Adverse effects of Influenza A(H1N1)pdm09 virus infection on growth performance of Norwegian pigs - a longitudinal study at a boar testing station

BMC Veterinary Research

Edgar Brun³  Tore Framstad¹  Carl Andreas Grøntvedt¹  Anna Germundsson Hauge³  Hilde Forberg³  Peer Ola Hofmo²  Saraya Tavornpanich³  Bjørn Lium³  Chiek Er³ 

[1] Norwegian University of Life Sciences, Campus Adamstuen, Ullevålsveien 72, Oslo, 0454, Norway;Norsvin (Norwegian Pig Breeders Association), Hamar, 2304, Oslo, Norway;Norwegian Veterinary Institute, Oslo, 0106, Norway

关键词: Influenza A(H1N1)pdm09 virus;    Feed intake;    Pigs;    Random intercept model;    Multi-level regression analysis;    Longitudinal study;    Feed conversion efficiency;    Daily growth;    Growth performance;   

Others  :  1092004
DOI  :  10.1186/s12917-014-0284-6

 received in 2014-07-04, accepted in 2014-11-18,  发布年份 2014

【 摘 要 】

Background

Influenza A(H1N1)pdm09 virus infection in Norwegian pigs was largely subclinical. This study tested the hypothesis that the infection causes negligible impact on pigs’ growth performance in terms of feed conversion efficiency, daily feed intake, daily growth, age on reaching 100 kg bodyweight and overall feed intake. A sample of 1955 pigs originating from 43 breeding herds was classified into five infection status groups; seronegative pigs (n = 887); seropositive pigs (n = 874); pigs positive for virus at bodyweight between 33 kg and 60 kg (n = 123); pigs positive for virus at bodyweight between 61 kg and 80 kg (n = 34) and pigs positive for virus at bodyweight between 81 kg and 100 kg (n = 37). Each pig had daily recordings of feed intake and bodyweight from 33 kg to 100 kg. Marginal effects of the virus infection on the outcomes were estimated by multi-level linear regression, which accounted for known fixed effects (breed, birthdate, average daily feed intake and growth phase) and random effects (cluster effects of pig and herd).

Results

The seropositive and virus positive pigs had decreased (P value<0.05) growth performance compared to seronegative pigs even though feed intake was not decreased. Reduced feed conversion efficiency led to lower average daily growth, additional feed requirement and longer time needed to reach the 100 kg bodyweight. The effects were more marked (P value<0.03) in pigs infected at a younger age and lasted a longer period. Despite increased feed intake observed, their growth rates were lower and they took more time to reach 100 kg bodyweight compared to the seronegative pigs.

Conclusion

Our study rejected the null hypothesis that the virus infection had negligible adverse effects on growth performance of Norwegian pigs.

【 授权许可】

   
2014 Er et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Van Alstine WG: Respiratory System. In Disease of Swine. 10th edition. Edited by Zimmerman J, Karriker L, Ramirez A, Schwartz KJ. Wiley-Blackwell; 2012.
• [2]Loeffen WLA, Heinen PP, Bianchi ATJ, Hunneman WA, Verheijden JHM: Effect of maternally derived antibodies on the clinical signs and immune response in pigs after primary and secondary infection with an influenza H1N1 virus. Vet Immunol Immunopathol 2003, 92(1–2):23-35.
• [3]Khatri M, Goyal SM, Saif YM: Oct4+ stem/progenitor swine lung epithelial cells are targets for influenza virus replication. J Virol 2012, 86(12):6427-6433.
• [4]Crisci E, Mussá T, Fraile L, Montoya M: Review: influenza virus in pigs. Mol Immunol 2013, 55(3–4):200-211.
• [5]Torremorell M, Allerson M, Corzo C, Diaz A, Gramer M: Transmission of influenza a virus in pigs. Transbound Emerg Dis 2012, 59:68-84.
• [6]Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu XY, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, Fouchier RA, Pappas C, Alpuche-Aranda CM, López-Gatell H, Olivera H, López I, Myers CA, Faix D, Blair PJ, Yu C, Keene KM, et al.: Antigenic and genetic characteristics of swine-origin 2009 a(H1N1) influenza viruses circulating in humans. Science 2009, 325(5937):197-201.
• [7]Van Reeth K, Brown IH, Olsen CW: Influenza Virus. In Diseases of Swine. 10th edition. Edited by Zimmerman J, Karriker LA, Ramirez A, Schwartz K, Stevenson G. Wiley-Blackwell, ᅟ; 2012.
• [8]Brookes SM, Brown IH: A/H1N1/pdm09 virus: dynamics of infection in pigs and people. Vet Rec 2011, 169(6):151-152.
• [9]Brookes SM, Núñez A, Choudhury B, Matrosovich M, Essen SC, Clifford D, Slomka MJ, Kuntz-Simon G, Garcon F, Nash B, Hanna A, Heegaard PMH, Quéguiner S, Chiapponi C, Bublot M, Garcia JM, Gardner R, Foni E, Loeffen W, Larsen L, Van Reeth K, Banks J, Irvine RM, Brown IH: Replication, pathogenesis and transmission of pandemic (H1N1) 2009 virus in Non-immune pigs. PLoS One 2010, 5(2):e9068.
• [10]Lange E, Kalthoff D, Blohm U, Teifke JP, Breithaupt A, Maresch C, Starick E, Fereidouni S, Hoffmann B, Mettenleiter TC, Mettenleiter TC, Beer M, Vahlenkamp TW: Pathogenesis and transmission of the novel swine-origin influenza virus A/H1N1 after experimental infection of pigs. J Gen Virol 2009, 90(Pt 9):2119-2123.
• [11]Thacker EL, Thacker BJ, Janke BH: Interaction between Mycoplasma hyopneumoniae and swine influenza virus. J Clin Microbiol 2001, 39(7):2525-2530.
• [12]Lium B, Er C, Zerihun A: The Surveillance and Control Programme for Specific Virus Infections in Swine Herd in Norway 2013. In Surveillance and Control Programmes for Terrestrial and Aquatic Animals in Norway Annual Report 2012. Edited by Sviland S, Hellberg H. Norwegian Veterinary Institute, Oslo, Norway; 2014.
• [13]Grontvedt CA, Er C, Gjerset B, Hauge AG, Brun E, Jorgensen A, Lium B, Framstad T: Influenza A(H1N1)pdm09 virus infection in Norwegian swine herds 2009/10: the risk of human to swine transmission. Prev Vet Med 2013, 110(3–4):429-434.
• [14]Hofshagen M, Gjerset B, Er C, Tarpai A, Brun E, Dannevig B, Bruheim T, Fostad IG, Iversen B, Hungnes O, Lium B: Pandemic influenza A(H1N1)v: human to pig transmission in Norway? Euro Surveill 2009, 14(45):ᅟ.
• [15]Gjerset B, Er C, Lotvedt S, Jorgensen A, Hungnes O, Lium B, Germundsson A: Experiences after twenty months with pandemic influenza a (H1N1) 2009 infection in the naive Norwegian Pig population. Influenza Res Treat 2011, 2011:206975.
• [16]Grontvedt CA, Er C, Gjerset B, Germundsson A, Framstad T, Brun E, Jorgensen A, Lium B: Clinical impact of infection with pandemic influenza (H1N1) 2009 virus in naive nucleus and multiplier Pig herds in Norway. Influenza Res Treat 2011, 2011:163745.
• [17]Kitikoon P, Nilubol D, Erickson BJ, Janke BH, Hoover TC, Sornsen SA, Thacker EL: The immune response and maternal antibody interference to a heterologous H1N1 swine influenza virus infection following vaccination. Vet Immunol Immunopathol 2006, 112(3–4):117-128.
• [18]Straw BE, Shin SJ, Yeager AE: Effect of pneumonia on growth-rate and feed-efficiency of minimal disease pigs exposed to actinobacillus-pleuropneumoniae and mycoplasma-hyopneumoniae. Prev Vet Med 1990, 9(4):287-294.
• [19]Wetten M, Odegard J, Vangen O, Meuwissen TH: Simultaneous estimation of daily weight and feed intake curves for growing pigs by random regression. Animal 2012, 6(3):433-439.
• [20]Schnyder U, Hofer A, Labroue F, Kunzi N: Genetic parameters of a random regression model for daily feed intake of performance tested French landrace and large white growing pigs. Genet Sel Evol 2001, 33(6):635-658. BioMed Central Full Text
• [21]USCGf: What Happens if you Omit the Main Effect in a Regression Model With an Interaction? In 2012. http://www.ats.ucla.edu/stat/stata/faq/no_main_effect.htm.
• [22]Burnham KP, Anderson DR: Model Selection and Multi-Model Inference: A Practical Information - Theoretic Apprach. 2nd edition. Springer-Verlag, USA; 2002.
• [23]Orsini N, Bellocco R, Greenland S: EPISENS: Stata Module for Basic Sensitivity Analysis of Epidemiological Results. Statistical Software Components. 2006.
• [24]Wellenberg GJ, Bouwkamp FT, Wolf PJ, Swart WAJM, Mombarg MJ, de Gee ALW: A study on the severity and relevance of porcine circovirus type 2 infections in Dutch fattening pigs with respiratory diseases. Vet Microbiol 2010, 142(3–4):217-224.
• [25]Wesley RD, Lager KM: Overcoming maternal antibody interference by vaccination with human adenovirus 5 recombinant viruses expressing the hemagglutinin and the nucleoprotein of swine influenza virus. Vet Microbiol 2006, 118(1–2):67-75.
• [26]Markowska-Daniel I, Pomorska-Mól M, Pejsak Z: The influence of age and maternal antibodies on the postvaccinal response against swine influenza viruses in pigs. Vet Immunol Immunopathol 2011, 142(1–2):81-86.
• [27]Busquets N, Segalés J, Córdoba L, Mussá T, Crisci E, Martín-Valls GE, Simon-Grifé M, Pérez-Simó M, Pérez-Maíllo M, Núñez JI, Abad FX, Fraile L, Pina S, Majó N, Bensaid A, Domingo M, Montoya M: 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(5):74.
• [28]Snijders TAB, Bosker RJ: Multilevel Analysis: An Introduction to Basic and Advanced Multilevel Modeling. 2nd edition. Sage Publishers, London; 2012.
• [29]Dohoo IR, Martin W, Stryhn H: Veterinary Epidemiologic Research. 2nd edition. VER Inc, Charlottetown. Prince Edward Island. Canada; 2010.
• [30]Diggle P, Liang K, Zeger S: Analysis of Longitudinal Data. In Edited by Atkinson AC, Copas JB, Pierce DA, Schervish MJ, Titterington DM. Oxford: Clarendon Press; 1996:64–68.
• [31]Loving CL, Brockmeier SL, Vincent AL, Palmer MV, Sacco RE, Nicholson TL: Influenza virus coinfection with Bordetella bronchiseptica enhances bacterial colonization and host responses exacerbating pulmonary lesions. Microb Pathog 2010, 49(5):237-245.
• [32]Done SH: Environmental factors affecting the severity of pneumonia in pigs. Vet Rec 1991, 128(25):582-586.