Detection and isolation of swine influenza a virus in spiked oral fluid and samples from individually housed, experimentally infected pigs: Potential role of porcine oral fluid in active influenza a virus surveillance in swine

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Decorte, Inge ^a   Steensels, Mieke ^b   Lambrecht, Benedicte ^b   Cay, Ann Brigitte ^a   Regge, Nick De ^a  

^a Enzootic and (Re)emerging Diseases   (Belgium)

^b Direction Viral Diseases   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BODY FLUID; CONTROLLED STUDY; DISEASE SURVEILLANCE; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); NONHUMAN; NOSE SMEAR; ORAL FLUID; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SWINE INFLUENZA VIRUS; VIRUS DETECTION; VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS STRAIN; VIRUS TITRATION; ANIMAL; CHICK EMBRYO; GENETICS; ISOLATION AND PURIFICATION; PIG; REAL TIME POLYMERASE CHAIN REACTION; SALIVA; VIROLOGY;

ANIMALS; CHICK EMBRYO; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALIVA; SWINE;

EID: 84947279354     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139586     Document Type: Article

References (55)

1. Fouchier RA, Osterhaus AD, Brown IH. Animal influenza virus surveillance. Vaccine. 2003; 21: 1754-1757.
2. Crisci E, Mussa T, Fraile L, Montoya M. Review: Influenza virus in pigs. Mol Immunol. 2013; 55: 200-211. doi: 10.1016/j.molimm.2013.02.008
3. Nelson MI, Vincent AL. Reverse zoonosis of influenza to swine: new perspectives on the human-animal interface. Trends in Microbiol. 2015. 23: 142-153.
4. Zhou NN, Senne DA, Landgraf JS, Swenson SL, Erickson G, Rossow K, et al. Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol. 1999; 73: 8851-8856.
5. Zell R, Motzke S, Krumbholz A, Wutzler P, Herwig V, Durrwald R. Novel reassortant of swine influenza H1N2 virus in Germany. J Gen Virol. 2008; 89: 271-276.
6. Starick E, Lange E, Fereidouni S, Bunzenthal C, Höveler R, Kuczka A, et al. Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J Gen Virol. 2011; 92: 1184-1188.doi: 10.1099/vir.0.028662-0
7. Liu QF, Ma JJ, Liu HX, Qi W, Anderson J, Henry SC, et al. Emergence of novel reassortant H3N2 swine influenza viruses with the 2009 pandemic H1N1 genes in the United States. Arch Virol. 2012; 157: 555-562. doi: 10.1007/s00705-011-1203-9
8. Karasin AI, Schutten MM, Cooper LA, Smith CB, Subbarao K, Anderson GA, et al. 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: 71-85.
9. Fan XH, Zhu HC, Zhou BP, Smith DK, Chen X, LAM TT, et al. Emergence and Dissemination of a Swine H3N2 Reassortant Influenza Virus with 2009 Pandemic H1N1 Genes in Pigs in China. J Virol. 2012; 86: 2375-2378. doi: 10.1128/JVI.06824-11
10. Claas ECJ, Kawaoka Y, Dejong JC, Masurel N, Webster RG. Infection of Children with Avian-Human Reassortant Influenza-Virus from Pigs in Europe. Virology. 1994; 204: 453-457.
11. Castrucci MR, Donatelli I, Sidoli L, Barigazzi G, Kawaoka Y, Webster RG. Genetic Reassortment between Avian and Human Influenza-a Viruses in Italian Pigs. Virology. 1993; 193: 503-506.
12. Marshall N, Priyamvada L, Ende Z, Steel J, Lowen AC. Influenza Virus Reassortment Occurs with High Frequency in the Absence of Segment Mismatch. PLoS pathogens. 2013; 9: e1003421. doi: 10.1371/journal.ppat.1003421
13. Welsh MD, Baird PM, Guelbenzu-Gonzalo MP, Hanna A, Reid SM, Essen S, et al. Initial incursion of pandemic (H1N1) 2009 influenza A virus into European pigs. Vet Rec. 2010; 166: 642-645. doi: 10. 1136/vr.4851
14. Vijaykrishna D, Poon LL, Zhu HC, Ma SK, Li OT, Cheung CL, et al. Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science. 2010; 328: 1529. doi: 10.1126/science.1189132
15. Song MS, Lee JH, Pascua PN, Baek YH, Kwon HI, Park KJ, et al. Evidence of human-to-swine transmission of the pandemic (H1N1) 2009 influenza virus in South Korea. J Clin Microbiol. 2010; 48: 3204-3211. doi: 10.1128/JCM.00053-10
16. Nelson MI, Vincent AL, Kitikoon P, Holmes EC, Gramer MR. Evolution of novel reassortant A/H3N2 influenza viruses in North American swine and humans, 2009-2011. J Virol. 2012; 86: 8872-8878. doi: 10.1128/JVI.00259-12
17. Moreno A, Di Trani L, Faccini S, Vaccari G, Nigrelli D, Boniotti MB, et al. Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet Microbiol. 2011; 149: 472-477. doi: 10.1016/j.vetmic.2010.12.011
18. Kitikoon P, Vincent AL, Gauger PC, Schlink SN, Bayles DO, Gramer MR, et al. Pathogenicity and transmission in pigs of the novel A(H3N2)v influenza virus isolated from humans and characterization of swine H3N2 viruses isolated in 2010-2011. J Virol. 2012; 86: 6804-6814. doi: 10.1128/JVI.00197-12
19. Ducatez MF, Hause B, Stigger-Rosser E, Darnell D, Corzo C, Juleen K, et al. Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis. 2011; 17: 1624-1629. doi: 10.3201/eid1709.110338
20. Lindstrom S, Garten R, Balish A, Shu B, Emery S, Berman L, et al. Human Infections with Novel Reassortant Influenza A(H3N2)v Viruses, United States, 2011. Emerg Infect Dis. 2012; 18: 834-837. doi: 10.3201/eid1805.111922
21. Cox CM, Neises D, Garten RJ, Bryant B, Hesse RA, Anderson GA, et al. Swine Influenza Virus A (H3N2) Infection in Human, Kansas, USA, 2009. Emerg Infect Dis. 2011; 17: 1143-1144. doi: 10.3201/eid/1706.101488
22. Wong KK, Greenbaum A, Moll ME, Lando J, Moore EL, Ganatra R, et al. Outbreak of influenza A (H3N2) variant virus infection among attendees of an agricultural fair, Pennsylvania, USA, 2011. Emerg Infect Dis. 2012; 18: 1937-1944. doi: 10.3201/eid1812.121097
23. Bowman AS, Sreevatsan S, Killian ML, Page SL, Nelson SW, Nolting JM, et al. Molecular evidence for interspecies transmission of H3N2pM/H3N2v influenza A viruses at an Ohio agricultural fair, July 2012. Emerging Microbes &Infections. 2012; 1:e33. doi: 10.1038/emi.2012.33
24. Corzo CA. Active Surveillance for Influenza A Virus among Swine, Midwestern United States, 2009-2011. Emerg Inf Dis. 2013; 19: 954-960.
25. Kyriakis CS, Brown IH, Foni E, Kuntz-Simon G, Maldonado J, Madec F, et al. Virological Surveillance and Preliminary Antigenic Characterization of Influenza Viruses in Pigs in Five European Countries from 2006 to 2008. Zoonoses Public Health. 2011; 58: 93-101. doi: 10.1111/j.1863-2378.2009.01301.
26. Mak PWY, Jayawardena S, Poon LLM. The Evolving Threat of Influenza Viruses of Animal Origin and the Challenges in Developing Appropriate Diagnostics. Clin Chem. 2012; 58: 1527-1533. doi: 10. 1373/clinchem.2012.182626
27. Janke B. Clinicopathological Features of Swine Influenza. Curr Top Microbiol Immunol. 2013; 370: 69-83. doi: 10.1007/82-2013-308
28. Detmer SE, Patnayak DP, Jiang Y, Gramer MR, Goyal SM. Detection of Influenza A virus in porcine oral fluid samples. J Vet Diag Invest. 2011; 23: 241-247.
29. Goodell CK, Prickett J, Kittawornrat A, Zhou F, Rauh R, Nelson W, et al. Probability of detecting influenza A virus subtypes H1N1 and H3N2 in individual pig nasal swabs and pen-based oral fluid specimens over time. Vet Microbiol. 2013; 166: 450-460. doi: 10.1016/j.vetmic.2013.06.029
30. Prickett J, Simer R, Christopher-Hennings J, Yoon KJ, Evans RB, Zimmerman JJ. Detection of Porcine reproductive and respiratory syndrome virus infection in porcine oral fluid samples: a longitudinal study under experimental conditions. J Veterinary Diag Invest. 2008; 20: 156-163.
31. Decorte I, Van der Stede Y, Nauwynck H, De Regge N, Cay AB. Effect of saliva stabilisers on detection of porcine reproductive and respiratory syndrome virus in oral fluid by quantitative reverse transcriptase real-time PCR. Vet J. 2013; 197: 224-228. doi: 10.1016/j.tvjl.2013.02.001
32. Webster RG, Krauss S. WHO manual on animal influenza diagnosis and surveillance. World Health Organization, Department of Communicable Disease Surveillance and Response. 2002.
33. Decorte I, Van Campe W, Mostin L, Cay AB, De Regge N. Diagnosis of the Lelystad strain of Porcine reproductive and respiratory syndrome virus infection in individually housed pigs: comparison between serum and oral fluid samples for viral nucleic acid and antibody detection. J Vet Diag Invest. 2015; 27: 47-54.
34. Detmer S, Gramer M, Goyal S, Torremorell M, Torrison J. Diagnostics and surveillance for swine influenza. Curr Top Microbiol Immunol 370: 85-112. doi: 10.1007/82-2012-220
35. Romagosa A, Gramer M, Joo HS, Torremorell M. Sensitivity of oral fluids for detecting influenza A virus in populations of vaccinated and non-vaccinated pigs. Influenza Other Respir Viruses. 2012; 6: 110-118. doi: 10.1111/j.1750-2659.2011.00276
36. Van Reeth K, Braeckmans D, Cox E, Van Borm S, van den Berg T, Goddeeris B, et al. Prior infection with an H1N1 swine influenza virus partially protects pigs against a low pathogenic H5N1 avian influenza virus. Vaccine. 2002; 27: 6330-6339.
37. Rubin BK. Physiology of airway mucus clearance. Resp Care. 2002; 47: 761.
38. Jung T, Choi C, Chae C. Localization of swine influenza virus in naturally infected pigs. Vet Pathol Online. 2002; 39: 10-16.
39. Shorter RG, Titus JL, Divertie MB. Cell turnover in the respiratory tract. CHEST J. 1964; 46: 138-142.
40. Spencer H, Shorter R. Cell turnover in pulmonary tissues. Nature. 1962; 194: 880.
41. Reeth KV, Brown I, Essen S, Pensaert M. Genetic relationships, serological cross-reaction and crossprotection between H1N2 and other influenza A virus subtypes endemic in European pigs. Virus Res. 2004; 103: 115-124.
42. Tamura SI, Tanimoto T, Kurata T. Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. Jpn J Infect Dis. 2005; 58: 195-207.
43. Lombardo T, Dotti S, Renzi S, Ferrari M. Susceptibility of different cell lines to Avian and Swine Influenza viruses. J Virol Meth. 2012; 185:82-88.
44. Chiapponi C, Zanni I, Garbarino C, Barigazzi G, Foni E. Comparison of the usefulness of the CACO-2 cell line with standard substrates for isolation of swine influenza A viruses. J Virol Meth. 2010; 163: 162-165.
45. Fábián TK, Hermann P, Beck A, Fejerdy P, Fabian G. Salivary defense proteins: their network and role in innate and acquired oral immunity. Int J Mol Sci. 2012; 13: 4295-420. doi: 10.3390/ijms13044295
46. gPotts WTW, Gwyneth Parry G. Osmotic and Ionic Regulation in Animals: International Series of Monographs. London: Pergamon Press Ltd; 1964.
47. Eaton MD, Scala AR. Reversible effect of hypotonic solutions on growth of influenza virus in tissue cultures. Proc Soc Exp Biol Med. 1956; 92:289-297.
48. Tolskaya EA, Agol VI, Voroshilova MK, Lipskaya GY. The osmotic pressure of the maintenance medium and reproduction of poliovirus. Virology. 1966; 29: 613-621.
49. Park NJ, Li Y, Yu T, Brinkman BMN, Wong DT. Characterization of RNA in saliva. Clin Chem. 2006; 52: 988-994.
50. Decorte I, Van BreedamW, Van der Stede Y, Nauwynck HJ, De Regge N, Cay AB. Detection of total and PRRSV-specific antibodies in oral fluids collected with different rope types from PRRSV-vaccinated and experimentally infected pigs. BMC Vet Res. 2014; 17: 134.
51. Olsen C, Karriker L, Wang C, Binjawadagi B, Renukaradhya G, Kittawornrat A, et al. Effect of collection material and sample processing on pig oral fluid testing results. Vet J. 2013; 198: 158-163. doi: 10. 1016/j.tvjl.2013.06.014
52. Hansen AM, Garde AH, Persson R. Measurement of salivary cortisol-effects of replacing polyester with cotton and switching antibody. Scand J Clin Lab Invest. 2008; 68: 826-829. doi: 10.1080/00365510802056207
53. Edwards JL, Nelson SW, Workman JD, Slemons RD, Szablewski CM, Nolting JM, et al. Utility of snout wipe samples for influenza A virus surveillance in exhibition swine populations. Influenza Other Respir Viruses. 2014; 8: 574-579. doi: 10.1111/irv.12270
54. Hanson BR, Schipper IA. Effects of swab materials on infectious bovine rhinotracheitis virus. Am J Vet Res. 1976; 37: 707-708.
55. Lloyd G, Baskerville A. Effects of swab materials and transport media on Aujeszky's disease virus. Res Vet Sci. 1978; 25: 257-259.