Beyond Antigenic Match: Possible Agent-Host and Immuno-epidemiological Influences on Influenza Vaccine Effectiveness during the 2015-2016 Season in Canada

Journal of Infectious Diseases

Volumn 216, Issue 12, 2017, Pages 1487-1500

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

^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 TORONTO   (Canada)

^h UNIVERSITY OF CALGARY   (Canada)

ⁱ Prov Laboratory of Northern Alberta   (Canada)

^j UNIVERSITY OF ALBERTA   (Canada)

^k PUBLIC HEALTH AGENCY OF CANADA   (Canada)

more..

Author keywords

birth cohort effects; hemagglutination inhibition; Influenza; influenza A subtype; influenza B lineage; influenza vaccine; original antigenic sin; repeat vaccination; sequencing; vaccine effectiveness

Indexed keywords

INFLUENZA VACCINE; VIRUS ANTIGEN;

ADOLESCENT; ADULT; AGED; ARTICLE; CANADA; CHILD; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; GENE SEQUENCE; GENETIC VARIATION; GROUPS BY AGE; HEMAGGLUTINATION INHIBITION TEST; HUMAN; IMMUNITY; INFLUENZA A (H1N1); INFLUENZA A VIRUS (H1N1); INFLUENZA B; INFLUENZA VACCINATION; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PRIORITY JOURNAL; VIRAL GENETICS; YOUNG ADULT; AGE; ANTIGENIC VARIATION; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; IMMUNIZATION; IMMUNOLOGY; INFANT; INFLUENZA; INFLUENZA B VIRUS; ISOLATION AND PURIFICATION; PHYLOGENY; PRESCHOOL CHILD; PROCEDURES; SEQUENCE HOMOLOGY; TREATMENT OUTCOME; VACCINE IMMUNOGENICITY; VERY ELDERLY; VIROLOGY;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; ANTIGENIC VARIATION; ANTIGENS, VIRAL; CANADA; CHILD; CHILD, PRESCHOOL; CLUSTER ANALYSIS; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HUMANS; IMMUNIZATION; IMMUNOGENICITY, VACCINE; INFANT; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA B VIRUS; INFLUENZA VACCINES; INFLUENZA, HUMAN; MALE; MIDDLE AGED; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; TREATMENT OUTCOME; YOUNG ADULT;

EID: 85031676644     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jix526     Document Type: Article

References (51)

1. Public Health Agency of Canada. FluWatch report: August 14 to August 27, 2016 (weeks 33-34). http://healthycanadians. gc.ca/publications/diseases-conditions-maladies-affections/fluwatch-2015-2016-33-34-surveillance-influenza/index-eng.php. Accessed 14 August 2017.
2. United States Centers for Disease Control and Prevention. Fluview 2015-2016 influenza season week 39 ending October 1, 2016. https://www.cdc.gov/flu/weekly/weeklyarchives2015-2016/Week39.htm. Accessed 14 August 2017.
3. Public Health Agency of Canada. FluWatch report: 27 July to 9 August, 2014 (weeks 31 & 32). http://publications. gc.ca/collections/collection-2014/aspc-phac/HP58-1-2014-32-eng.pdf. Accessed 14 August 2017.
4. Skowronski DM, Chambers C, Sabaiduc S, et al. Integrated sentinel surveillance linking genetic, antigenic, and epidemiologic monitoring of influenza vaccine-virus relatedness and effectiveness during the 2013-2014 influenza season. J Infect Dis 2015; 212:726-39.
5. Epperson S, Blanton L, Kniss K, et al. Influenza activity- United States, 2013-14 season and composition of the 2014-15 influenza vaccines. MMWR Morb Mortal Wkly Rep 2014; 63:483-90. https://www.cdc.gov/mmwr/pdf/wk/mm6322.pdf. Accessed 14 August 2017.
6. 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.
7. British Columbia Centre for Disease Control. Canadian Sentinel Practitioner Surveillance Network (SPSN) vaccine effectiveness (VE) estimates (95%CI), 2004-05 to 2015-16 seasons. http://www.bccdc.ca/resource-gallery/Documents/Statistics%20and%20Research/Publications/Epid/Influenza%20and%20Respiratory/SPSN-VE-By- Year-Table.pdf. Accessed 14 August 2017.
8. Skowronski DM, Janjua NZ, De Serres G, et al. Effectiveness of AS03 adjuvanted pandemic H1N1 vaccine: case-control evaluation based on sentinel surveillance system in Canada, autumn 2009. BMJ 2011; 342:c7297.
9. 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.
10. Skowronski DM, Janjua NZ, Sabaiduc S, et al. Influenza A/subtype and B/lineage effectiveness estimates for the 2011-2012 trivalent vaccine: cross-season and cross-lineage protection with unchanged vaccine. J Infect Dis 2014; 210:126-37.
11. 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.
12. Skowronski DM, Chambers C, Sabaiduc S, et al. Interim estimates of 2013/14 vaccine effectiveness against influenza A(H1N1)pdm09 from Canada's sentinel surveillance network, January 2014. Euro Surveill 2014; 19:pii=20690. http://www.eurosurveillance.org/ViewArticle.aspxArticleId= 20690. Accessed 14 August 2017.
13. Chambers C, Skowronski D, Sabaiduc S, et al. Interim estimates of 2015/16 vaccine effectiveness against influenza A(H1N1)pdm09, Canada, February 2016. Euro Surveill 2016; 21:pii=30168. http://www.eurosurveillance.org/ViewArticle.aspxArticleId=21415. Accessed 14 August 2017.
14. 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.
15. Belongia EA, Skowronski DM, McLean HQ, Chambers C, Sundaram ME, De Serres G. Repeated annual influenza vaccination and vaccine effectiveness: review of evidence. Expert Rev Vaccines 2017; 16:1-14.
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. Fonville JM, Wilks SH, James SL, et al. Antibody landscapes after influenza virus infection or vaccination. Science 2014; 346:996-1000.
18. Linderman SL, Chambers BS, Zost SJ, et al. Potential antigenic explanation for atypical H1N1 infections among middle-aged adults during the 2013-2014 influenza season. Proc Natl Acad Sci U S A 2014; 111:15798-803.
19. Cobey S, Hensley SE. Immune history and influenza virus susceptibility. Curr Opin Virol 2017; 22:105-11.
20. Hensley SE. Challenges of selecting seasonal influenza vaccine strains for humans with diverse pre-exposure histories. Curr Opin Virol 2014; 8:85-9.
21. Huang KY, Rijal P, Schimanski L, et al. Focused antibody response to influenza linked to antigenic drift. J Clin Invest 2015; 125:2631-45.
22. Petrie JG, Parkhouse K, Ohmit SE, Malosh RE, Monto AS, Hensley SE. Antibodies against the current influenza A(H1N1) vaccine strain do not protect some individuals from infection with contemporary circulating influenza A(H1N1) virus strains. J Infect Dis 2016; 214:1947-51.
23. Morens DM, Burke DS, Halstead SB. The wages of original antigenic sin. Emerg Infect Dis 2010; 16:1023-4.
24. Gaglani M, Pruszynski J, Murthy K, et al. Influenza vaccine effectiveness against 2009 pandemic Influenza A(H1N1) virus differed by vaccine type during 2013-2014 in the United States. J Infect Dis 2016; 213:1546-56.
25. Ohmit SE, Petrie JG, Malosh RE, et al. Substantial influenza vaccine effectiveness in households with children during the 2013-2014 influenza season, when 2009 pandemic influenza A(H1N1) virus predominated. J Infect Dis 2016; 213:1229-36.
26. 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.
27. National Advisory Committee on Immunization (NACI). Canadian Immunization Guide Chapter on Influenza and Statement on Seasonal Influenza Vaccine for 2015-2016. http://www.phac-aspc.gc.ca/naci-ccni/assets/pdf/flu-2015-grippe-eng.pdf. Accessed 14 August 2017.
28. Grohskopf LA, Sokolow LZ, Olsen SJ, Bresee JS, Broder KR, Karron RA. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices, United States, 2015-16 influenza season. MMWR Morb Mortal Wkly Rep 2015; 64:818-
29. https://www.cdc.gov/mmwr/preview/mmwrhtml/mm6430a3.htms-c. Accessed 14 August 2017.
30. Bodewes R, de Mutsert G, van der Klis FR, et al. Prevalence of antibodies against seasonal influenza A and B viruses in children in Netherlands. Clin Vaccine Immunol 2011; 18:469-76.
31. Jackson ML, Chung JR, Jackson LA, et al. Influenza vaccine effectiveness in the United States during the 2015-2016 season. N Engl J Med 2017; 377:534-43.
32. Kissling E, Valenciano M, Reuss A, et al. Influenza vaccine effectiveness (VE) estimates from the I-MOVE multicentre case control study in Europe, 2015-16: Feasibility of representative clade-specific VE. ESCAIDE conference 29th of November 2016; Stockholm, Sweden. page 101. http://www. escaide.eu/sites/escaide/files/documents/ESCAIDE%20 Abstract%20Book%202016.pdf. Accessed 14 August 2017.
33. Valenciano M, Kissling E, Reuss A, et al. The European I-MOVE Multicentre 2013-2014 case-control study. Homogeneous moderate influenza vaccine effectiveness against A(H1N1)pdm09 and heterogenous results by country against A(H3N2). Vaccine 2015; 2813-22.
34. Flannery B, Chung J. Influenza vaccine effectiveness, including LAIV vs. IIV in children and adolescents, US Flu VE Network, 2015-16. https://www.cdc.gov/vaccines/acip/meetings/meetings-info.html. Accessed 4 June 2017.
35. Ambrose C. 2015-2016 US influenza vaccine effectiveness-Influenza Clinical Investigation for Children (ICICLE) Study. https://www.cdc.gov/vaccines/acip/meetings/meetings-info.html. Accessed 4 June 2017.
36. Pebody R, Warburton F, Ellis J, et al. Effectiveness of seasonal influenza vaccine for adults and children in preventing laboratory-confirmed influenza in primary care in the United Kingdom: 2015/16 end-of-season results. Euro Surveill 2016; 21:pii=30348. http://www.eurosurveillance. org/ViewArticle.aspxArticleId=22592. Accessed 14 August 2017.
37. Tate MD, Job ER, Deng YM, Gunalan V, Maurer-Stroh S, Reading PC. Playing hide and seek: how glycosylation of the influenza virus hemagglutinin can modulate the immune response to infection. Viruses 2014; 6:1294-316.
38. Kissling E, Valenciano M. Early influenza vaccine effectiveness results 2015-16: I-MOVE multicentre case-control study. Euro Surveill 2016; 21:pii=30134. http://www. eurosurveillance.org/ViewArticle.aspxArticleId=21378. Accessed 14 August 2017.
39. Jimenez-Jorge S, Savulescu C, Pozo F, et al.; cycEVA Study Team; Spanish Influenza Sentinel Surveillance System. Effectiveness of the 2010-11 seasonal trivalent influenza vaccine in Spain: cycEVA study. Vaccine 2012; 30:3595-602.
40. 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.
41. Te Beest DE, de Bruin E, Imholz S, Koopmans M, van Boven M. Heterosubtypic cross-reactivity of HA1 antibodies to influenza A, with emphasis on nonhuman subtypes (H5N1, H7N7, H9N2). PLoS One 2017; 12:e0181093.
42. Monto AS, Malosh RE, Petrie JG, Martin ET. The doctrine of original antigenic sin: separating good from evil. J Infect Dis 2017; 215:1782-8.
43. Skowronski DM, Hottes TS, McElhaney JE, et al. Immunoepidemiologic correlates of pandemic H1N1 surveillance observations: higher antibody and lower cell-mediated immune responses with advanced age. J Infect Dis 2011; 203:158-67.
44. Centers for Disease Control and Prevention. Estimates of deaths associated with seasonal influenza-United States, 1976-2007. MMWR Morb Mortal Wkly Rep 2010; 59:1057-62. https://www.cdc.gov/mmwr/preview/mmwrhtml/mm5933a1.htm. Accessed 14 August 2017.
45. Skowronski DM, Chambers C, Sabaiduc S, et al. Pre-and postpandemic estimates of 2009 pandemic influenza A(H1N1) seroprotection to inform surveillance-based incidence, by age, during the 2013-2014 epidemic in Canada. J Infect Dis 2015; 211:109-14.
46. Skowronski DM, Hamelin ME, Janjua NZ, et al. Crosslineage influenza B and heterologous influenza A antibody responses in vaccinated mice: immunologic interactions and B/Yamagata dominance. PLoS One 2012; 7:e38929.
47. Skowronski DM, Hottes TS, De Serres G, et al. Influenza /Victoria antigen induces strong recall of /Yamagata but lower /Victoria response in children primed with two doses of /Yamagata. Pediatr Infect Dis J 2011; 30:833-9.
48. Tricco AC, Chit A, Soobiah C, et al. Comparing influenza vaccine efficacy against mismatched and matched strains: a systematic review and meta-analysis. BMC Med 2013; 11:153.
49. Skowronski DM, Chambers C, De Serres G, et al. Agerelated differences in influenza B infection by lineage in a community-based sentinel system, 2010-11 to 2015-16, Canada. J Infect Dis 2017; 15:697-702.
50. Robertson JS, Naeve CW, Webster RG, Bootman JS, Newman R, Schild GC. Alterations in the hemagglutinin associated with adaptation of influenza B virus to growth in eggs. Virology 1985; 143:166-74.
51. Public Health Agency of Canada. Influenza vaccine uptake: Results from the 2015/16 national influenza immunization coverage survey in Canada. Government of Canada: Ottawa, 2017. https://www.canada.ca/en/public-health/services/publications/healthy-living/vaccine-uptake-results-2015-16-national-influenza-immunization-coverage-survey.html. Accessed 14 August 2017.