Emergence of the pandemic H1N1 2009 influenza A virus in swine herds in Poland

Markowska-Daniel, Iwona; Urbaniak, Kinga; Porowski, Marian; Karbowiak, Paweł; Kowalczyk, Andrzej; Kozak, Edyta; Pejsak, Zygmunt

doi:10.2478/bvip-2013-0051

Abstract

The outbreaks of pandemic H1N1 influenza A virus (pdm-like H1N1 2009), detected for the first time in farrow-to-finish farms in Poland, were described. The nasal swabs and lung tissue collected from diseased/dead animals were tested using molecular techniques (RRT-PCR, MRT-PCR, RT-PCR, SSG-PCR, sequencing) and virus isolation. The amplification of the genetic material extracted from the tested samples confirmed the presence of the M1 gene sequence of type A influenza virus. Using MRT-PCRs no products characteristic for HA and NA of any swine influenza virus subtypes were obtained. Using SSGPCR, products specific for pandemic HA and NA gene fragments were detected. Six new pdm-like H1N1 2009 strains were isolated and characterised. Phylogenetic analysis of the HA and NA genes revealed that they belong to one lineage with the pandemic strain A/California/04/2009 and other human strains, including human strains isolated in Poland in 2011.

References

1. Arias C.F., Escalera-Zamudio M., Soto-Del Rio M., Cobián- Güemes A.G., Isa P., López S.: Molecular anatomy of 2009 influenza virus A (H1N1). Arch Medical Res 2009, 40, 643-654.10.1016/j.arcmed.2009.10.00720304251
Search in Google Scholar
2. Bálint A., Kiss I., Bányai K., Biksi I., Szentpáli-Gavallér K., Magyar T., Jankovics I., Rózsa M., Szalai B., Takács M., Tóth A.G., Dán A.: Emergence and characterisation of pandemic H1N1 influenza viruses in Hungarian swine herds. Acta Vet Hungarica 2013, 61, 125-134.10.1556/avet.2012.05923439297
Search in Google Scholar
3. Brookes S.M., Núnez A., Choudhury B., Matrosovich M., Essen S.C., Clifford D., Slomka M.J., Kuntz-Simon G., Garcon F., Nash B., Hanna A., Heegaard P.M.H., Queguiner S., Chiapponi C., Bublot M., Garcia J.M., Gardner R., Foni E., Loeffen W., Larsen L., Van Reeth K., Banks J., Irvine R.M., Brown I.H.: Replication, pathogenesis, and transmission of pandemic (H1N1) 2009 virus in non-immune pigs. PLoS ONE 2010, 5, 1-9.10.1371/journal.pone.0009068281672120140096
Search in Google Scholar
4. Cardinale E., Pascalis H., Temmam S., Hervé S., Saulnier A., Turpin M., Barbier N., Hoarau J., Quéguiner S., Gorin S., Foray C., Roger M., Porphyre V., André P., Thomas T., de Lamballerie X., Dellagi K., Simon G.: Influenza A(H1N1)pdm09 virus in pigs, Réunion Island. Emerg Infect Dis 2012, 18, 1665-1668.10.3201/eid1810.120398347162923017204
Search in Google Scholar
5. Chen Y., Zhang J., Qiao C., Yang H., Zhang Y., Xin X., Chen H.: Co-circulation of pandemic 2009 H1N1, classical swine H1N1 and avian-like swine H1N1 influenza viruses in pigs in China. Infect Genet Evol 2013, 13, 331-338.10.1016/j.meegid.2012.09.02123146831
Search in Google Scholar
6. Chiapponi C., Moreno A., Barbieri I., Merenda M., Foni E.: Multiplex RT-PCR assay for differentiating European swine influenza virus subtypes H1N1, H1N2, and H3N2. J Virol Methods 2012, 184, 117-120.10.1016/j.jviromet.2012.05.02022664185
Search in Google Scholar
7. Deng Y.M., Iannello P., Smith I., Watson J., Barr I.G., Daniels P., Komadina N., Harrower B., Wong F.J.K.: Transmission of influenza A(H1N1) 2009 pandemic viruses in Australian swine. Influenza Other Resp Viruses 2012, 6, 42-47.10.1111/j.1750-2659.2012.00337.x494167822336333
Search in Google Scholar
8. Ducatez M.F., Sonnberg S., Hall R.J., Peacey M., Ralston J., Webby R.J., Huang O.S.: Genotyping assay for the identification of 2009-2010 pandemic and seasonal H1N1 influenza virus reassortants. J Virol Methods 2010, 168, 78-81.10.1016/j.jviromet.2010.04.020291011920435067
Search in Google Scholar
9. Grøntvedt C.A., Er C., Gjerset B., Germundsson A., Framstad T., Brun E., Jørgensen 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, 1-7.10.1155/2011/206975344730223074654
Search in Google Scholar
10. Guercio A., Purpari G., Conaldi P.G.: Pandemic influenza A/H1N1 virus in a swine farm house in Sicily, Italy. J Environ Biol 2012, 33, 155-157.
Search in Google Scholar
11. Hiromoto Y., Parchariyanon S., Ketusing N., Netrabukkana P., Hayashi T., Kobayashi T., Takemae N., Saito T.: Isolation of the pandemic (H1N1) 2009 virus and its reassortant with an H3N2 swine influenza virus from healthy weaning pigs in Thailand in 2011. Virus Res 2012, 169, 175-181.10.1016/j.virusres.2012.07.02522906589
Search in Google Scholar
12. Holyoake P.K., Kirkland P.D., Davis R.J., Arzey K.E., Watson J., Lunt R.A., Wang J., Wong F., Moloney B.J., Dunn S.E.: The first identified case of pandemic H1N1 influenza in pigs in Australia. Aust Vet J 2011, 89, 427-431.10.1111/j.1751-0813.2011.00844.x22008120
Search in Google Scholar
13. Howden K.J., Brockhoff E.J., Caya F.D., McLeod L.J., Lavoie M., Ing J.D., Bystrom J.M., Alexandersen S., Pasick J.M., Berhane Y., Morrison M.E., Keenliside J.M., Laurendeau S., Rohonczy E.B.: An investigation into human pandemic influenza virus (H1N1) 2009 on an Alberta swine farm. Can Vet J 2009, 50, 1153-1161.
Search in Google Scholar
14. Kim S.H., Moon O.K., Lee K.K., Song Y.K., Yeo C.I., Bae C.W., Yoon H., Lee O.S., Lee J.H., Park C.K.: Outbreak of pandemic influenza (H1N1) 2009 in pigs in Korea. Vet Rec 2011, 169, 155-158.10.1136/vr.c746421610000
Search in Google Scholar
15. Kyriakis C., Olsen C.W., Carman S., Brown I.H., Brookes S.M., Van Doorsselaere J., Van Reeth K.: Serological cross-reactivity with pandemic (H1N1) 2009 virus in pigs, Europe. Emerging Infect Dis 2010, 16, 96-99.10.3201/eid1601.091190287438120031049
Search in Google Scholar
16. Lange E., Kalthoff D., Blohm U., Teifke J.P., Breithaupt A., Maresch C., Starick E., Fereidouni S., Hoffmann B., Mettenleiter T.C., Beer M., Vahlenkamp T.W.: Pathogenesis and transmission of the novel swine-origin influenza virus A/H1N1 after experimental infection of pigs. J Gen Virol 2009, 90, 2119-2123.10.1099/vir.0.014480-019592456
Search in Google Scholar
17. Markowska-Daniel I., Pejsak Z.: The sero-prevalence of influenza virus amongst pigs and wild boars in Poland. Med Weter 1999, 55, 302-305.
Search in Google Scholar
18. Matsuu A., Uchida Y., Takemae N., Mawatari T., Yoneyama S.K., Kasai T., Nakamura R., Eto M., Saito T.: Genetic characterization of swine influenza viruses isolated in Japan between 2009 and 2012. Microbiol Immunol 2012, 56, 792-803.10.1111/j.1348-0421.2012.00501.x22924526
Search in Google Scholar
19. Moreno A., Di Trani L., Alborali L., Vaccari G., Barbieri I., Falcone E., Sozzi E., Puzelli S., Ferri G., Cordioli P.: First pandemic H1N1 outbreak from a pig farm in Italy. Open Virol J 2010, 4, 52-56.10.2174/1874357901004010052290577220648221
Search in Google Scholar
20. Moreno A., Di Trani L., Faccvini S., Vaccari G., Nigrelli D., Boniotti M.B., Falcone E., Boni A., Chiapponi C., Sozzi E.: Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet Microbiol 2011, 149, 472-477.10.1016/j.vetmic.2010.12.01121208754
Search in Google Scholar
21. Nfon C.K., Berhane Y., Hisanaga T., Zhang S., Handel K., Kehler H., Labrecque O., Lewis N.S., Vincent A.L., Copps J., Alexandersen S., Pasick J.: Characterization of H1N1 swine influenza viruses circulating in Canadian pigs in 2009. J Virol 2011, 85, 8667-8679.10.1128/JVI.00801-11316578821697484
Search in Google Scholar
22. Njabo K.Y., Fuller T.L., Chasar A., Pollinger J.P., Cattoli G., Terregino C., Monne I., Reynes J.M., Njouom R., Smith T.B.: Pandemic A/H1N1/2009 influenza virus in swine, Cameroon, 2010. Vet Microbiol 2012, 156, 189-192.10.1016/j.vetmic.2011.09.003325163821963416
Search in Google Scholar
23. Pasma T., Joseph T.: Pandemic (H1N1) 2009 infection in swine herds, Manitoba, Canada. Emerg Infect Dis 2010, 16, 706-708.10.3201/eid1604.091636332196820350394
Search in Google Scholar
24. Pereda A., Cappuccio J., Quiroga M.A., Baumeister E., Insarralde L., Ibar M., Sanguinetti R., Cannilla M.L., Franzese D., Escobar Cabrera O.E., Craig M.I., Rimondi A., Machuca M., Debenedetti R.T., Zenobi C., Barral L., Balzano R., Capalbo S., Risso A., Perfumo C.J.: Pandemic (H1N1) 2009 outbreak on pig farm, Argentina. Emerg Infect Dis 2010, 16, 304-307.10.3201/eid1602.091230295802220113566
Search in Google Scholar
25. Pereda A., Rimondi A., Cappuccio J., Sanguinetti R., Angel M., Ye J., Sutton T., Diba´rbora M., Olivera V., Craig M.I., Quiroga M.A., Machuca M., Ferrero A., Perfumo C., Perez D.R.: Evidence of reassortment of pandemic H1N1 influenza virus in swine in Argentina: are we facing the expansion of potential epicenters of influenza emergence? Influenza Other Resp Viruses, 2011, 5, 409-412.10.1111/j.1750-2659.2011.00246.x317531821668680
Search in Google Scholar
26. Poon L.L.M., Mak P.W.Y., Li O.T.W., Chan K.H., Cheung C.L., Ma E.S., Yen H.L., Vijaykrishna D., Guan Y., Peiris J.S.M.: Rapid detection of reassortment of pandemic H1N1/2009 influenza virus. Clin Chem 2010, 56, 1340-1344.10.1373/clinchem.2010.149179295641020567024
Search in Google Scholar
27. Schaefer R., Zanella J.R.C., Brentano L., Vincent A.L., Ritterbusch G.A., Silveira S., Caron L., Mores N.: Isolation and characterization of a pandemic H1N1 influenza virus in pigs in Brazil. Pesq Vet Bras 2011, 31, 761-767.10.1590/S0100-736X2011000900007
Search in Google Scholar
28. Slomka M.J., Densham A.L., Coward V.J., Essen S., Brookes S.M., Irvine R.M., Spackman E., Ridgeon J., Gardner R., Hanna A., Suarez D.L., Brown I.H.: Real time reverse transcription (RRT)-polymerase chain reaction (PCR) methods for detection of pandemic (H1N1) 2009 influenza virus and European swine influenza A virus infections in pigs. Influenza Other Resp Viruses 2010, 4, 277-293.10.1111/j.1750-2659.2010.00149.x463465020716157
Search in Google Scholar
29. Song M.S., Lee J.H, Pascua P.N.Q, Baek Y.H., Kwon H., Park K.J., Choi H.W., Shin Y.K., Song J.Y., Kim C.J., Choi J.K.: Evidence of human-to-swine transmission of the pandemic (H1N1) 2009 influenza virus in South Korea. J Clin Microbiol 2010, 48, 3204-3211.10.1128/JCM.00053-10293772220610681
Search in Google Scholar
30. Sreta D., Tantawet S., Ayudhya S., Thontiravong A., Wongphatcharachai M., Lapkuntod J., Bunpapong N., Tuanudom R., Suradhat S., Vimolket L., Poovorawan Y., Thanawongnuwech R., Amonsin A., Kitikoon P.: Pandemic (H1N1) 2009 virus on commercial swine farm, Thailand. Emerg Infect Dis 2010, 16, 1587-1590.10.3201/eid1610.100665329828920875285
Search in Google Scholar
31. Starick E., Lange E., Fereidouni S., Bunzenthal C., Höveler R., Kuczka A., Grosse Beilage A., Hamann H.P., Klingelhöfer I., Steinhauer D., Vahlenkamp T., Beer M., Harder T.: Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J Gen Virol 2011, 92, 1184-1188.10.1099/vir.0.028662-021307227
Search in Google Scholar
32. Tang J.W., Tambyah P.A., Wilder-Smith A., Puong K.Y., Shaw R., Barr I.G., Chan K.P.: Cross-reactive antibodies to pandemic (H1N1)2009 virus, Singapore. Emerg Infect Dis 2010, 16, 874-876.10.3201/eid1605.091678295400420409391
Search in Google Scholar
33. Tremblay D., Allard V., Doyon J.F., Bellehumeur C., Spearman J.G., Harel J., Gagnon C.A.: Emergence of a new swine H3N2 and pandemic (H1N1) 2009 influenza A virus reassortant in two Canadian animal populations, mink and swine. J Clin Microbiol 2011, 49, 4386-4390.10.1128/JCM.05676-11323293222012020
Search in Google Scholar
34. Trevennec K., Leger L., Lyazrhi F., Baudon E., Cheung C.Y., Roger F., Peiris M., Garcia J.M.: Transmission of pandemic influenza H1N1 (2009) in Vietnamese swine in 2009-2010. Influenza Other Resp Viruses 2012, 6, 348-357.10.1111/j.1750-2659.2011.00324.x332863722212737
Search in Google Scholar
35. Vijaykrishna D., Poon L.L.M., Zhu H.C., Ma S.K., Li O.T.W., Cheung C.L., Smith G.J.D., Peiris J.S.M., Guan Y.: Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 2010, 328, 1529.10.1126/science.1189132356984720558710
Search in Google Scholar
36. Weingartl H.M., Berhane Y., Hisanaga T., Neufeld J., Kehler H., Emburry-Hyatt C., Hooper-McGreevy K., Kasloff S., Dalman B., Bystrom J., Alexandersen S., Li Y., Pasick J.: Genetic and pathobiologic characterization of pandemic H1N1 2009 influenza viruses from a naturally infected swine herd. J Virol 2010, 84, 2245-2256.10.1128/JVI.02118-09282090420015998
Search in Google Scholar
37. Welsh M.D., Baird P.M., Guelbenzu-Gonzalo M.P., Hanna A., Reid S.M., Essen S., Russell C., Thomas S., Barrass L., McNeilly F., McKillen J., Todd D., Harkin V., McDowell S., Choudhury B., Irvine R. M., Borobia J., Grant J., Brown I.H.: Initial incursion of pandemic (H1N1) 2009 influenza A virus into European pigs. Vet Rec 2010, 166, 642-645.10.1136/vr.485120495164
Search in Google Scholar
38. Williamson S.M., Tucker A.W., McCrone I.S., Bidewell C.A., Brons N., Habernoll H., Essen S.C., Brown I.H., COSI, Wood J.L.N.: Descriptive clinical and epidemiological characteristics of influenza A H1N1 2009 virus infections in pigs in England. Vet Rec 2012, 171, 271-277.10.1136/vr.10067322865115
Search in Google Scholar
39. www.oie.int
Search in Google Scholar
40. www.promedmail.org
Search in Google Scholar
41. Yan J.H., Xiong Y., Yi C.H., Sun X.X., He Q.S., Fu W., Xu X.K., Jiang J.X., Ma L., Liu Q.: Pandemic (H1N1) 2009 virus circulating in pigs, Guangxi, China. Emerg Infect Dis 2012, 18, 357-358. 10.3201/eid1802.111346331046422305479
Search in Google Scholar

Emergence of the pandemic H1N1 2009 influenza A virus in swine herds in Poland

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