Seasonal influenza vaccination of children induces humoral and cell-mediated immunity beyond the current season: Cross-reactivity with past and future strains

Journal of Infectious Diseases

Volumn 214, Issue 10, 2016, Pages 1477-1486

  Reber, Adrian J ^a   Kim, Jin Hyang ^a   Coleman, Laura A ^b   Spencer, Sarah M ^a   Chung, Jessie R ^a   Chen, Jufu ^a   Gargiullo, Paul ^a   Sundaram, Maria E ^b   Belongia, Edward A ^b   Shay, David K ^a   Katz, Jacqueline M ^a   Sambhara, Suryaprakash ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b MARSHFIELD CLINIC   (United States)

Author keywords

B cell; children; cross reactivity; hemagglutination inhibition; immune response; influenza; T cell; vaccine

Indexed keywords

INFLUENZA VACCINE; TUMOR NECROSIS FACTOR; INACTIVATED VACCINE; VIRUS ANTIBODY;

2009 H1N1 INFLUENZA; ADOLESCENT; ARTICLE; CD4+ T LYMPHOCYTE; CD69+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS REACTION; FEMALE; HEMAGGLUTINATION INHIBITION; HUMAN; HUMORAL IMMUNITY; INFECTION PREVENTION; INFLUENZA A VIRUS (A/PERTH/16/2009(H3N2)); INFLUENZA A VIRUS (H3N2); INFLUENZA VACCINATION; MALE; MEMORY CELL; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SEASONAL INFLUENZA; T LYMPHOCYTE; VIRUS STRAIN; BLOOD; HEMAGGLUTINATION INHIBITION TEST; IMMUNOLOGY; INFLUENZA, HUMAN; ORTHOMYXOVIRIDAE; TIME FACTOR;

ADOLESCENT; ANTIBODIES, VIRAL; CHILD; CROSS REACTIONS; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; INFLUENZA VACCINES; INFLUENZA, HUMAN; MALE; ORTHOMYXOVIRIDAE; T-LYMPHOCYTES; TIME FACTORS; VACCINES, INACTIVATED;

EID: 85006482331     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiw380     Document Type: Article

References (37)

1. Taubenberger JK, Morens DM. Influenza: the once and future pandemic. Public Health Rep 2010; 125(suppl 3):16-26.
2. Carrat F, Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine 2007; 25:6852-62.
3. Flannery B, Clippard J, Zimmerman RK, et al. Early estimates of seasonal influenza vaccine effectiveness-United States, January 2015. MMWR Morb Mortal Wkly Rep 2015; 64:10-5.
4. Smith DJ, Lapedes AS, de Jong JC, et al. Mapping the antigenic and genetic evolution of influenza virus. Science 2004; 305:371-6.
5. Fonville JM, Wilks SH, James SL, et al. Antibody landscapes after influenza virus infection or vaccination. Science 2014; 346:996-1000.
6. Shuler CM, Iwamoto M, Bridges CB, et al. Vaccine effectiveness against medically attended, laboratory-confirmed influenza among children aged 6 to 59 months, 2003-2004. Pediatrics 2007; 119:e587-95.
7. Ohmit SE, Victor JC, Rotthoff JR, et al. Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. N Engl J Med 2006; 355:2513-22.
8. Fiore AE, Shay DK, Broder K, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2008. MMWR Recomm Rep 2008; 57:1-60.
9. McIntyre AF, Gonzalez-Feliciano AG, Bryan LN, et al. Seasonal influenza vaccination coverage-United States, 2009-10 and 2010-11. MMWR Surveill Summ 2013; 62(suppl 3):65-8.
10. Hancock K, Veguilla V, Lu X, et al. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med 2009; 361:1945-52.
11. Reber AJ, Kim JH, Biber R, et al. Preexisting immunity, more than aging, influences influenza vaccine responses. Open Forum Infect Dis 2015; doi:10.1093/ofid/ofv052.
12. Potter CW, Oxford JS. Determinants of immunity to influenza infection in man. Br Med Bull 1979; 35:69-75.
13. Hobson D, Curry RL, Beare AS, Ward-Gardner A. The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J Hyg (Lond) 1972; 70:767-77.
14. Ng S, Fang VJ, Ip DK, et al. Estimation of the association between antibody titers and protection against confirmed influenza virus infection in children. J Infect Dis 2013; 208:1320-4.
15. Black S, Nicolay U, Vesikari T, et al. Hemagglutination inhibition antibody titers as a correlate of protection for inactivated influenza vaccines in children. Pediatr Infect Dis J 2011; 30:1081-5.
16. Richards KA, Topham D, Chaves FA, Sant AJ. Cutting edge: CD4 T cells generated from encounter with seasonal influenza viruses and vaccines have broad protein specificity and can directly recognize naturally generated epitopes derived from the live pandemic H1N1 virus. J Immunol 2010; 185:4998-5002.
17. Nayak JL, Fitzgerald TF, Richards KA, Yang H, Treanor JJ, Sant AJ. CD4+ T-cell expansion predicts neutralizing antibody responses to monovalent, inactivated 2009 pandemic influenza A(H1N1) virus subtype H1N1 vaccine. J Infect Dis 2013; 207:297-305.
18. Li GM, Chiu C, Wrammert J, et al. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci U S A 2012; 109:9047-52.
19. Wrammert J, Smith K, Miller J, et al. Rapid cloning of high-Affinity human monoclonal antibodies against influenza virus. Nature 2008; 453:667-71.
20. Forrest BD, PrideMW, Dunning AJ, et al. Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children. Clin Vaccine Immunol 2008; 15:1042-53.
21. Ferguson M, Risi G, Davis M, et al. Safety and long-Term humoral immune response in adults after vaccination with an H1N1 2009 pandemic influenza vaccine with or without AS03 adjuvant. J Infect Dis 2012; 205:733-44.
22. Song JY, Cheong HJ, Seo YB, et al. Comparison of the long-Term immunogenicity of two pandemic influenza A/H1N1 2009 vaccines, the MF59-Adjuvanted and unadjuvanted vaccines, in adults. Clin Vaccine Immunol 2012; 19:638-41.
23. Kruetzmann S, Rosado MM, Weber H, et al. Human immunoglobulin M memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen. J Exp Med 2003; 197:939-45.
24. Yates JL, Racine R, McBride KM, Winslow GM. T cell-dependent IgM memory B cells generated during bacterial infection are required for IgG responses to antigen challenge. J Immunol 2013; 191:1240-9.
25. Dogan I, Bertocci B, Vilmont V, et al. Multiple layers of B cell memory with different effector functions. Nat Immunol 2009; 10:1292-9.
26. Pape KA, Taylor JJ, Maul RW, Gearhart PJ, Jenkins MK. Different B cell populations mediate early and late memory during an endogenous immune response. Science 2011; 331:1203-7.
27. Seifert M, Przekopowitz M, Taudien S, et al. Functional capacities of human IgM memory B cells in early inflammatory responses and secondary germinal center reactions. Proc Natl Acad Sci U S A 2015; 112:E546-55.
28. LuytjesW, Enouf V, Schipper M, et al. HI responses induced by seasonal influenza vaccination are associated with clinical protection and with seroprotection against non-homologous strains. Vaccine 2012; 30:5262-9.
29. Vesikari T, Pellegrini M, Karvonen A, et al. Enhanced immunogenicity of seasonal influenza vaccines in young children using MF59 adjuvant. Pediatr Infect Dis J 2009; 28:563-71.
30. Vesikari T, Knuf M, Wutzler P, et al. Oil-in-water emulsion adjuvant with influenza vaccine in young children. N Engl J Med 2011; 365:1406-16.
31. Greenbaum JA, Kotturi MF, Kim Y, et al. Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc Natl Acad Sci U S A 2009; 106:20365-70.
32. Subbramanian RA, Basha S, Shata MT, Brady RC, Bernstein DI. Pandemic and seasonal H1N1 influenza hemagglutinin-specific T cell responses elicited by seasonal influenza vaccination. Vaccine 2010; 28:8258-67.
33. Lambe T, Spencer AJ, Mullarkey CE, et al. T-cell responses in children to internal influenza antigens, 1 year after immunization with pandemic H1N1 influenza vaccine, and response to revaccination with seasonal trivalent-inactivated influenza vaccine. Pediatr Infect Dis J 2012; 31:e86-91.
34. He XS, Holmes TH, Zhang C, et al. Cellular immune responses in children and adults receiving inactivated or live attenuated influenza vaccines. J Virol 2006; 80:11756-66.
35. Hoft DF, Babusis E, Worku S, et al. Live and inactivated influenza vaccines induce similar humoral responses, but only live vaccines induce diverse T-cell responses in young children. J Infect Dis 2011; 204:845-53.
36. He XS, Holmes TH, Mahmood K, et al. Phenotypic changes in influenza-specific CD8+ T cells after immunization of children and adults with influenza vaccines. J Infect Dis 2008; 197:803-11.
37. Sealy R, Webby RJ, Crumpton JC, Hurwitz JL. Differential localization and function of antibody-forming cells responsive to inactivated or live-Attenuated influenza virus vaccines. Int Immunol 2013; 25:183-95.