Discordant correlation between serological assays observed when measuring heterosubtypic responses against avian influenza H5 and H7 viruses in unexposed individuals

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Molesti, Eleonora ^a   Ferrara, Francesca ^a   Lapini, Giulia ^b   Montomoli, Emanuele ^b   Temperton, Nigel ^a  

^a MEDWAY SCHOOL OF PHARMACY   (United Kingdom)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; AVIAN INFLUENZA; AVIAN INFLUENZA H5 VIRUS; AVIAN INFLUENZA H7 VIRUS; AVIAN INFLUENZA VIRUS; BLOOD SAMPLING; COMPLEMENT HEMOLYSIS TEST; HEMAGGLUTINATION INHIBITION; HUMAN; HUMORAL IMMUNITY; INFLUENZA VIRUS A H5N1; ITALY; MAJOR CLINICAL STUDY; SENSITIVITY ANALYSIS; SEROLOGY; VIRUS NEUTRALIZATION; ANIMAL; BIRD; BLOOD; IMMUNOLOGY; INFLUENZA; INFLUENZA IN BIRDS; INFLUENZA VIRUS A H1N1; ISOLATION AND PURIFICATION; PATHOGENICITY; VIROLOGY;

VIRUS ANTIBODY;

ANIMALS; ANTIBODIES, VIRAL; BIRDS; HUMANS; IMMUNITY, HUMORAL; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN;

EID: 84903648013     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/231365     Document Type: Article

References (51)

1. Cox N. J., Brammer T. L., Regnery H. L., Influenza: global surveillance for epidemic and pandemic variants. European Journal of Epidemiology 1994 10 4 467 470 2-s2.0-0028037244 10.1007/BF01719678 (Pubitemid 24339217)
2. Veguilla V., Hancock K., Schiffer J., Gargiullo P., Lu X., Aranio D., Branch A., Dong L., Holiday C., Liu F., Steward-Clark E., Sun H., Tsang B., Wang D., Whaley M., Bai Y., Cronin L., Browning P., Dababneh H., Noland H., Thomas L., Foster L., Quinn C. P., Soroka S. D., Katz J. M., Sensitivity and specificity of serologic assays for detection of human infection with 2009 pandemic H1N1 virus in U.S. populations. Journal of Clinical Microbiology 2011 49 6 2210 2215 2-s2.0-79957451495 10.1128/JCM.00229-11
3. Brokstad K. A., Cox R. J., Major D., Wood J. M., Haaheim L. R., Cross-reaction but no avidity change of the serum antibody response after influenza vaccination. Vaccine 1995 13 16 1522 1528 2-s2.0-0028829535 10.1016/0264-410X(95)00095-I
4. Powers D. C., Belshe R. B., Vaccine-induced antibodies to heterologous influenza A H1N1 viruses: effects of aging and 'original antigenic sin'. Journal of Infectious Diseases 1994 169 5 1125 1129 2-s2.0-0028027082
5. Schulman J. L., Kilbourne E. D., Induction of partial specific heterotypic immunity in mice by a single infection with influenza A virus. Journal of bacteriology 1965 89 170 174 2-s2.0-78651171439
6. Yetter R. A., Barber W. H., Small P. A. Jr., Heterotypic immunity to influenza in ferrets. Infection and Immunity 1980 29 2 650 653 2-s2.0-0018945241 (Pubitemid 10040183)
7. Heinen P. P., de Boer-Luijtze E. A., Bianchi A. T., Respiratory and systemic humoral and cellular immune responses of pigs to a heterosubtypic influenza A virus infection. Journal of General Virology 2001 82 11 2697 2707 2-s2.0-0034782578 (Pubitemid 32998648)
8. Han T., Marasco W. A., Structural basis of influenza virus neutralization. Annals of the New York Academy of Sciences 2011 1217 1 178 190 2-s2.0-79251583146 10.1111/j.1749-6632.2010.05829.x
9. Ekiert D. C., Bhabha G., Elsliger M.-A., Friesen R. H. E., Jongeneelen M., Throsby M., Goudsmit J., Wilson I. A., Antibody recognition of a highly conserved influenza virus epitope. Science 2009 324 5924 246 251 2-s2.0-64849114224 10.1126/science.1171491
10. Sui J., Hwang W. C., Perez S., Wei G., Aird D., Chen L.-M., Santelli E., Stec B., Cadwell G., Ali M., Wan H., Murakami A., Yammanuru A., Han T., Cox N. J., Bankston L. A., Donis R. O., Liddington R. C., Marasco W. A., Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nature Structural and Molecular Biology 2009 16 3 265 273 2-s2.0-62049083943 10.1038/nsmb.1566
11. Corti D., Voss J., Gamblin S. J., Codoni G., Macagno A., Jarrossay D., Vachieri S. G., Pinna D., Minola A., Vanzetta F., Silacci C., Fernandez-Rodriguez B. M., Agatic G., Bianchi S., Giacchetto-Sasselli I., Calder L., Sallusto F., Collins P., Haire L. F., Temperton N., Langedijk J. P. M., Skehel J. J., Lanzavecchia A., A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011 333 6044 850 856 2-s2.0-80051670323 10.1126/science.1205669
12. Ekiert D. C., Friesen R. H. E., Bhabha G., Kwaks T., Jongeneelen M., Yu W., Ophorst C., Cox F., Korse H. J. W. M., Brandenburg B., Vogels R., Brakenhoff J. P. J., Kompier R., Koldijk M. H., Cornelissen L. A. H. M., Poon L. L. M., Peiris M., Koudstaal W., Wilson I. A., Goudsmit J., A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 2011 333 6044 843 850 2-s2.0-80051635697 10.1126/science.1204839
13. Tsuchiya E., Sugawara K., Hongo S., Matsuzaki Y., Muraki Y., Li Z.-N., Nakamura K., Antigenic structure of the haemagglutinin of human influenza A/H2N2 virus. Journal of General Virology 2001 82 10 2475 2484 2-s2.0-0034795117 (Pubitemid 32936780)
14. Garcia J.-M., Pepin S., Lagarde N., Ma E. S. K., Vogel F. R., Chan K. H., Chiu S. S. S., Peiris J. S. M., Heterosubtype neutralizing responses to influenza A (H5N1) viruses are mediated by antibodies to virus haemagglutinin. PLoS ONE 2009 4 11 2-s2.0-71049124869 10.1371/journal.pone.0007918 e7918
15. Liu X., Liu Y., Zhang Y., Chen Z., Tang Z., Xu Q., Wang Y., Zhao P., Qi Z., Pre-existing immunity with high neutralizing activity to 2009 pandemic H1N1 influenza virus in Shanghai population. PLoS ONE 2013 8 3 2-s2.0-84875101603 10.1371/journal.pone.0058810 e58810
16. Plotkin S. A., Correlates of protection induced by vaccination. Clinical and Vaccine Immunology 2010 17 7 1055 1065 2-s2.0-77954357410 10.1128/CVI.00131-10
17. Kreijtz J. H., Fouchier R. A., Rimmelzwaan G. F., Immune responses to influenza virus infection. Virus Research 2011 162 1-2 19 30 2-s2.0-81555228707 10.1016/j.virusres.2011.09.022
18. Plotkin S. A., Vaccines: correlates of vaccine-induced immunity. Clinical Infectious Diseases 2008 47 3 401 409 2-s2.0-47549116006 10.1086/589862 (Pubitemid 352009364)
19. Al-Khayatt R., Jennings R., Potter C. W., Interpretation of responses and protective levels of antibody against attenuated influenza A viruses using single radial haemolysis. Journal of Hygiene 1984 93 2 301 312 2-s2.0-0021701947 (Pubitemid 15207959)
20. Wood J. M., Montomoli E., Newman R. W., Daas A., Buchheit K.-H., Terao E., Collaborative study on influenza vaccine clinical trial serology-part 2: reproducibility study. Pharmeuropa Bio & Scientific Notes 2011 2011 1 36 54 2-s2.0-80052344794
21. Keitel W. A., Atmar R. L., Vaccines for pandemic influenza: summary of recent clinical trials. Current Topics in Microbiology and Immunology 2009 333 1 431 451 2-s2.0-73949107102 10.1007/978-3-540-92165-3-21
22. Ng S., Ip D. K. M., Fang V. J., Chan K.-H., Chiu S. S., Leung G. M., Peiris J. S. M., Cowling B. J., The effect of age and recent influenza vaccination history on the immunogenicity and efficacy of 2009-10 seasonal trivalent inactivated influenza vaccination in children. PLoS ONE 2013 8 3 2-s2.0-84874923852 10.1371/journal.pone.0059077 e59077
23. Beyer W. E. P., Palache A. M., Lüchters G., Nauta J., Osterhaus A. D., Seroprotection rate, mean fold increase, seroconversion rate: which parameter adequately expresses seroresponse to influenza vaccination? Virus Research 2004 103 1-2 125 132 2-s2.0-2442585128 10.1016/j.virusres.2004.02.024 (Pubitemid 38649071)
24. Wood J. M., Gaines-Das R. E., Taylor J., Chakraverty P., Comparison of influenza serological techniques by international collaborative study. Vaccine 1994 12 2 167 174 2-s2.0-0028044778 10.1016/0264-410X(94)90056-6 (Pubitemid 24041936)
25. Eichelberger M., Golding H., Hess M., Weir J., Subbarao K., Luke C. J., Friede M., Wood D., FDA/NIH/WHO public workshop on immune correlates of protection against influenza A viruses in support of pandemic vaccine development, Bethesda, Maryland, US, December 10-11, 2007. Vaccine 2008 26 34 4299 4303 2-s2.0-47849101644 10.1016/j.vaccine.2008.06.012
26. Krammer F., Pica N., Hai R., Margine I., Palesea P., Chimeric hemagglutinin influenza virus vaccine constructs elicit broadly protective stalk-specific antibodies. Journal of Virology 2013 87 12 6542 6550 2-s2.0-84878611784 10.1128/JVI.00641-13
27. Nicholson K. G., Colegate A. E., Podda A., Stephenson I., Wood J., Ypma E., Zambon M. C., Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomised trial of two potential vaccines against H5N1 influenza. The Lancet 2001 357 9272 1937 1943 2-s2.0-0035897889 10.1016/S0140-6736(00)05066-2 (Pubitemid 32568336)
28. Rowe T., Abernathy R. A., Hu-Primmer J., Thompson W. W., Lu X., Lim W., Fukuda K., Cox N. J., Katz J. M., Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. Journal of Clinical Microbiology 1999 37 4 937 943 2-s2.0-0033041241 (Pubitemid 29140593)
29. Stephenson I., Das R. G., Wood J. M., Katz J. M., Comparison of neutralising antibody assays for detection of antibody to influenza A/H3N2 viruses: an international collaborative study. Vaccine 2007 25 20 4056 4063 2-s2.0-34247275658 10.1016/j.vaccine.2007.02.039 (Pubitemid 46616989)
30. Alberini I., Del Tordello E., Fasolo A., Temperton N. J., Galli G., Gentile C., Montomoli E., Hilbert A. K., Banzhoff A., Del Giudice G., Donnelly J. J., Rappuoli R., Capecchi B., Pseudoparticle neutralization is a reliable assay to measure immunity and cross-reactivity to H5N1 influenza viruses. Vaccine 2009 27 43 5998 6003 2-s2.0-70349298313 10.1016/j.vaccine.2009.07.079
31. Garcia J.-M., Lagarde N., Ma E. S., de Jong M. D., Peiris J. S., Optimization and evaluation of an influenza A (H5) pseudotyped lentiviral particle-based serological assay. Journal of Clinical Virology 2010 47 1 29 33 2-s2.0-72049126376 10.1016/j.jcv.2009.10.009
32. Molesti E., Milani A., Terregino C., Cattoli G., Temperton N. J., Comparative serological assays for the study of h5 and h7 avian influenza viruses. Influenza Research and Treatment 2013 2013 9 286158 10.1155/2013/286158
33. Temperton N. J., Hoschler K., Major D., Nicolson C., Manvell R., Hien V. M., Ha D. Q., de Jong M., Zambon M., Takeuchi Y., Weiss R. A., A sensitive retroviral pseudotype assay for influenza H5N1-neutralizing antibodies. Influenza and Other Respiratory Viruses 2007 1 3 105 112 2-s2.0-47049101983 10.1111/j.1750-2659.2007.00016.x
34. Wang W., Butler E. N., Veguilla V., Vassell R., Thomas J. T., Moos M. Jr., Ye Z., Hancock K., Weiss C. D., Establishment of retroviral pseudotypes with influenza hemagglutinins from H1, H3, and H5 subtypes for sensitive and specific detection of neutralizing antibodies. Journal of Virological Methods 2008 153 2 111 119 2-s2.0-53049089447 10.1016/j.jviromet.2008.07.015
35. Hai R., Krammer F., Tan G. S., Pica N., Eggink D., Maamary J., Margine I., Albrecht R. A., Palese P., Influenza viruses expressing chimeric hemagglutinins: globular head and stalk domains derived from different subtypes. Journal of Virology 2012 86 10 5774 5781 2-s2.0-84861325359 10.1128/JVI.00137-12
36. Gentile C., Manini I., Alberini I., Piccirella S., Ansaldi F., Gasparini R., Montomoli E., Katz J., Seroepidemiology of influenza A/H5N1 virus in the Italian population from 1992 to 2007. June 2007 Toronto,Ontario, Canada 17 23
37. WHO, WHO Global Influenza Surveillance Network: Manual for the Laboratory Diagnosis and Virological Survaillance of Influenza 2011 Malta WHO Press
38. Landry N., Ward B. J., Trépanier S., Montomoli E., Le Dargis M., Lapini G., Vézina L.-P., Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PLoS ONE 2010 5 12 2-s2.0-78650981716 10.1371/journal.pone.0015559 e15559
39. Keitel W. A., Campbell J. D., Treanor J. J., Walter E. B., Patel S. M., He F., Noah D. L., Hill H., Safety and immunogenicity of an inactivated influenza A/H5N1 vaccine given with or without aluminum hydroxide to healthy adults: results of a phase I-II randomized clinical trial. Journal of Infectious Diseases 2008 198 9 1309 1316 2-s2.0-54249154153 10.1086/592172
40. European Committee for Medicinal Products for Human Use, Note for Guidance on Harmonisation of Requirements for influenza Vaccines 1997 Brussels, Belgium Industry ECoEa
41. Molesti E., Cattoli G., Ferrara F., Böttcher-Friebertshäuser E., Terregino C., Temperton N., The production and development of H7 Influenza virus pseudotypes for the study of humoral responses against avian viruses. Journal of Molecular and Genetic Medicine 2012 7 315 320
42. Sui J., Sheehan J., Hwang W. C., Bankston L. A., Burchett S. K., Huang C.-Y., Liddington R. C., Beigel J. H., Marasco W. A., Wide prevalence of heterosubtypic broadly neutralizing human anti-influenza A antibodies. Clinical Infectious Diseases 2011 52 8 1003 1009 2-s2.0-79953885168 10.1093/cid/cir121
43. Kaminski D. A., Lee F. E., Antibodies against conserved antigens provide opportunities for reform in influenza vaccine design. Frontiers in Immunology 2011 2, article 76 2-s2.0-84866309001 10.3389/fimmu.2011.00076
44. Oxford J. S., Schild G. C., Potter C. W., Jennings R., The specificity of the anti-haemagglutinin antibody response induced in man by inactivated influenza vaccines and by natural infection. Journal of Hygiene 1979 82 1 51 61 2-s2.0-0018757401 (Pubitemid 9092466)
45. Farrohi K., Farrohi F. K., Noble G. R., Kaye H. S., Kendal A. P., Evaluation of the single radial hemolysis test for measuring hemagglutinin- and neuraminidase-specific antibodies to H3N2 influenza strains and antibodies to influenza B. Journal of Clinical Microbiology 1977 5 3 353 360 2-s2.0-0017466786
46. Profeta M. L., Palladino G., Serological evidence of human infections with avian influenza viruses. Brief report. Archives of Virology 1986 90 3-4 355 360 2-s2.0-0022457134 (Pubitemid 16062326)
47. Lu B. L., Webster R. G., Hinshaw V. S., Failure to detect hemagglutination-inhibiting antibodies with intact avian influenza virions. Infection and Immunity 1982 38 2 530 535 2-s2.0-0019935856 (Pubitemid 12002668)
48. Corti D., Suguitan A. L. Jr., Pinna D., Silacci C., Fernandez-Rodriguez B. M., Vanzetta F., Santos C., Luke C. J., Torres-Velez F. J., Temperton N. J., Weiss R. A., Sallusto F., Subbarao K., Lanzavecchia A., Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. Journal of Clinical Investigation 2010 120 5 1663 1673 2-s2.0-77951876927 10.1172/JCI41902
49. Burlington D. B., Wright P. F., van Wyke K. L., Phelan M. A., Mayner R. E., Murphy B. R., Development of subtype-specific and heterosubtypic antibodies to the influenza A virus hemagglutinin after primary infection in children. Journal of Clinical Microbiology 1985 21 5 847 849 2-s2.0-0021959063 (Pubitemid 15093154)
50. Lynch G. W., Selleck P.W., Axell A.-M., Cross-reactive anti-avian H5N1 influenza neutralizing antibodies in a normal "exposure-naïve" Australian blood donor population. The Open Immunology Journal 2008 1 13 19
51. Yamashita A., Kawashita N., Kubota-Koketsu R., Inoue Y., Watanabe Y., Ibrahim M. S., Ideno S., Yunoki M., Okuno Y., Takagi T., Yasunaga T., Ikuta K., Highly conserved sequences for human neutralization epitope on hemagglutinin of influenza A viruses H3N2, H1N1 and H5N1: implication for human monoclonal antibody recognition. Biochemical and Biophysical Research Communications 2010 393 4 614 618 2-s2.0-77949491670 10.1016/j.bbrc.2010.02.031