Serial vaccination and the antigenic distance hypothesis: Effects on influenza vaccine effectiveness during A(H3N2) epidemics in Canada, 2010-2011 to 2014-2015

Journal of Infectious Diseases

Volumn 215, Issue 7, 2017, Pages 1059-1069

  Skowronski, Danuta M ^a,b   Chambers, Catharine ^a   De Serres, Gaston ^c,d,e   Sabaiduc, Suzana ^a   Winter, Anne Luise ^f   Dickinson, James A ^g   Gubbay, Jonathan B ^f,h   Fonseca, Kevin ^g,i   Drews, Steven J ^j,k   Charest, Hugues ^c,l   Martineau, Christine ^c   Krajden, Mel ^a,b   Petric, Martin ^b   Bastien, Nathalie ^m   Li, Yan ^m   Smith, Derek J ⁿ  

^a BRITISH COLUMBIA CENTRE FOR DISEASE CONTROL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c INSTITUT NATIONAL DE SANTÉ PUBLIQUE DU QUÉBEC   (Canada)

^d UNIVERSITÉ LAVAL   (Canada)

^e LAVAL UNIVERSITY   (Canada)

^f PUBLIC HEALTH ONTARIO   (Canada)

^g UNIVERSITY OF CALGARY   (Canada)

^h UNIVERSITY OF TORONTO   (Canada)

ⁱ Alberta Provincial Laboratory   (Canada)

^j Provincial Laboratory (ProvLab)   (Canada)

^k UNIVERSITY OF ALBERTA   (Canada)

^l UNIVERSITÉ DE MONTRÉAL   (Canada)

^m PUBLIC HEALTH AGENCY OF CANADA   (Canada)

ⁿ UNIVERSITY OF CAMBRIDGE   (United Kingdom)

more..

Author keywords

Antigenic distance hypothesis; Antigenic site; Genomic sequencing; Hemagglutination inhibition; Influenza; Influenza A(H3N2) subtype; Influenza vaccine; Negative interference; Repeat vaccination; Vaccine effectiveness

Indexed keywords

INFLUENZA VACCINE;

ADOLESCENT; ADULT; AGED; ANTIGENIC DISTANCE HYPOTHESIS; CANADA; CHILD; CONFERENCE PAPER; CONTROLLED STUDY; DISEASE SURVEILLANCE; DRUG EFFICACY; EPIDEMIC; FEMALE; HUMAN; INFLUENZA A (H3N2); INFLUENZA VACCINATION; MAJOR CLINICAL STUDY; MALE; OUTPATIENT; PRIORITY JOURNAL; SEASONAL VARIATION; STATISTICAL MODEL; CASE CONTROL STUDY; EPIDEMICS; HEMAGGLUTINATION INHIBITION TEST; IMMUNOLOGY; INFLUENZA A VIRUS (H3N2); INFLUENZA, HUMAN; MIDDLE AGED; SEASON; SENTINEL SURVEILLANCE; STATISTICS AND NUMERICAL DATA; VACCINATION; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; CANADA; CASE-CONTROL STUDIES; CHILD; EPIDEMICS; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; LOGISTIC MODELS; MALE; MIDDLE AGED; SEASONS; SENTINEL SURVEILLANCE; VACCINATION; YOUNG ADULT;

EID: 85020233692     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jix074     Document Type: Conference Paper

References (51)

1. Hoskins TW, Davies JR, Allchin A, Miller CL, Pollock TM. Controlled trial of inactivated influenza vaccine containing the A-Hong Kong strain during an outbreak of influenza due to the A-England-42-72 strain. Lancet 1973; 2:116-20.
2. Hoskins TW, Davies JR, Smith AJ, Allchin A, Miller CL, Pollock TM. Influenza at Christ's Hospital: March, 1974. Lancet 1976; 1:105-8.
3. Hoskins TW, Davies JR, Smith AJ, Miller CL, Allchin A. Assessment of inactivated influenza-A vaccine after three outbreaks of influenza A at Christ's Hospital. Lancet 1979; 1:33-5.
4. 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.
5. 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.
6. Thompson MG, Li DK, Shifflett P, et al.; Pregnancy and Influenza Project Workgroup. 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.
7. 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.
8. Skowronski DM, Janjua NZ, De Serres G, et al. A sentinel platform to evaluate influenza vaccine effectiveness and new variant circulation, Canada 2010-2011 season. Clin Infect Dis 2012; 55:332-42.
9. 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.
10. Skowronski DM, Chambers C, Sabaiduc S, et al. A perfect storm: impact of genomic variation and serial vaccination on low influenza vaccine effectiveness during the 2014-2015 season. Clin Infect Dis 2016; 63:21-32.
11. Valenciano M, Kissling E, Reuss A, Rizzo C, Gherasim A, Horvath JK, et al. Vaccine effectiveness in preventing laboratory-confirmed influenza in primary care patients in a season of co-circulation of influenza A(H1N1)pdm09, B and drifted A(H3N2), I-MOVE multicentre case-control study, Europe 2014/15. Euro Surveill 2016; 21: pii:30139.
12. Thompson MG, Naleway A, Fry AM, et al. Effects of repeated annual inactivated influenza vaccination among healthcare personnel on serum hemagglutinin inhibition antibody response to A/Perth/16/2009 (H3N2)-like virus during 2010-11. Vaccine 2016; 34:981-8.
13. Ohmit SE, Petrie JG, Malosh RE, Fry AM, Thompson MG, Monto AS. 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.
14. Beyer WE, de Bruijn IA, Palache AM, Westendorp RG, Osterhaus AD. Protection against influenza after annually repeated vaccination: a meta-analysis of serologic and field studies. Arch Intern Med 1999; 159:182-8.
15. Smith DJ, Forrest S, Ackley DH, Perelson AS. Variable efficacy of repeated annual influenza vaccination. Proc Natl Acad Sci U S A 1999; 96:14001-6.
16. Katz JM, Hancock K, Xu X. Serologic assays for influenza surveillance, diagnosis and vaccine evaluation. Expert Rev Anti Infect Ther 2011; 9:669-83.
17. Belongia EA, Simpson MD, King JP, et al. Variable influenza vaccine effectiveness by subtype: a systematic review and meta-analysis of test-negative design studies. Lancet Infect Dis 2016; 16:942-51.
18. World Health Organization. WHO recommendations on the composition of influenza virus vaccines. http://www.who.int/influenza/vaccines/virus/recommendations/en/.Accessed 30 November 2016.
19. Francis Crick Institute. Annual and interim reports. https://www.crick.ac.uk/research/worldwide-influenza-centre/annual-and-interim-reports/.Accessed 30 November, 2016.
20. Skowronski DM, Sabaiduc S, Chambers C, et al. Mutations acquired during cell culture isolation may affect antigenic characterisation of influenza A(H3N2) clade 3C.2a viruses. Euro Surveill 2016; 21:30112.
21. Thompson MG, Shay DK, Zhou H, et al. Estimates of deaths associated with seasonal influenza-United States, 1976-2007. Morb Mortal Wkly Rep 2010; 59:1057-62. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5933a1.htm?s-cid=mm5933a1-w.Accessed 30 November 2016.
22. Flannery B, Zimmerman RK, Gubareva LV, et al. Enhanced genetic characterization of influenza A(H3N2) viruses and vaccine effectiveness by genetic group, 2014-2015. J Infect Dis 2016; 214:1010-9.
23. Zimmerman RK, Nowalk MP, Chung J, et al. 2014-2015 influenza vaccine effectiveness in the United States by vaccine type. Clin Infect Dis 2016; 63:1564-73.
24. Rizzo C, Bella A, Alfonsi V, et al. Influenza vaccine effectiveness in Italy: Age, subtype- specific and vaccine type estimates 2014/15 season. Vaccine 2016; 34:3102-8.
25. Public Health Agency of Canada. Vaccine coverage amongst adult Canadians: results from the 2012 adult National Immunization Coverage (aNIC) survey. http://www.phac-aspc.gc.ca/im/nics-enva/vcac-cvac-eng.php. Accessed 30 November 2016.
26. Government of Canada. Vaccine uptake in Canadian adults: results from the 2014 adult National Immunization Coverage Survey (aNICS). http://www.healthycanadians.gc.ca/publications/healthy-living-vie-saine/vaccine-coverage-adults-results-2014-resultats-couverture-vaccinale-adultes/index-eng.php.Accessed 30 November 2016.
27. Skowronski DM, De Serres G, Crowcroft NS, et al.; Canadian SAVOIR Team. Association between the 2008-09 seasonal influenza vaccine and pandemic H1N1 illness during Spring-Summer 2009: four observational studies from Canada. PLoS Med 2010; 7:e1000258.
28. Gilca R, Deceuninck G, De Serres G, et al. Effectiveness of pandemic H1N1 vaccine against influenza-related hospitalization in children. Pediatrics 2011; 128:e1084-91.
29. Crum-Cianflone NF, Blair PJ, Faix D, et al. Clinical and epidemiologic characteristics of an outbreak of novel H1N1 (swine origin) influenza A virus among United States military beneficiaries. Clin Infect Dis 2009; 49:1801-10.
30. Tsuchihashi Y, Sunagawa T, Yahata Y, et al. Association between seasonal influenza vaccination in 2008-2009 and pandemic influenza A (H1N1) 2009 infection among school students from Kobe, Japan, April-June 2009. Clin Infect Dis 2012; 54:381-3.
31. Skowronski DM, Hamelin ME, De Serres G, et al. Randomized controlled ferret study to assess the direct impact of 2008-09 trivalent inactivated influenza vaccine on A(H1N1)pdm09 disease risk. PLoS One 2014; 9:e86555.
32. Gauger PC, Vincent AL, Loving CL, et al. Kinetics of lung lesion development and pro-inflammatory cytokine response in pigs with vaccine-associated enhanced respiratory disease induced by challenge with pandemic A/H1N1 influenza virus. Vet Pathol 2012; 49:900-12.
33. Public Health Agency of Canada. Statement on seasonal influenza vaccine for 2011-12. An Advisory Committee Statement (ACS). National Advisory Committee on Immunization (NACI). Canada Communicable Disease Report 2011; 37:1-55. http://www.phac-aspc.gc.ca/publicat/ccdr-rmtc/11vol37/acs-dcc-5/index-eng.php. Accessed 30 November 2016.
34. Public Health Agency of Canada. Statement on seasonal influenza vaccine for 2013-14. National Advisory Committee on Immunization (NACI). Canada Communicable Disease Report 2013; 39:1-37. http://www.phac-aspc.gc.ca/publicat/ccdr-rmtc/13vol39/acs-dcc-4/index-eng.php. Accessed 30 November 2016.
35. Fonville JM, Wilks SH, James SL, et al. Antibody landscapes after influenza virus infection or vaccination. Science 2014; 346:996-1000.
36. Neher RA, Bedford T, Daniels RS, Russell CA, Shraiman BI. Prediction, dynamics, and visualization of antigenic phenotypes of seasonal influenza viruses. Proc Natl Acad Sci U S A 2016; 113:E1701-9.
37. Morens DM, Burke DS, Halstead SB. The wages of original antigenic sin. Emerg Infect Dis 2010; 16:1023-4.
38. Skowronski DM, Hottes TS, McElhaney JE, et al. Immuno-epidemiologic correlates of pandemic H1N1 surveillance observations: higher antibody and lower cell-mediated immune responses with advanced age. J Infect Dis 2011; 203:158-67.
39. Skowronski DM, Janjua NZ, De Serres G, et al. Cross-reactive and vaccine-induced antibody to an emerging swine-origin variant of influenza A virus subtype H3N2 (H3N2v). J Infect Dis 2012; 206:1852-61.
40. Miller MS, Gardner TJ, Krammer F, et al. Neutralizing antibodies against previously encountered influenza virus strains increase over time: a longitudinal analysis. Sci Transl Med 2013; 5:198ra107.
41. Hensley SE. Challenges of selecting seasonal influenza vaccine strains for humans with diverse pre-exposure histories. Curr Opin Virol 2014; 8:85-9.
42. Gostic KM, Ambrose M, Worobey M, Lloyd-Smith JO. Potent protection against H5N1 and H7N9 influenza via childhood hemagglutinin imprinting. Science 2016; 354:722-6.
43. Huang KY, Rijal P, Schimanski L, et al. Focused antibody response to influenza linked to antigenic drift. J Clin Invest 2015; 125:2631-45.
44. O'Gorman WE, Huang H, Wei YL, et al. The split virus influenza vaccine rapidly activates immune cells through Fc? receptors. Vaccine 2014; 32:5989-97.
45. Halstead SB, Mahalingam S, Marovich MA, Ubol S, Mosser DM. Intrinsic antibody- dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 2010; 10:712-22.
46. Bodewes R, Fraaij PL, Geelhoed-Mieras MM, et al. Annual vaccination against influenza virus hampers development of virus-specific CD8? T cell immunity in children. J Virol 2011; 85:11995-2000.
47. Ndifon W. A simple mechanistic explanation for original antigenic sin and its alleviation by adjuvants. J R Soc Interface 2015; 12:20150627.
48. Tsang JS. Utilizing population variation, vaccination, and systems biology to study human immunology. Trends Immunol 2015; 36:479-93.
49. Irving SA, Donahue JG, Shay DK, Ellis-Coyle TL, Belongia EA. Evaluation of self-reported and registry-based influenza vaccination status in a Wisconsin cohort. Vaccine 2009; 27:6546-9.
50. Hottes TS, Skowronski DM, Hiebert B, et al. Influenza vaccine effectiveness in the elderly based on administrative databases: change in immunization habit as a marker for bias. PLoS One 2011; 6:e22618.
51. Davies JR, Grilli EA. Natural or vaccine-induced antibody as a predictor of immunity in the face of natural challenge with influenza viruses. Epidemiol Infect 1989; 102:325-33.