Influenza vaccine: the challenge of antigenic drift.

Influenza continues to have a major worldwide impact, resulting in considerable human suffering and economic burden. The regular recurrence of influenza epidemics is thought to be caused by antigenic drift, and a number of studies have shown that sufficient changes can accumulate in the virus to allow influenza to reinfect the same host. To address this, influenza vaccine content is reviewed annually to ensure protection is maintained, despite the emergence of drift variants; however, it is not always possible to capture every significant drift, partly due to the timing of the recommendations. Vaccine mismatch can impact on vaccine effectiveness, and has significant epidemiological and economical consequences, as was seen most apparently in the 1997-1998 influenza season. To meet the challenge of antigenic drift, vaccines that confer broad protection against heterovariant strains are needed against seasonal, epidemic and pandemic influenza. In addition to the use of vaccine adjuvants, emerging research areas include development of a universal vaccine and the use of vaccines that exploit mechanisms of cross-protective immunity.

[1]  N. Sugaya,et al.  Efficacy of inactivated vaccine in preventing antigenically drifted influenza type A and well-matched type B. , 1994, JAMA.

[2]  R. Rappuoli,et al.  An MF59-adjuvanted inactivated influenza vaccine containing A/Panama/1999 (H3N2) induced broader serological protection against heterovariant influenza virus strain A/Fujian/2002 than a subunit and a split influenza vaccine. , 2006, Vaccine.

[3]  Julia R Gog,et al.  Influenza drift and epidemic size: the race between generating and escaping immunity. , 2004, Theoretical population biology.

[4]  R. Walker,et al.  Live attenuated versus inactivated influenza vaccine in infants and young children. , 2007, The New England journal of medicine.

[5]  A. Flahault,et al.  Real-time monitoring of the influenza vaccine field effectiveness. , 2006, Vaccine.

[6]  S. Lindstrom,et al.  Comparative Analysis of Evolutionary Mechanisms of the Hemagglutinin and Three Internal Protein Genes of Influenza B Virus: Multiple Cocirculating Lineages and Frequent Reassortment of the NP, M, and NS Genes , 1999, Journal of Virology.

[7]  T. Schumacher,et al.  Selective Expansion of Cross-Reactive Cd8+ Memory T Cells by Viral Variants , 1999, The Journal of experimental medicine.

[8]  N. Blackburn,et al.  Impact of the introduction of A/Sydney/5/97 H3N2 influenza virus into South Africa , 1999, Journal of medical virology.

[9]  F. Hayden,et al.  Safety and immunogenicity of a baculovirus-expressed hemagglutinin influenza vaccine: a randomized controlled trial. , 2007, JAMA.

[10]  Jonathan Dushoff,et al.  Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Ying-hua Chen,et al.  The epitope recognized by a monoclonal antibody in influenza A virus M2 protein is immunogenic and confers immune protection. , 2005, International immunopharmacology.

[12]  G L Ada,et al.  Options for the control of influenza III. Cairns, North Queensland, Australia (4-9 May 1996). , 1997, Vaccine.

[13]  C. Glaser,et al.  Severe Pediatric Influenza in California, 2003–2005: Implications for Immunization Recommendations , 2006, Pediatrics.

[14]  Y. Kawaoka,et al.  Intranasal immunization with formalin-inactivated virus vaccine induces a broad spectrum of heterosubtypic immunity against influenza A virus infection in mice. , 2003, Vaccine.

[15]  John Cruz,et al.  Human Cytotoxic T-Lymphocyte Repertoire to Influenza A Viruses , 1998, Journal of Virology.

[16]  W. Fitch,et al.  Positive Darwinian evolution in human influenza A viruses. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Min-Shi Lee,et al.  Predicting Antigenic Variants of Influenza A/H3N2 Viruses , 2004, Emerging infectious diseases.

[18]  Elizabeth C. Theil,et al.  Epochal Evolution Shapes the Phylodynamics of Interpandemic Influenza A (H3N2) in Humans , 2006, Science.

[19]  N. Ferguson,et al.  Ecological and immunological determinants of influenza evolution , 2003, Nature.

[20]  A. Monto,et al.  Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. , 2006, The New England journal of medicine.

[21]  H. Sacks,et al.  The Efficacy of Influenza Vaccine in Elderly Persons , 1995, Annals of Internal Medicine.

[22]  Viggo Andreasen,et al.  Dynamics of annual influenza A epidemics with immuno-selection , 2003, Journal of mathematical biology.

[23]  J. Wood Selection of influenza vaccine strains and developing pandemic vaccines. , 2002, Vaccine.

[24]  M. Eichelberger,et al.  Evidence of a cross-protective immune response to influenza A in the cotton rat model. , 2006, Vaccine.

[25]  W. Fiers,et al.  Universal influenza A vaccine: optimization of M2-based constructs. , 2005, Virology.

[26]  E. Holmes,et al.  The evolution of epidemic influenza , 2007, Nature Reviews Genetics.

[27]  T. Kuiken,et al.  Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. , 2007, Vaccine.

[28]  T. Kurata,et al.  Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. , 2005, Japanese journal of infectious diseases.

[29]  N. Cox,et al.  Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: multiple evolutionary pathways and sequential amino acid changes at key antigenic sites , 1983, Journal of virology.

[30]  A. Lapedes,et al.  Mapping the Antigenic and Genetic Evolution of Influenza Virus , 2004, Science.

[31]  M. Zambon,et al.  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 , 2001, The Lancet.

[32]  A. Hay,et al.  Recent changes among human influenza viruses. , 2004, Virus research.

[33]  M. Faccini,et al.  Safety and immunogenicity of MF59-adjuvanted influenza vaccine in the elderly. , 1999, Vaccine.

[34]  M. Zambon,et al.  Epidemiology and pathogenesis of influenza. , 1999, The Journal of antimicrobial chemotherapy.

[35]  Bryan T Grenfell,et al.  Whole-Genome Analysis of Human Influenza A Virus Reveals Multiple Persistent Lineages and Reassortment among Recent H3N2 Viruses , 2005, PLoS biology.

[36]  Michael W Deem,et al.  Quantifying influenza vaccine efficacy and antigenic distance. , 2005, Vaccine.

[37]  Y. Iwakura,et al.  Secretory IgA antibodies provide cross‐protection against infection with different strains of influenza B virus , 2004, Journal of medical virology.

[38]  M. Meltzer,et al.  Effectiveness and cost-benefit of influenza vaccination of healthy working adults: A randomized controlled trial. , 2000, JAMA.

[39]  Keiji Fukuda,et al.  Evolution of H5N1 Avian Influenza Viruses in Asia , 2005, Emerging infectious diseases.

[40]  C W Potter,et al.  A history of influenza , 2001, Journal of applied microbiology.

[41]  W. Fiers,et al.  A "universal" human influenza A vaccine. , 2004, Virus research.

[42]  R. Spier On the need for, and the delivery of, cross-protective vaccines. , 2005, Vaccine.

[43]  Gavin J. D. Smith,et al.  Emergence and predominance of an H5N1 influenza variant in China , 2006, Proceedings of the National Academy of Sciences.

[44]  K. Nichol,et al.  Influenza vaccine effectiveness in preventing hospitalizations and deaths in persons 65 years or older in Minnesota, New York, and Oregon: data from 3 health plans. , 2001, The Journal of infectious diseases.

[45]  J. Wilschut,et al.  The virosome concept for influenza vaccines. , 2005, Vaccine.

[46]  J. Ulmer,et al.  Protective CD4+ and CD8+ T Cells against Influenza Virus Induced by Vaccination with Nucleoprotein DNA , 1998, Journal of Virology.

[47]  A. Meijer,et al.  Epidemiological and virological assessment of influenza activity in Europe, during the 2006-2007 winter. , 2005 .

[48]  B. Schweiger,et al.  Reassortment between human A(H3N2) viruses is an important evolutionary mechanism. , 2006, Vaccine.

[49]  R. Webster,et al.  Emergence of influenza A viruses. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  K. Matsui,et al.  A fused gene of nucleoprotein (NP) and herpes simplex virus genes (VP22) induces highly protective immunity against different subtypes of influenza virus. , 2006, Virology.

[51]  A. Kendal,et al.  Impact of influenza epidemics on mortality in the United States from October 1972 to May 1985. , 1987, American journal of public health.

[52]  I. Brown,et al.  Genetic relationships, serological cross-reaction and cross-protection between H1N2 and other influenza A virus subtypes endemic in European pigs. , 2004, Virus research.

[53]  L. Simonsen,et al.  Surveillance and impact of influenza in the United States. , 1999, Vaccine.

[54]  F. Ennis,et al.  HLA-RESTRICTED VIRUS-SPECIFIC CYTOTOXIC T-LYMPHOCYTE RESPONSES TO LIVE AND INACTIVATED INFLUENZA VACCINES , 1981, The Lancet.

[55]  W. Fiers,et al.  Improved design and intranasal delivery of an M2e-based human influenza A vaccine. , 2006, Vaccine.

[56]  J. Treanor Influenza vaccine--outmaneuvering antigenic shift and drift. , 2004, The New England journal of medicine.

[57]  B. Lina,et al.  Surveillance and impact of influenza in Europe , 1999 .

[58]  C. Bridges,et al.  Influenza vaccine effectiveness among 50-64-year-old persons during a season of poor antigenic match between vaccine and circulating influenza virus strains: Colorado, United States, 2003-2004. , 2007, Vaccine.

[59]  J. Weber,et al.  Influenza vaccine match with circulating strains and indicators of influenza strain impact - Canada 1980 to 1992. , 1998, The Canadian journal of infectious diseases = Journal canadien des maladies infectieuses.

[60]  A. Osterhaus,et al.  Influenza virus: a master of metamorphosis. , 2000, The Journal of infection.

[61]  Glezen Wp Emerging Infections: Pandemic Influenza , 1996 .

[62]  N. Cox,et al.  Global epidemiology of influenza: past and present. , 2000, Annual review of medicine.

[63]  W. Fitch,et al.  Long term trends in the evolution of H(3) HA1 human influenza type A. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[64]  R. Bugarini,et al.  Cross-reactivity to highly pathogenic avian influenza H5N1 viruses after vaccination with nonadjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a potential priming strategy. , 2005, The Journal of infectious diseases.

[65]  A. Monto Epidemiology and Virology of Influenza Illness , 2000 .

[66]  Alan S. Lapedes,et al.  Recognition of Homo- and Heterosubtypic Variants of Influenza A Viruses by Human CD8+ T Lymphocytes1 , 2004, The Journal of Immunology.

[67]  Albert D. M. E. Osterhaus,et al.  Characterization of a Novel Influenza A Virus Hemagglutinin Subtype (H16) Obtained from Black-Headed Gulls , 2005, Journal of Virology.

[68]  Alex S. Morton,et al.  Modelling antigenic drift in weekly flu incidence , 2005, Statistics in medicine.

[69]  I. Barr,et al.  An influenza A(H3) reassortant was epidemic in Australia and New Zealand in 2003 , 2005, Journal of medical virology.

[70]  J. Nauta,et al.  The virosomal influenza vaccine Invivac: immunogenicity and tolerability compared to an adjuvanted influenza vaccine (Fluad in elderly subjects. , 2006, Vaccine.

[71]  A. Hampson,et al.  Annual report of the National Influenza Surveillance Scheme, 2003. , 2004, Communicable diseases intelligence quarterly report.

[72]  A. Douglas,et al.  The evolution of human influenza viruses. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[73]  T. Tumpey,et al.  Matrix Protein 2 Vaccination and Protection against Influenza Viruses, Including Subtype H5N1 , 2007, Emerging infectious diseases.

[74]  D. Skowronski,et al.  Estimating vaccine effectiveness against laboratory-confirmed influenza using a sentinel physician network: results from the 2005-2006 season of dual A and B vaccine mismatch in Canada. , 2007, Vaccine.

[75]  R. Belshe,et al.  Enhancement of anti-influenza A virus cytotoxicity following influenza A virus vaccination in older, chronically ill adults , 1990, Journal of clinical microbiology.

[76]  N. Cox,et al.  Cross-protective immunity in mice induced by live-attenuated or inactivated vaccines against highly pathogenic influenza A (H5N1) viruses. , 2006, Vaccine.