Probability of detecting influenza A virus subtypes H1N1 and H3N2 in individual pig nasal swabs and pen-based oral fluid specimens over time

Veterinary Microbiology

Volumn 166, Issue 3-4, 2013, Pages 450-460

  Goodell, Christa K ^a   Prickett, John ^a   Kittawornrat, Apisit ^a   Zhou, Fanghong ^a   Rauh, Rolf ^c   Nelson, William ^c   O'Connell, Cate ^d   Burrell, Angela ^d   Wang, Chong ^a,b   Yoon, Kyoung Jin ^a   Zimmerman, Jeffrey J ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Iowa State University   (United States)

^c TETRACORE INC   (United States)

^d Life Technologies Corporation   (United States)

Author keywords

Influenza A virus; Nasal swabs; Oral fluids; PCR; Swine; Virus isolation

Indexed keywords

CIRCOVIRUS VACCINE; CIRCUMVENT; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VIRUS VACCINE;

ANIMAL CELL; ANTIGEN DETECTION; ARTICLE; BODY FLUID; CIRCOVIRIDAE INFECTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; INFLUENZA A; INFLUENZA VACCINATION; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; NONHUMAN; NOSE SMEAR; ORAL FLUID; PIGLET; POINT OF CARE TESTING; PROBABILITY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VACCINATION; VIRUS DETECTION; VIRUS ISOLATION;

INFLUENZA A VIRUS; MYCOPLASMA HYOPNEUMONIAE; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE;

INFLUENZA A VIRUS; NASAL SWABS; ORAL FLUIDS; PCR; SWINE; VIRUS ISOLATION;

ANIMALS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; MOUTH; NOSE; PROBABILITY; SWINE; SWINE DISEASES; TIME FACTORS;

EID: 84883266246     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2013.06.029     Document Type: Article

References (56)

1. Ali A., Khatri M., Wang L., Saif Y.M., Lee C.W. Identification of swine H1N2/pandemic H1N1 reassortant influenza virus in pigs, United States. Vet. Microbiol. 2012, 158:60-68.
2. Al Johani S.M., Al Balawi M., Al Alwan B., Al Hefdhi R., Hajeer A. Validity of two rapid point of care influenza tests and direct fluorescence assay in comparison of real time PCR for swine of origin Influenza virus. J. Infect. Public Health 2011, 4:7-11.
3. Allerson M., Deen J., Detmer S.E., Gramer M.R., Soo Joo H., Romagosa A., Torremorell M. The impact of maternally derived immunity on influenza A virus transmission in neonatal pig populations. Vaccine 2013, 31:500-505.
4. Babin S.M., Hsieh Y.H., Rothman R.E., Gaydos C.A. A meta-analysis of point-of-care laboratory tests in the diagnosis of novel 2009 swine-lineage pandemic influenza A (H1N1). Diagn. Microbiol. Infect. Dis. 2011, 69:410-418.
5. Bikour M.H., Cornaglia E., Elazhary Y. Evaluation of a protective immunity induced by an inactivated influenza H3N2 vaccine after an intratracheal challenge of pigs. Can. J. Vet. Res. 1996, 60:312-314.
6. Boesenberg K. Procedure for AIV MultiS-Screen ELISA. Doc 9.1330. Quality Systems, Veterinary Diagnostic Laboratory 2012, Iowa State University, Ames, Iowa.
7. Bos M.E., Nielen M., Koch G., Stegeman A., De Jong M.C. Effect of H7N1 vaccination on highly pathogenic avian influenza H7N7 virus transmission in turkeys. Vaccine 2008, 26:6322-6328.
8. Bowman A.S., Nelson S.W., Edwards J.L., Hofer C.C., Nolting J.M., Davis I.C., Slemons R.D. Comparative effectiveness of isolation techniques for contemporary Influenza A virus strains circulating in exhibition swine. J. Vet. Diagn. Invest. 2013, 25:82-90.
9. Chartrand C., Leeflang M.M., Minion J., Brewer T., Pai M. Accuracy of rapid influenza diagnostic tests: a meta-analysis. Ann. Intern. Med. 2012, 156:500-511.
10. 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. Infect. Genet. Evol. 2013, 13:331-338.
11. Cheng P.K., Wong K.K., Mak G.C., Wong A.H., Ng A.Y., Chow S.Y., Lam R.K., Lau C.S., Ng K.C., Lim W. Performance of laboratory diagnostics for the detection of influenza A(H1N1)v virus as correlated with the time after symptom onset and viral load. J. Clin. Virol. 2010, 47:182-185.
12. Cheng S.M., Vainionpaa R., Zhao P., Li F., Hu A., Forrest B., Rappaport R. Detection of influenza B in clinical specimens: comparison of high throughput RT-PCR and culture confirmation. Virus Res. 2004, 103:85-90.
13. Ciacci-Zanella J.R., Vincent A.L., Prickett J.R., Zimmerman S.M., Zimmerman J.J. Detection of anti-influenza A nucleoprotein antibodies in pigs using a commercial influenza epitope-blocking enzyme-linked immunosorbent assay developed for avian species. J. Vet. Diagn. Invest. 2010, 22:3-9.
14. Detmer S.E., Patnayak D.P., Jiang Y., Gramer M.R., Goyal S.M. Detection of Influenza A virus in porcine oral fluid samples. J. Vet. Diagn. Invest. 2011, 23:241-247.
15. Eshelman R. Procedure for Ambion AgPath-ID Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) Real-time PCR. Doc ID: [9.496] v3. Quality Systems, Veterinary Diagnostic Laboratory, Iowa State University 2010.
16. Eshelman R. Procedure for Kingfisher96 or 24 MagMAX Viral RNA Extraction. Doc ID: [9. 459]. Quality Systems, Veterinary Diagnostic Laboratory, Iowa State University 2010.
17. Fuenzalida L., Blanco S., Prat C., Vivancos M., Dominguez M.J., Mòdol J.M., Rodrigo C., Ausina V. Utility of the rapid antigen detection BinaxNOW Influenza A&B test for detection of novel influenza A (H1N1) virus. Clin. Microbiol. Infect. 2010, 16:1574-1576.
18. Flynn K.J., Belz G.T., Altman J.D., Ahmed R., Woodland D.L., Doherty P.C. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 1998, 8:683-691.
19. Ganzenmueller T., Kluba J., Hilfrich B., Puppe W., Verhagen W., Heim A., Schulz T., Henke-Gendo C. Comparison of the performance of direct fluorescent antibody staining, a point-of-care rapid antigen test and virus isolation with that of RT-PCR for the detection of novel 2009 influenza A (H1N1) virus in respiratory specimens. J. Med. Microbiol. 2010, 59:713-717.
20. Gao F., Loring C., Laviolette M., Bolton D., Daly E.R., Bean C. Detection of 2009 pandemic influenza A(H1N1) virus Infection in different age groups by using rapid influenza diagnostic tests. Influenza Other Respi. Viruses 2012, 6:e30-e34.
21. Garten R.J., Davis C.T., Russell C.A., Shu B., Lindstrom S., Balish A., Sessions W.M., Xu X., Skepner E., Deyde V., Okomo-Adhiambo M., Gubareva L., Barnes J., Smith C.B., Emery S.L., Hillman M.J., Rivailler P., Smagala J., de Graaf M., Burke D.F., Fouchier R.A., Pappas C., Alpuche-Aranda C.M., López-Gatell H., Olivera H., López I., Myers C.A., Faix D., Blair P.J., Yu C., Keene K.M., Dotson P.D., Boxrud D., Sambol A.R., Abid S.H., St George K., Bannerman T., Moore A.L., Stringer D.J., Blevins P., Demmler-Harrison G.J., Ginsberg M., Kriner P., Waterman S., Smole S., Guevara H.F., Belongia E.A., Clark P.A., Beatrice S.T., Donis R., Katz J., Finelli L., Bridges C.B., Shaw M., Jernigan D.B., Uyeki T.M., Smith D.J., Klimov A.I., Cox N.J. Antigenic and genetic characteristics of swine-origin 2009 A (H1N1) influenza viruses circulating in humans. Science 2009, 325:197-201.
22. Gimeno C., Bravo D., Ocete D., Tormo N., Navalpotro D., Costa E., de Lomas J.G., Navarro D. Comparison of BinaxNOW Influenza A&B assay and real-time reverse transcription polymerase chain reaction for diagnosis of influenza A pandemic (H1N1) 2009 virus infection in adult patients. Diagn. Microbiol. Infect. Dis. 2010, 68:456-458.
23. Hurt A.C., Baas C., Deng Y.M., Roberts S., Kelso A., Barr I.G. Performance of influenza rapid point-of-care tests in the detection of swine lineage A(H1N1) influenza viruses. Influenza Other Respi. Viruses 2009, 3:171-176.
24. Jones F.R., Gabitzsch E.S., Xu Y., Balint J.P., Borisevich V., Smith J., Smith J., Peng B.H., Walker A., Salazar M., Paessler S. Prevention of influenza virus shedding and protection from lethal H1N1 challenge using a consensus 2009 H1N1 HA and NA adenovirus vector vaccine. Vaccine 2011, 29:7020-7026.
25. Kitikoon P., Nilubol D., Erickson B.J., Janke B.H., Hoover T.C., Sornsen S.A., Thacker E.L. The immune response and maternal antibody interference to a heterologous H1N1 swine influenza virus infection following vaccination. Vet. Immunol. Immunopathol. 2006, 112:117-128.
26. Kittawornrat A., Prickett J., Chittick W., Wang C., Engle M., Johnson J., Patnayak D., Schwartz T., Whitney D., Olsen C., Schwartz K., Zimmerman J. Porcine reproductive and respiratory syndrome virus (PRRSV) in serum and oral fluid samples from individual boars: will oral fluid replace serum for PRRSV surveillance?. Virus Res. 2010, 154:170-176.
27. Kittawornrat A., Zimmerman J. Toward a better understanding of pig behavior and pig welfare. Anim. Health Res. Rev. 2011, 12:25-32.
28. Kyriakis C.S., Gramer M.R., Barbé F., Van Doorsselaere J., Van Reeth K. Efficacy of commercial swine influenza vaccines against challenge with a recent European H1N1 field isolate. Vet. Microbiol. 2010, 144:67-74.
29. Larsen D.L., Karasin A., Zuckermann F., Olsen C.W. Systemic and mucosal immune responses to H1N1 influenza virus infection in pigs. Vet. Microbiol. 2000, 74:117-131.
30. Levandowski R.A., Gerrity T.R., Garrard C.S. Modifications of lung clearance mechanisms by acute influenza A infection. J. Lab. Clin. Med. 1985, 106:428-432.
31. Liao R.S., Landt O., Hill J.T. Comparison of a laboratory-developed RT-PCR and the CDC RT-PCR protocol with rapid immunodiagnostic testing during the 2009 H1N1 influenza A pandemic. Diagn. Microbiol. Infect. Dis. 2011, 70:236-239.
32. Liao R.S., Tomalty L.L., Majury A., Zoutman D.E. Comparison of viral isolation and multiplex real-time reverse transcription-PCR for confirmation of respiratory syncytial virus and influenza virus detection by antigen immunoassays. J. Clin. Microbiol. 2009, 47:527-532.
33. Loeffen W.L., Heinen P.P., Bianchi A.T., Hunneman W.A., Verheijden J.H. 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, 92:23-35.
34. Nguyen H.H., Moldoveanu Z., Novak M.J., van Ginkel F.W., Ban E., Kiyono H., McGhee J.R., Mestecky J. Heterosubtypic immunity to lethal influenza A virus infection is associated with virus-specific CD8(+) cytotoxic T lymphocyte responses induced in mucosa-associated tissues. Virology 1999, 254:50-60.
35. Paillot R., Prowse L., Montesso F., Huang C.M., Barnes H., Escala J. Whole inactivated equine influenza vaccine: efficacy against a representative clade 2 equine influenza virus. IFNgamma synthesis and duration of humoral immunity. Vet. Microbiol. 2013, 162:396-407.
36. Panyasing Y., Goodell C.K., Wang C., Kittawornrat A., Prickett J.R., Schwartz K.J., Ballagi A., Lizano S., Zimmerman J.J. Detection of influenza A virus nucleoprotein antibodies in oral fluid specimens from pigs infected under experimental conditions using a blocking ELISA. Transbound. Emerg. Dis. 2012, 10.1111/tbed.12019.
37. Pregliasco F., Mensi C., Camorali L., Anselmi G. Comparison of RT-PCR with other diagnostic assays for rapid detection of influenza viruses. J. Med. Virol. 1998, 56:168-173.
38. Prickett J., Simer R., Christopher-Hennings J., Yoon K.J., Evans R.B., Zimmerman J.J. Detection of Porcine reproductive and respiratory syndrome virus infection in porcine oral fluid samples: a longitudinal study under experimental conditions. J. Vet. Diagn. Invest. 2008, 20:156-163.
39. Prickett J., Simer R., Yoon K.J., Kim W.I., Zimmerman J.J. Oral-fluid samples for surveillance of commercial growing pigs for porcine reproductive and respiratory syndrome virus and porcine circovirus type 2 infections. J. Swin. Health Prod. 2008, 16:86-91.
40. Prickett J.R., Zimmerman J.J. The development of oral fluid-based diagnostics and applications in veterinary medicine. Anim. Health Res. Rev. 2010, 11:207-216.
41. Ramirez A., Wang C., Prickett J.R., Pogranichniy R., Yoon K.J., Main R., Johnson J.K., Rademacher C., Hoogland M., Hoffmann P., Kurtz A., Kurtz E., Zimmerman J. Efficient surveillance of pig populations using oral fluids. Prev. Vet. Med. 2012, 104:292-300.
42. Richt J.A., Lager K.M., Clouser D.F., Spackman E., Suarez D.L., Yoon K.J. Real-time reverse transcription-polymerase chain reaction assays for the detection and differentiation of North American swine influenza viruses. J. Vet. Diagn. Invest. 2004, 16:367-373.
43. Romagosa A., Allerson M., Gramer M., Joo H.S., Deen J., Detmer S., Torremorell M. Vaccination of influenza a virus decreases transmission rates in pigs. Vet. Res. 2011, 42:120.
44. Romagosa A., Gramer M., Joo H.S., Torremorell M. Sensitivity of oral fluids for detecting influenza A virus in populations of vaccinated and non-vaccinated pigs. Influenza Other Respi. Viruses 2012, 6:110-118.
45. Starick E., Lange E., Grund C., Grosse Beilage E., Döhring S., Maas A., Noé T., Beer M., Harder T.C. Reassortants of pandemic influenza A virus H1N1/2009 and endemic porcine HxN2 viruses emerge in swine populations in Germany. J. Gen. Virol. 2012, 93:1658-1663.
46. Swenson S.L., Vincent L.L., Lute B.M., Janke B.H., Lechtenberg K.E., Landgraf J.G., Schmitt B.J., Kinker D.R., McMillen J.K. A comparison of diagnostic assays for the detection of type A swine influenza virus from nasal swabs and lungs. J. Vet. Diagn. Invest. 2001, 13:36-42.
47. Takada A., Matsushita S., Ninomiya A., Kawaoka Y., Kida H. Intranasal immunization with formalin-inactivated virus vaccine induces a broad spectrum of heterosubtypic immunity against influenza A virus infection in mice. Vaccine 2003, 21:3212-3218.
48. Torremorell M., Allerson M., Corzo C., Diaz A., Gramer M. Transmission of Influenza A Virus in Pigs. Transbound. Emerg. Dis. 2012, 10.1111/j.1865-1682.2011.01300.x.
49. USDA July, 2010. Influenza surveillance in swine - procedures manual. (accesssed 12.12.12). http://www.aphis.usda.gov/animal_health/animal_dis_spec/swine/downloads/influenza_surv_swine_proc_manual.pdf.
50. Van Reeth K., Brown I., Essen S., Pensaert M. Genetic relationships, serological cross-reaction and cross-protection between H1N2 and other influenza A virus subtypes endemic in European pigs. Virus. Res. 2004, 103:115-124.
51. Van Reeth K., Brown I.A., Olsen C.W. Ch 40 influenza virus. Diseases of Swine 2012, 557-572. John Wiley & Sons Inc, Ames, IA. 10th ed. J.J. Zimmerman, L. Karriker, A. Ramirez, K. Schwartz, G. Stevenson (Eds.).
52. Vincent A.L., Swenson S.L., Lager K.M., Gauger P.C., Loiacono C., Zhang Y. Characterization of an influenza A virus isolated from pigs during an outbreak of respiratory disease in swine and people during a county fair in the United States. Vet. Microbiol. 2009, 137:51-59.
53. Vincent A.L., Ciacci-Zanella J.R., Lorusso A., Gauger P.C., Zanella E.L., Kehrli M.E., Janke B.H., Lager K.M. Efficacy of inactivated swine influenza virus vaccines against the 2009 A/H1N1 influenza virus in pigs. Vaccine 2010, 28:2782-2787.
54. Webster R.G., Askonas B.A. Cross-protection and cross-reactive cytotoxic T cells induced by influenza virus vaccines in mice. Eur. J. Immunol. 1980, 10:396-401.
55. World Health Organization, 2009. CDC protocol of realtimeRT-PCR for swine influenza A(H1N1). (accessed 12.12.12). http://www.who.int/csr/resources/publications/swineflu/realtimeptpcr/en/index.html.
56. World Health Organization Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. Wkly. Epidemiol. Rec. 2011, 86:469-480.