Comparative analysis of influenza A(H3N2) virus hemagglutinin specific IgG subclass and IgA responses in children and adults after influenza vaccination

Vaccine

Volumn 35, Issue 1, 2017, Pages 191-198

  Manenti, Alessandro ^a   Tete, Sarah M ^b,c   Mohn, Kristin G I ^b   Jul Larsen, Åsne ^b,c   Gianchecchi, Elena ^d   Montomoli, Emanuele ^a,d   Brokstad, Karl A ^b   Cox, Rebecca J ^b,c  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY OF BERGEN   (Norway)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^d VisMederi Srl   (Italy)

Author keywords

Antibody response; IgA; IgG subclass; Influenza; LAIV3; Live attenuated influenza vaccine

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN A1; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; INACTIVATED VACCINE; LIVE VACCINE; VIRUS ANTIBODY;

ADOLESCENT; ADULT; AGE; ANTIBODY RESPONSE; ARTICLE; CHILD; CLINICAL ARTICLE; CLINICAL TRIAL; COMPARATIVE STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMAGGLUTINATION INHIBITION; HUMAN; HUMAN EXPERIMENT; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFLUENZA A VIRUS (H3N2); INFLUENZA VACCINATION; MALE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; ANTIBODY AFFINITY; ANTIBODY PRODUCTION; BLOOD; HEMAGGLUTINATION INHIBITION TEST; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; INTRANASAL DRUG ADMINISTRATION; MIDDLE AGED; PRESCHOOL CHILD; YOUNG ADULT;

ADMINISTRATION, INTRANASAL; ADOLESCENT; ADULT; AGE FACTORS; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; ANTIBODY FORMATION; CHILD; CHILD, PRESCHOOL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA VACCINES; INJECTIONS, INTRAMUSCULAR; MALE; MIDDLE AGED; VACCINES, ATTENUATED; VACCINES, INACTIVATED; YOUNG ADULT;

EID: 84999884998     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2016.10.024     Document Type: Article

References (40)

1. [1] Meyer, A.G., Wilke, C.O., Geometric constraints dominate the antigenic evolution of influenza H3N2 hemagglutinin. PLoS Pathog, 11(5), 2015, e1004940.
2. [2] Ramakrishnan, A., Althoff, K.N., Lopez, J.A., Coles, C.L., Bream, J.H., Differential serum cytokine responses to inactivated and live attenuated seasonal influenza vaccines. Cytokine 60:3 (2012), 661–666.
3. [3] Organization WH. Influenza (seasonal) factsheet 211; 2014. Available from: http://www.who.int/mediacentre/factsheets/fs211/en/.
4. [4] Goodwin, K., Viboud, C., Simonsen, L., Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine, 24(8), 2006, 1159.
5. [5] Ohmit, S.E., Thompson, M.G., Petrie, J.G., Thaker, S.N., Jackson, M.L., Belongia, E.A., et al. Influenza vaccine effectiveness in the 2011–2012 season: protection against each circulating virus and the effect of prior vaccination on estimates. Clin Infect Dis 58:3 (2014), 319–327.
6. [6] Frasca, D., Diaz, A., Romero, M., Mendez, N.V., Landin, A.M., Blomberg, B.B., Effects of age on H1N1-specific serum IgG1 and IgG3 levels evaluated during the 2011–2012 influenza vaccine season. Immun Ageing, 10(1), 2013, 14.
7. [7] Katz, J.M., Hancock, K., Xu, X.Y., Serologic assays for influenza surveillance, diagnosis and vaccine evaluation. Expert Rev Anti-Infect 9:6 (2011), 669–683.
8. [8] Schild, G.C., Pereira, M.S., Chakraverty, P., Single-radial-haemolysis: a new method for the assay of antibody to influenza haemagglutinin: applications for diagnosis and seroepidemiologic surveillance of influenza. Bull World Health Organ, 52(1), 1975, 1.
9. [9] Trombetta, C.M., Perini, D., Vitale, L., Cox, R.J., Stanzani, V., Piccirella, S., et al. Validation of Single Radial Haemolysis assay: a reliable method to measure antibodies against influenza viruses. J Immunol Methods 422:July (2015), 95–101.
10. [10] 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 25:20 (2007), 4056–4063.
11. [11] Clements, M.L., Betts, R.F., Tierney, E.L., Murphy, B.R., Serum and nasal wash antibodies associated with resistance to experimental challenge with influenza A wild-type virus. J Clin Microbiol 24:1 (1986 Jul), 157–160.
12. [12] Crum-Cianflone, N.F., Collins, G., Defang, G., Iverson, E., Eberly, L.E., Duplessis, C., et al. Immunoglobulin G subclass levels and antibody responses to the 2009 influenza A (H1N1) monovalent vaccine among human immunodeficiency virus (HIV)-infected and HIV-uninfected adults. Clin Exp Immunol 168:1 (2012), 135–141.
13. [13] Schroeder, H.W. Jr., Cavacini, L., Structure and function of immunoglobulins. J Allergy Clin Immunol 125:2 (2010), S41–S52 [Suppl. 2].
14. [14] El-Madhun, A.S., Cox, R.J., Haaheim, L.R., The effect of age and natural priming on the IgG and IgA subclass responses after parenteral influenza vaccination. J Infect Dis, 180(4), 1999, 1356.
15. [15] Tamura, S.-i., Kurata, T., Defense mechanisms against influenza virus infection in the respiratory tract mucosa. Jpn J Infect Dis, 57(6), 2004, 236.
16. [16] Madhun, A.S., Akselsen, P.E., Sjursen, H., Pedersen, G., Svindland, S., Nostbakken, J.K., et al. An adjuvanted pandemic influenza H1N1 vaccine provides early and long term protection in health care workers. Vaccine 29:2 (2010), 266–273.
17. [17] Pedersen, G.K., Hoschler, K., Oie Solbak, S.M., Bredholt, G., Pathirana, R.D., Afsar, A., et al. Serum IgG titres, but not avidity, correlates with neutralizing antibody response after H5N1 vaccination. Vaccine 32:35 (2014), 4550–4557.
18. [18] Grohskopf, L.A., Olsen, S.J., Sokolow, L.Z., Bresee, J.S., Cox, N.J., Broder, K.R., et al. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP)-United States, 2014–15 influenza season. Am J Transplant 14:12 (2014), 2906–2913.
19. [19] Clements, M.L., O'Donnell, S., Levine, M.M., Chanock, R.M., Murphy, B.R., Dose response of A/Alaska/6/77 (H3N2) cold-adapted reassortant vaccine virus in adult volunteers: role of local antibody in resistance to infection with vaccine virus. Infect Immun 40:3 (1983), 1044–1051.
20. [20] Clements, M.L., Murphy, B.R., Development and persistence of local and systemic antibody responses in adults given live attenuated or inactivated influenza A virus vaccine. J Clin Microbiol 23:1 (1986), 66–72.
21. [21] Edwards, M.J., Dimmock, N.J., A haemagglutinin (HA1)-specific FAb neutralizes influenza A virus by inhibiting fusion activity. J Gen Virol 82:June (2001), 1387–1395.
22. [22] Skehel, J.J., Wiley, D.C., Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69 (2000), 531–569.
23. [23] Stepanova, L., Naykhin, A., Kolmskog, C., Jonson, G., Barantceva, I., Bichurina, M., et al. The humoral response to live and inactivated influenza vaccines administered alone and in combination to young adults and elderly. J Clin Virol 24:3 (2002), 193–201.
24. [24] Frasca, D., Blomberg, B.B., Aging affects human B cell responses. J Clin Immunol 31:3 (2011), 430–435.
25. [25] Ashkenazi, S., Vertruyen, A., Aristegui, J., Esposito, S., McKeith, D.D., Klemola, T., et al. Superior relative efficacy of live attenuated influenza vaccine compared with inactivated influenza vaccine in young children with recurrent respiratory tract infections. Pediatr Infect Dis J 25:10 (2006), 870–879.
26. [26] Fleming, D.M., Crovari, P., Wahn, U., Klemola, T., Schlesinger, Y., Langussis, A., et al. Comparison of the efficacy and safety of live attenuated cold-adapted influenza vaccine, trivalent, with trivalent inactivated influenza virus vaccine in children and adolescents with asthma. Pediatr Infect Dis J 25:10 (2006), 860–869.
27. [27] Treanor, J.J., Kotloff, K., Betts, R.F., Belshe, R., Newman, F., Iacuzio, D., et al. Evaluation of trivalent, live, cold-adapted (CAIV-T) and inactivated (TIV) influenza vaccines in prevention of virus infection and illness following challenge of adults with wild-type influenza A (H1N1), A (H3N2), and B viruses. Vaccine 18:9–10 (1999), 899–906.
28. [28] Powell, T.J., Strutt, T., Reome, J., Hollenbaugh, J.A., Roberts, A.D., Woodland, D.L., et al. Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J Immunol 178:2 (2007), 1030–1038.
29. [29] Cheng, X., Zengel, J.R., Suguitan, A.L. Jr., Xu, Q., Wang, W., Lin, J., et al. Evaluation of the humoral and cellular immune responses elicited by the live attenuated and inactivated influenza vaccines and their roles in heterologous protection in ferrets. J Infect Dis 208:4 (2013), 594–602.
30. [30] Ambrose, C.S., Wu, X., Jones, T., Mallory, R.M., The role of nasal IgA in children vaccinated with live attenuated influenza vaccine. Vaccine 30:48 (2012), 6794–6801.
31. [31] Belshe, R.B., Gruber, W.C., Mendelman, P.M., Cho, I., Reisinger, K., Block, S.L., et al. Efficacy of vaccination with live attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine against a variant (A/Sydney) not contained in the vaccine. J Pediatr 136:2 (2000), 168–175.
32. [32] Block, S.L., Yogev, R., Hayden, F.G., Ambrose, C.S., Zeng, W., Walker, R.E., Shedding and immunogenicity of live attenuated influenza vaccine virus in subjects 5–49 years of age. Vaccine 26:38 (2008), 4940–4946.
33. [33] Brokstad, K.A., Cox, R.J., Olofsson, J., Jonsson, R., Haaheim, L.R.B.K.A., Parenteral influenza vaccination induces a rapid systemic and local immune response. J Infect Dis, 171, 1995, 198.
34. [34] el-Madhun, A.S., Cox, R.J., Soreide, A., Olofsson, J., Haaheim, L.R., Systemic and mucosal immune responses in young children and adults after parenteral influenza vaccination. J Infect Dis, 178(4), 1998, 933.
35. [35] Boyce, T.G., Hsu, H.H., Sannella, E.C., Coleman-Dockery, S.D., Baylis, E., Zhu, Y., et al. Safety and immunogenicity of adjuvanted and unadjuvanted subunit influenza vaccines administered intranasally to healthy adults. Vaccine 19:2–3 (2000), 217–226.
36. [36] Barria, M.I., Garrido, J.L., Stein, C., Scher, E., Ge, Y., Engel, S.M., et al. Localized mucosal response to intranasal live attenuated influenza vaccine in adults. J Infect Dis 207:1 (2013), 115–124.
37. [37] Johnson, P.R., Feldman, S., Thompson, J.M., Mahoney, J.D., Wright, P.F., Immunity to influenza A virus infection in young children: a comparison of natural infection, live cold-adapted vaccine, and inactivated vaccine. J Infect Dis 154:1 (1986), 121–127.
38. [38] Mohn, K.G., Bredholt, G., Brokstad, K.A., Pathirana, R.D., Aarstad, H.J., Tondel, C., et al. Longevity of B-cell and T-cell responses after live attenuated influenza vaccination in children. J Infect Dis, 25(November), 2014.
39. [39] Goldblatt, D., Vaz, A.R., Miller, E., Antibody avidity as a surrogate marker of successful priming by Haemophilus influenzae type b conjugate vaccines following infant immunization. J Infect Dis 177:4 (1998 Apr), 1112–1115.
40. [40] Eidem, S., Tete, S.M., Jul-Larsen, A., Hoschler, K., Montomoli, E., Brokstad, K.A., et al. Persistence and avidity maturation of antibodies to A(H1N1)pdm09 in healthcare workers following repeated annual vaccinations. Vaccine 33:33 (2015), 4146–4154.