Persistence of antibodies to influenza hemagglutinin and neuraminidase following one or two years of influenza vaccination

Journal of Infectious Diseases

Volumn 212, Issue 12, 2015, Pages 1914-1922

  Petrie, Joshua G ^a   Ohmit, Suzanne E ^a   Johnson, Emileigh ^a   Truscon, Rachel ^a   Monto, Arnold S ^a  

^a UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Antibody persistence; Hemagglutinin; Immune correlates; Influenza; Influenza vaccine; Longevity of antibody; Neuraminidase; Serologic assays; Waning

Indexed keywords

HEMAGGLUTININ; INFLUENZA VACCINE; MEMBRANE ANTIGEN; PLACEBO; SIALIDASE; INFLUENZA VIRUS HEMAGGLUTININ; LIVE VACCINE; VIRUS ANTIBODY;

ADULT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; ENZYME INHIBITION; FEMALE; HEMAGGLUTINATION INHIBITION; HUMAN; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VACCINATION; MALE; NORMAL HUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; TREATMENT DURATION; ADOLESCENT; BLOOD; IMMUNOASSAY; IMMUNOLOGY; MIDDLE AGED; PROCEDURES; TIME FACTOR; VACCINATION; YOUNG ADULT;

ADOLESCENT; ADULT; ANTIBODIES, VIRAL; FEMALE; HEALTHY VOLUNTEERS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOASSAY; INFLUENZA VACCINES; MALE; MIDDLE AGED; NEURAMINIDASE; PLACEBOS; TIME FACTORS; VACCINATION; VACCINES, ATTENUATED; YOUNG ADULT;

EID: 84959387613     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiv313     Document Type: Article

References (43)

1. Committee for Proprietary Medicinal Products. Note for guidance on harmonization of requirements for influenza vaccines. 1997. CPMP/BWP/214/96 (circular 96-0666):1-22. http://www.ema.europa.eu/docs/en-GB/document-library/Scientific-guideline/2009/09/WC500003945. pdf. Accessed 23 March 2014.
2. US Department of Health and Human Services, Food and Drug Administration, Center for Biologics Evaluation and Research. Guidance for industry: clinical data needed to support the licensure of seasonal inactivated influenza vaccines. 2007. http://www.fda.gov/cber/gdlns/trifluvac.htm. Accessed 23 March 2014.
3. Gamblin SJ, Skehel JJ. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem 2010; 285:28403-9.
4. Johansson BE, Cox MMJ. Influenza viral neuraminidase: the forgotten antigen. Expert Rev Vaccines 2011; 10:1683-95.
5. Hobson D, Curry RL, Beare AS, Ward-Gardner A. The role of serum hae-magglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J Hyg Camb 1972; 70:767-77.
6. Ohmit SE, Petrie JG, Cross RT, Johnson E, Monto AS. Influenza hem-agglutination-inhibition antibody as a correlate of vaccine-induced protection. J Infect Dis 2011; 204:1879-85.
7. Hannoun C, Megas F, Piercy J. Immunogenicity and protective efficacy of influenza vaccination. Virus Res 2004; 103:133-8.
8. Couch RB, Atmar RL, Franco LM, et al. Antibody correlates and predictors of immunity to naturally occurring influenza in humans and the importance of antibody to the neuraminidase. J Infect Dis 2013; 207:974-81.
9. Centers for Disease Control and Prevention. Prevention and control of influenza: recommendations of the Immunization Practices Advisory Committee (ACIP). MMWR Recomm Rep 1990; 39(RR-7):1-15.
10. Smith NM, Bresee JS, Shay DK, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2006; 55(RR-10):1-42.
11. Fiore AE, Shay DK, Haber P, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2007. MMWR Recomm Rep 2007; 56(RR-6):1-54.
12. Skowronski DM, Tweed SA, De Serres G. Rapid decline of influenza vaccine-induced antibody in the elderly: is it real, or is it relevant? J Infect Dis 2008; 197:490-502.
13. Beyer WEP, Palache AM, Sprenger MJW, et al. Effects of repeated annual influenza vaccination on vaccine sero-response in young and elderly adults. Vaccine 1996; 14:1331-9.
14. Sasaki S, He XS, Holmes TH, et al. Influence of prior influenza vaccination on antibody and B-cell responses. PLOS One 2008; 3:e2975.
15. Huijskens E, Rossen J, Mulder P, et al. Immunogenicity, boostability and sustainability of the immune response after vaccination against influenza A virus (H1N1) 2009 in a healthy population. Clin Vaccine Immunol 2011; 18:1401-5.
16. Künzel W, Glathe H, Engelmann H, Van Hoecke C. Kinetics of humoral antibody response to trivalent inactivated split influenza vaccine in subjects previously vaccinated or vaccinated for the first time. Vaccine 1996; 14:1108-10.
17. Beyer WE, de Bruijn IA, Palache AM, Westendorp RG, Osterhaus ADME. Protection against influenza after annually repeated vaccination; a meta-analysis of serologic and field studies. Arch Intern Med 1999; 159:182-8.
18. Keitel WA, Cate TR, Couch RB, Huggins LL, Hess KR. Efficacy of repeated annual immunization with inactivated influenza virus vaccines over a five year period. Vaccine 1997; 15:1114-22.
19. Ohmit SE, Petrie JG, Malosh RE, et al. Influenza vaccine effectiveness in the community and the household. Clin Infect Dis 2013; 56:1363-9.
20. Ohmit SE, Thompson MG, Petrie JG, 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 2014; 58:319-27.
21. Sullivan SG, Kelly H. Stratified estimates of influenza vaccine effectiveness by prior vaccination: caution required. Clin Infect Dis 2013; 57:474-6.
22. Thompson MG, Li DK, Shifflett P, et al. Effectiveness of seasonal trivalent influenza vaccine for preventing influenza virus illness among pregnant women:a population-based case-control study during the 2010-2011 and 2011-2012 influenza seasons. Clin Infect Dis 2014; 58:449-57.
23. Skowronski DM, Janjua NZ, De Serres G, et al. Low 2012-13 influenza vaccine effectiveness associated with mutation in the egg-adapted H3N2 vaccine strain not antigenic drift in circulating viruses. PLOS One 2014; 9:e92153.
24. McLean HQ, Thompson MG, Sundaram ME, et al. Influenza vaccine effectiveness in the United States during 2012-2013: variable protection by age and virus type. J Infect Dis 2015; 211:1529-40.
25. Ohmit SE, Petrie JG, Malosh RE, et al. Influenza vaccine effectiveness in households with children during the 2012-2013 season: assessments of prior vaccination and serologic susceptibility. J Infect Dis 2015; 211:1519-28.
26. McLean HQ, Thompson MG, Sundaram ME, et al. Impact of repeated vaccination on vaccine effectiveness against influenza A (H3N2) and B during 8 seasons. Clin Infect Dis 2014; 59:1375-85.
27. Aymard-Henry M, Coleman MT, Dowdle WR, Laver WG, Schild GC, Webster RG. Influenza virus neuraminidase and neuraminidase inhibition test procedures. Bull WHO 1973; 48:199-202.
28. Sandbulte MR, Gao J, Straight TM, Eichelberger MC. A miniaturized assay for influenza neuraminidase-inhibiting antibodies utilizing reverse genetics-derived antigens. Influenza Other Respi Viruses 2009; 3:233-40.
29. Ohmit SE, Victor JC, Teich ER, et al. Prevention of symptomatic seasonal influenza in 2005-2006 by inactivated and live-attenuated vaccines. J Infect Dis 2008; 198:312-7.
30. Katz JM, Hancock K, Xu X. Serologic assays for influenza surveillance, diagnosis and vaccine evaluation. Exp Rev Vacc 2011; 9:669-83.
31. World Health Organization. Recommended composition of influenza virus vaccines for use in the 2005-2006 influenza season. Wkly Epidemiol Rec 2005; 80:65-76.
32. Couzens L, Gao J, Westgeest K, et al. An optimized enzyme-linked lectin assay to measure influenza A virus neuraminidase inhibition antibody titers in human sera. J Virol Meth 2014; 210:7-14.
33. Beyer WE, Palache AM, Luchters G, Nauta J, Osterhaus AD. Seropro-tection rate, mean fold increase, seroconversion rate: which parameter adequately expresses seroresponse to influenza vaccination? Virus Res 2004; 103:125-32.
34. Moran JJ, Rose WE, Darga AJ, Rohde KA, Hayney MS. Persistence of influenza vaccine-induced antibodies in lung transplant patients between seasons. Transpl Infect Dis 2011; 13:466-70.
35. Cox RJ. Correlates of protection to influenza virus, where do we go from here? Hum Vaccin Immunother 2013; 9:405-8.
36. Tsang TK, Cauchemez S, Mahen Perera RAP, et al. Association between antibody titers and protection against influenza virus infection within households. J Infect Dis 2014; 210:684-92.
37. Schild GC, Newman RW. Antibody against influenza A2 virus neur-aminidase in human sera. J Hyg Camb 1969; 67:353-65.
38. Smith AJ, Davies JR. Natural infection with influenza A (H3N2). The development, persistence and effect of antibodies to the surface antigens. J Hyg Camb 1976; 77:271-82.
39. Grilli EA, Davies JR, Smith AJ. Infection with influenza A (H1N1) 1. Production and persistence of antibody. J Hyg Camb 1986; 96:335-43.
40. Monto AS, Kendal AP. Effect of neuraminidase antibodyon Hong Kong influenza. Lancet 1973; 1:623-5.
41. Monto AS, Petrie JG, Cross RT, et al. Antibody to the influenza neur-aminidase: an independent correlate of protection. J Infect Dis 2015; 212:1191-9.
42. Cate TR, Couch RB, Parker D, Baxter B. Reactogenicity, immunogenic-ity, and antibody persistence in adults given inactivated influenza virus vaccines-1978. Rev Infect Dis 1983; 5:737-47.
43. Carrat F, Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine 2007; 25:6852-62.