1. bookVolume 70 (2020): Issue 1 (March 2020)
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
access type Open Access

Phylogenetic Analysis of HA and NA Genes of Swine Influenza Viruses in Serbia in 2016-2018

Published Online: 03 Apr 2020
Volume & Issue: Volume 70 (2020) - Issue 1 (March 2020)
Page range: 110 - 125
Received: 15 Nov 2019
Accepted: 18 Feb 2020
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
Abstract

Pigs are very important for the epidemiology of influenza A viruses, being commonly infected with the lineages of most adapted H1N1, H3N2, H1N2 swine subtypes. Epidemiological complexity of swine influenza is increasing by a periodic spillover of human or avian viruses in the pig population when genetic shifts can occur. The objectives of this research were to determine the presence of the influenza A virus in nasal and tracheobronchial swabs and lung tissue samples of ill and dead pigs on commercial farms, to determine circulating subtypes and characterize them through the phylogenetic analysis of hemagglutinin (HA) and neuraminidase (NA) genes. A total of 255 samples collected from 13 farms were analyzed by means of real-time RTPCR. The genome of influenza A virus was detected in 24 samples, which represented a 61.5% prevalence at the farms level (influenza A virus was confirmed in 8 out of 13 farms included in this study). Based on HA and NA gene sequences of 8 viruses, the circulation of H1N1 and H3N2 subtypes of influenza A viruses were determined. In addition, one farm exhibited a time separated circulation of H1N1 and H3N2 virus subtypes. Using Influenza Research Database, our viruses of the H1 subtype were classified into 1C.2.1 and 1A.3.3.2. clade. Based on the nucleotide sequences of HA genes, three viruses of the H1N1 subtype belong to the H1N1pdm09 lineage, and the other four to Eurasian “avian-like” H1avN1 lineage; while based on NA genes sequences, these seven viruses belong to Eurasian “avian-like” H1avN1 lineage. Both HA and NA genes of the virus of the H3N2 subtype belonged to the A/swine/ Gent/1/1984-like H3N2 lineage.

Keywords

1. Ducatez FM, Pelletier C, Meyer G: Influenza D virus in cattle, 2011-2014. Emerg Infect Dis 2015, 21(2): 368-371.10.3201/eid2102.141449Search in Google Scholar

2. Chiapponi C, Faccini S, De Mattia A, Baioni L, Barbieri I, Rosignoli C, Nigrelli A, Foni E. Detection of Influenza D virus among swine and cattle, Italy. Emerg Infect Dis 2016, 22(2): 342-344.10.3201/eid2202.151439Search in Google Scholar

3. Taubenberger JK, Morens DM: Influenza: The once and future pandemic. Public Health Rep Supplement 3 2010, 125: 16-26.10.1177/00333549101250S305Search in Google Scholar

4. Awada VL, Brown I, Chen H, Claes F, Dauphin G, Donis R, Culhane M, Hamilton K, Lewis N, Mumford E, Nguyen T, Parchariyanon S, Pasick J, Pavade G, Pereda A, Peiris M, Saito T, Swenson S, Van Reeth K, Webby R, Wong F, Ciacci Zanella J: Review of influenza A virus in swine worldwide: A call for increased surveillance and research. Zoonoses Public Health 2014, 61:4–17.10.1111/zph.12049Search in Google Scholar

5. Pleschka S: Overview of influenza viruses. In: Swine Influenza. New York, USA, Springer, 370:1–20.10.1007/82_2012_272Search in Google Scholar

6. Simon G, Larsen LE, Durrwald R, Foni E, Harder T, Van Reeth K, Markowska-Daniel I, Reid SM, Dan A, Maldonado J, Huovilainen A, Billinis C, Davidson I, Aguero M, Vila T, Herve S, Breum SØ, Chiapponi C, Urbaniak K, Kyriakis CS, ESNIP3 consortium, Brown IH, Loeffen W: European surveillance network for influenza in pigs: Surveillance programs, diagnostic tools and swine influenza virus subtypes identified in 14 European countries from 2010 to 2013. PLoS ONE 9(12): e115815. doi:10.1371/journal.pone.0115815.10.1371/journal.pone.0115815Search in Google Scholar

7. Brown IH: The epidemiology and evolution of infuenza viruses in pigs. Vet Microbiol 2010, 74(2000): 29-46.10.1016/S0378-1135(00)00164-4Search in Google Scholar

8. Zell R, Scholtissek C, Ludwig S: Genetics, Evolution, and the zoonotic capacity of european swine influenza viruses. In: Swine Influenza. New York, USA, Springer; 2013, 370:29–55.10.1007/82_2012_26723011571Search in Google Scholar

9. Savić B, Radanović O, Jovičić D, Nešić K, Ivanović S, Stevančević O, Cvetojević Đ, Kasagić D: Survey of infectious agents associated with porcine respiratory disease complex (PRDC) in Serbian swine herds using polymerase chain reaction (PCR) detection, Acta Vet 2015, 65 (1): 79-88.10.1515/acve-2015-0006Search in Google Scholar

10. Milicevic V, Radojicic S, Valcic M, Ivovic V, Radosavljevic V: Evidence of Aujeszky’s disease in wild boar in Serbia. BMC Vet Res 2016, 12:134.10.1186/s12917-016-0758-9492828027357597Search in Google Scholar

11. Influenza A virus of Swine. OIE Terrestrial Manual, Chapter 3.8.7.Search in Google Scholar

12. Spackman E, Senne A. Dennis SA, Myers TJ, Bulaga LL, Garber PL, Perdue LM, Lohman K, Daum TL, Suarez LD: Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J Clin Microbiol 2002, 40(9):3256–3260.10.1128/JCM.40.9.3256-3260.200213072212202562Search in Google Scholar

13. Brookes SM, Nunez A, Choudhury B, Matrosovich M, Essen SC, Clifford D, Slomka MJ, Kuntz-Simon G, Garcon F, Nash B, Hanna A, Heegaard PMH, Queguiner 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 5(2): e9068. doi:10.1371/journal.pone.0009068.10.1371/journal.pone.0009068281672120140096Search in Google Scholar

14. Kumar S, Stecher G, Tamura K: MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016, 33(7):1870–1874.10.1093/molbev/msw054821082327004904Search in Google Scholar

15. Zhang Y, Aevermann BD, Anderson TK, Burke DF, Dauphin G, Gu Z, He S, Kumar S, Larsen CN, Lee AJ, Li X, Macken C, Mahaffey C, Pickett BE, Reardon B, Smith T, Stewart L, Suloway C, Sun G, Tong L, Vincent AL, Walters B, Zaremba S, Zhao H, Zhou L, Zmasek C, Klem EB, Scheuermann RH: Influenza research database: An integrated bioinformatics resource for influenza virus research. Nucleic Acids Res 2017, 45:466–474.10.1093/nar/gkw857521061327679478Search in Google Scholar

16. Anderson TK, Macken CA, Lewis NS, Scheuermann RH, Van Reeth K, Brown IH, Swenson SL, Simon G, Saito T, Berhane Y, Ciacci-Zanella J, Pereda A, Davis CT, Donis RO, Webby RJ, Vincenta AL.2016. A phylogeny-based global nomenclature system and automated annotation tool for H1 hemagglutinin genes from swine influenza A viruses. mSphere 1(6):e00275-16. doi:10.1128/mSphere.00275-16.10.1128/mSphere.00275-16515667127981236Search in Google Scholar

17. Furuse Y, Suzuki A, Kamigaki T, Oshitani H: Evolution of the M gene of the influenza A virus in different host species: large-scale sequence analysis. Virol J 2009, 6:67.10.1186/1743-422X-6-67269478919476650Search in Google Scholar

18. Duh D, Blažič B: Single mutation in the matrix gene of seasonal influenza A viruses critically affects the performance of diagnostic molecular assay. J Virol Methods 2018, 251: 43–45.10.1016/j.jviromet.2017.10.00728993123Search in Google Scholar

19. Janke BH: Clinicopathological features of swine influenza. In: Swine Influenza. New York, USA, Springer; 2013, 370:69–83.10.1007/82_2013_30823404579Search in Google Scholar

20. Van Reeth K, Brown IH, Olsen CW: Influenza virus. In Chapter III Viral Diseases. In Swine diseases. Tenth Edition. Blackwell Publishing, United Kingdom 2012, 3:557-571.Search in Google Scholar

21. Vincent AL, Lewis N, Webby R: Global evolution of influenza A viruses in swine. In Animal Influenza, second edition. Oxford, United Kingdom, Wiley-Blackwell Publishing; 2017, 3(A):459-480.10.1002/9781118924341.ch18Search in Google Scholar

22. De Vleeschauwer A, Atanasova K, Van Borm S, Van den Berg T, Rasmussen TB, Uttenthal A, Van Reeth K: Comparative pathogenesis of an avian H5N2 and a swine H1N1 influenza virus in pigs. PLoS ONE 2009, 4(8): e6662. doi:10.1371/journal.pone.0006662.10.1371/journal.pone.0006662272272219684857Search in Google Scholar

23. Detmer S, Gramer M, Goyal S, Torremorell M: In vitro assessment of influenza A virus attachment in the upper and lower respiratory tracts of pigs. Vet Pathol 2012, 50(4):648-658.10.1177/030098581246746923169913Search in Google Scholar

24. Moreno A, Gabanelli E, Sozzi E, Lelli D, Chiapponi C, Ciccozzi M, Zehender G, Cordioli P: Different evolutionary trends of swine H1N2 influenza viruses in Italy compared to European viruses. Vet Res 2013, 44:112 http://www.veterinaryresearch.org/content/44/1/112.10.1186/1297-9716-44-112417609224289094Search in Google Scholar

25. Lewis NS, Russell CA, Langat P, Anderson TK, Berger K, Bielejec F, Burke DF, Dudas G, Fonville JM, Fouchier RAM, Kellam P, Koel BF, Lemey P, Nguyen T, Nuansrichy B, Peiris JSM, Saito T, Simon G, Skepner E, Takemae N, ESNIP3 consortium, Webby RJ, Van Reeth K, Brookes SM, Larsen L, Watson SJ, Brown IH, Vincent AL: The global antigenic diversity of swine influenza A viruses. eLife 2016;5:e12217. DOI: 10.7554/eLife.12217.10.7554/eLife.12217484638027113719Search in Google Scholar

26. Madić J, Barbić Lj, Savić V: Animal influenza outbreaks in Croatia: A short review to mark the the centenary of the 1918 influenza pandemic. Medical Sciences 2018, 45: 11-34.10.21857/yq32oh4579Search in Google Scholar

27. Pascu C, Costinar L, Herman V: Enzyme-linked immunosorbent assay detection of antibodies against swine influenza virus in western Romania. J Swine Health Prod 2012, 20(2):87–90.Search in Google Scholar

28. Shtjefni V, Kumbe I, Buonavoglia D: Serologic studies of swine influenza infection in Albania. Albanian j agric sci 2012, 2218-2020, (2012), Nr. 4/Vol. 11© Agricultural University of TiranaSearch in Google Scholar

29. Watson SJ, Langat P, Reid SM, Tsan-Yuk Lam T, Cotten M, Kelly M, Van Reeth K, Qiu Y, Simon G, Bonin E, Foni E, Chiapponi C, Larsen L, Hjulsager C, Markowska-Daniel I, Urbaniak K, Dürrwald R, Schlegel M, Huovilainen A, Davidson I, Dán A, Loeffen W, Edwards S, Bublot M, Vila T, Maldonado J, Valls L, ESNIP3 Consortium, Brown IH, Pybus OG, Kellama P: Molecular epidemiology and evolution of influenza viruses circulating within European swine between 2009 and 2013. J Virol 2015, 89 (19): 9920-9931.10.1128/JVI.00840-15457789726202246Search in Google Scholar

30. Galiano M, Agapow PM, Thompson C, Platt S, Underwood A, Ellis J, Myers R, Green J, Zambon M: Evolutionary pathways of the pandemic influenza A (H1N1) 2009 in the UK. PLoS ONE 2011, 6(8): e23779. doi:10.1371/journal.pone.002377910.1371/journal.pone.0023779316108221887318Search in Google Scholar

31. Sriwilaijaroen N, Suzuki Y: Molecular basis of the structure and function of H1 hemagglutinin of influenza virus. Proc Jpn Acad 2012, B 88: 226-249.10.2183/pjab.88.226341014122728439Search in Google Scholar

32. Ward CW, Dopheide TA: Amino acid sequence and oligosaccharide distribution of the haemagglutinin from an early Hong Kong influenza virus variant A/Aichi/2/68 (X-3 1). Biochem J 1981, 193:953-962.10.1042/bj193095311626907305969Search in Google Scholar

33. Cauldwell AV, Long JS, Moncorge´ O, Barclay WS: Viral determinants of influenza A virus host range. J Gen Virol 2014, 95: 1193–1210.10.1099/vir.0.062836-024584475Search in Google Scholar

34. Soundararajan V, Tharakaraman K, Raman, Raguram S, Shriver Z, Sasisekharan V, Sasisekharan R: Extrapolating from sequence—the 2009 H1N1 ‘swine’ influenza virus. Nat Biotechnol 2009, 27: 510-513.10.1038/nbt0609-51019513050Search in Google Scholar

35. Lycett SJ, Baillie G, Coulter E, Bhatt S, Kellam P, McCauley JW, Wood JLN, Brown IH, Pybus OG, Leigh Brown AJ for the Combating Swine Influenza Initiative (COSI) Consortium: Estimating reassortment rates in co-circulating Eurasian swine influenza viruses. J Gen Virol 2012, 93: 2326–2336.10.1099/vir.0.044503-0354212822971819Search in Google Scholar

36. Qi X, Pan Y, Qin Y, Zu R, Tang F, Zhou M, Wang H, Song Y: Molecular characterization of avian-like H1N1 swine influenza A viruses isolated in Eastern China, 2011. Virol Sin 2012, 27 (5):292-298.10.1007/s12250-012-3262-9821814523055004Search in Google Scholar

37. Kang HM, Lee EK, Song BM, Jeong J, Kim HR, Choi EJ, Shin YK, Lee HS, Lee YJ: Genetic and pathogenic characteristics of H1 avian and swine Influenza A viruses. J Gen Virol 2014, 95: 2118–2126.10.1099/vir.0.065524-024973238Search in Google Scholar

38. Rajao DS, Vincent AL, Perez DR: Adaptation of human influenza viruses to swine. Front Vet Sci 2019, 5(347):1-12.10.3389/fvets.2018.00347634977930723723Search in Google Scholar

39. Starick E, Lange E, Fereidouni S, Bunzentha C, Hoveler R, Kuczka A, Grosse Beilage E, Hamann HP, Klingelhofer 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.0.028662-021307227Search in Google Scholar

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