pH1N1 pigs (11.88%) at 6 days post-challenge. Cross reactivity was observed between the pH1N1 and swH1N1 viruses, as the maternal antibodies against the swH1N1 virus successfully neutralized the pH1N1 virus infection.


Influenza virus Pandemic virus Swine virus H1N1 



The authors express their gratitude to the staff of the Pathology Department and of the Department of Swine Medicine and Management, of the School of Veterinary Medicine and Animal Science, National Autonomous University of Mexico.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest regarding the publication of this study.

Supplementary material

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Supplementary material 1 (PPTX 53 kb)
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Supplementary material 2 (DOCX 21 kb)


  1. 1.
    Olsen CW, Brown IH, Easterday BC, Reeth KV. Swine Influenza. In: Straw BE, Zimmerman JJ, D’Allaire S, Taylor DJ, editors. Diseases of swine. 9th ed. Ames, Iowa: Blackwell Publishing. 2006. pp 469–482.Google Scholar
  2. 2.
    Karasin AI, Schutten MM, Cooper LA, Smith CB, Subbarao K, Anderson GA, Carman S, Olsen CW. Genetic characterization of H3N2 influenza viruses isolated from pigs in North America, 1977-1999: evidence for wholly human and reassortant virus genotypes. Virus Res. 2000;68(1):71–85.CrossRefGoogle Scholar
  3. 3.
    Zhou NN, Senne DA, Landgraf JS, Swenson SL, Erickson G, Rossow K, Liu L, Yoon KJ, Krauss S, Webster RG. Emergence of H3N2 reassortant influenza A viruses in North American pigs. Vet Microbiol. 2000;74(1–2):47–58.CrossRefGoogle Scholar
  4. 4.
    Kitikoon P, Nilubol D, Erickson BJ, Janke BH, Hoover TC, Sornsen SA, Thacker EL. The immune response and maternal antibody interference toa heterologous H1N1 swine influenza virus infection following vaccination. Vet ImmunolImmunopathol. 2006;112(3–4):117–28.CrossRefGoogle Scholar
  5. 5.
    Grebe KM, Yewdell JW, Bennink JR. Heterosubtypic immunity to influenza A virus: where do we stand? Microbes Infect. 2008;10(9):1024–9.CrossRefGoogle Scholar
  6. 6.
    Kyriakis CS, Olsen CW, Carman S, Brown IH, Brookes SM, Doorsselaere JV, et al. Serologic cross-reactivity with pandemic (H1N1) 2009 virus in pigs, Europe. Emerg Infect Dis. 2010;16:96–9.CrossRefGoogle Scholar
  7. 7.
    Howden KJ, Brockhoff EJ, Caya FD, McLeod LJ, Lavoie M, Ing JD, et al. An investigation into human pandemic influenza virus (H1N1) 2009 on an Alberta swine farm. Can Vet J. 2009;50:1153–61.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Pasma T, Joseph T. Pandemic (H1N1) 2009 infection in swine herds, Manitoba, Canada. Emerg Infect Dis. 2010;16:706–8.CrossRefGoogle Scholar
  9. 9.
    Pereda A, Cappuccio J, Quiroga MA, Baumeister E, Insarralde L, Ibar M, et al. Pandemic (H1N1) 2009 Outbreak on pig farm, Argentina. Emerg Infect Dis. 2010;16:304–7.CrossRefGoogle Scholar
  10. 10.
    Ramírez MH, Carreón NR, Mercado GC, Rodríguez TJ. Hemoaglutinación e inhibición de la hemoaglutinación del paramixovirus porcino a través de la modificación de algunas variables que participan en la prueba. Vet Mex. 1996;27(3):257–9.Google Scholar
  11. 11.
    Bollen AJP, Hansen KA, Rasmussen JH. The laboratory swine. Florida: CRC Press LLC; 2000.Google Scholar
  12. 12.
    Sorensen V, Jorsal SE, Mousing J. Diseases of the respiratory system. In: Straw BE, Zimmerman JJ, D’Allaire S, Taylor DJ, editors. Diseases of swine. 9th ed. Ames, Iowa: Blackwell Publishing; 2006. pp. 149–178.Google Scholar
  13. 13.
    Hair JF, Anderson RE, Tatham RL, Black WC. Multivariate data analysis. 4th ed. New Jersey: Prentice Hall; 1995.Google Scholar
  14. 14.
    Brookes SM, Núñez A, Choudhury B, Matrosovich M, Essen SC, et al. Replication, Pathogenesis an Transmission of Pandemic (H1N1) 2009 Virus in Non-Immune Pigs. PLoS ONE. 2009;5(2):e9068. Scholar
  15. 15.
    Lange E, Kalthoff D, Blohm U, Teifke JP, Breithaupt A, Maresch C, et al. Pathogenesis and transmission of the novel swine-origin influenza virus A/H1N1 after experimental infection of pigs. J Gen Virol. 2009;90(Pt9):2119–23.CrossRefGoogle Scholar
  16. 16.
    Busquets N, Segalés J, Córdoba L, Mussá T, Crisci E, Martin-Valls GE, et al. Experimental infection with H1N1 European swine influenza virus protects pigs from an infection with the 2009 pandemic H1N1 human influenza virus. Vet Res. 2010;41:74.CrossRefGoogle Scholar
  17. 17.
    Vincent AL, Larger KM, Ma W, Lekcharoensuk P, Gramer MR, Loiacono C, et al. Evaluation of hemagglutinin subtype 1 swine influenza viruses from the USA. Vet Microbiol. 2006;118:212–22.CrossRefGoogle Scholar
  18. 18.
    Van Reeth K, Nauwynck H. Proinflammatory cytokines and viral respiratory disease in pigs. Vet Res. 2000;31(2):187–213.CrossRefGoogle Scholar
  19. 19.
    Long BC, Goldberg TL, Swenson SL, Erickson G, Scherba G. Adaptation and limitations of established hemagglutination inhibition assays for the detection of porcine anti-swine influenza virus H1N2 antibodies. J Vet Diagn Invest. 2004;16(4):264–70.CrossRefGoogle Scholar
  20. 20.
    Leuwerke B, Kitikoon P, Evans R, Thacker E. Comparison of three serological assays to determine the cross-reactivity of antibodies from eight genetically diverse USA swine influenza virus. J Vet Diagn Invest. 2008;20:426–32.CrossRefGoogle Scholar
  21. 21.
    Perera RA, Riley S, Ma SK, Zhu HC, Guan Y, Peiris JS. Seroconversion to pandemic (H1N1) 2009 virus and cross-reactive immunity to other swine influenza viruses. Emerg Infect Dis. 2011;17:1897–9.CrossRefGoogle Scholar
  22. 22.
    Itoh Y, Shinya K, Kiso M, Watanabe T, Sakoda Y, Hatta M, et al. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature. 2009;460:1021–5.CrossRefGoogle Scholar
  23. 23.
    Munster VJ, de Wit E, van den Brand JM, Herfst S, Schrauwen EJ, Bestebroer TM, et al. Pathogenesis and transmission of swine-origin 2009 A (H1N1) influenza virus in ferrets. Science. 2009;325:481–3.CrossRefGoogle Scholar
  24. 24.
    Rowe T, León AJ, Crevar CJ, Carter DM, Xu L, Ran L, et al. Modeling host responses in ferrets during A/California/07/2009 influenza infection. Virology. 2010;401:257–65.CrossRefGoogle Scholar

Copyright information

© Indian Virological Society 2019

Authors and Affiliations

  1. 1.Department of Pathology, School of Veterinary Medicine and Animal ScienceNational Autonomous University of MexicoMexico CityMexico
  2. 2.Department of Swine Medicine and Management, School of Veterinary Medicine and Animal ScienceNational Autonomous University of MexicoMexico CityMexico
  3. 3.Laboratory of Virology and Microbiology of Swine Respiratory Diseases. Multidisciplinary Research Unit. Cuautitlán Campus 1National Autonomous University of MexicoMexico CityMexico
  4. 4.Teaching, Research, and Extension Center in Avian Production (C.E.I.E.P.Av.), School of Veterinary Medicine and Animal ScienceNational Autonomous University of MexicoMexico CityMexico

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