Pandemic paradox: Early life H2N2 pandemic influenza infection enhanced susceptibility to death during the 2009 H1N1 pandemic

mBio

Volumn 9, Issue 1, 2018, Pages

  Gagnon, Alain ^a   Acosta, Enrique ^a   Hallman, Stacey ^b   Bourbeau, Robert ^a   Dillon, Lisa Y ^a   Ouellette, Nadine ^a   Earn, David J D ^c   Herring, D Ann ^c   Inwood, Kris ^d   Madrenas, Joaquin ^e   Miller, Matthew S ^c,f  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b STATISTICS CANADA   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d UNIVERSITY OF GUELPH   (Canada)

^e UCLA MEDICAL CENTER   (United States)

^f MCMASTER UNIVERSITY   (Canada)

Author keywords

Influenza virus; Mortality; Pandemics; Susceptibility

Indexed keywords

2009 H1N1 INFLUENZA; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE PREDISPOSITION; EPIDEMIC; INFECTION RISK; INFLUENZA A (H2N2); MEXICO; MORTALITY; MORTALITY RATE; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; SEASONAL INFLUENZA; SEASONAL VARIATION; SPANISH INFLUENZA; UNITED STATES; EPIDEMIOLOGY; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H2N2); RISK FACTOR; VIROLOGY;

DISEASE SUSCEPTIBILITY; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H2N2 SUBTYPE; INFLUENZA, HUMAN; MEXICO; RISK FACTORS; UNITED STATES;

EID: 85043470767     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02091-17     Document Type: Article

References (55)

1. Earn DJD, Dushoff J, Levin SA. 2002. Ecology and evolution of the flu. Trends Ecol Evol 17:334–340.
2. Miller MS, Palese P. 2014. Peering into the crystal ball: influenza pandemics and vaccine efficacy. Cell 157:294–299. https://doi.org/10.1016/j.cell.2014.03.023.
3. Taubenberger JK, Morens DM. 2010. Influenza: the once and future pandemic. Public Health Rep 125(Suppl 3):16–26. https://doi.org/10.1177/00333549101250S305.
4. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, Fouchier RAM, Pappas C, Alpuche-Aranda CM, López-Gatell H, Olivera H, López I, Myers CA, Faix D, Blair PJ, Yu C, Keene KM, Dotson PD, Boxrud D, Sambol AR, Abid SH, St George K, Bannerman T, Moore AL, Stringer DJ, Blevins P, Demmler-Harrison GJ, Ginsberg M, Kriner P, Waterman S, Smole S, Guevara HF, Belongia EA, Clark PA, Beatrice ST, et al. 2009. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201. https://doi.org/10.1126/science.1176225.
5. Palese P, Shaw M. 2007. Orthomyxoviridae: the viruses and their replication, p 1647–1690. In Knipe DM, Griffin DE, Lamb RA, Straus SE, Howley PM, Martin MA, Roizman B (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
6. Gagnon A, Miller MS, Hallman SA, Bourbeau R, Herring DA, Earn DJ, Madrenas J. 2013. Age-specific mortality during the 1918 influenza pandemic: unravelling the mystery of high young adult mortality. PLoS One 8:e69586. https://doi.org/10.1371/journal.pone.0069586.
7. Gagnon A, Acosta JE, Madrenas J, Miller MS. 2015. Is antigenic sin always “original?” re-examining the evidence regarding circulation of a human H1 influenza virus immediately prior to the 1918 Spanish flu. PLoS Pathog 11:e1004615. https://doi.org/10.1371/journal.ppat.1004615.
8. Hallman SA. 2015. The demographic links between the 1890 and 1918 influenza pandemics in Ontario. PhD dissertation. University of Western Ontario, London, Ontario, Canada.
9. Oeppen JE, Wilson C. 2006. Epidemiological evidence for viral exposure in childhood as a risk-factor in subsequent influenza pandemics. Population Association of America, Los Angeles, CA.
10. Dowdle WR. 1999. Influenza A virus recycling revisited. Bull World Health Organ 77:820– 828.
11. McCullers JA, Van De Velde L-A, Allison KJ, Branum KC, Webby RJ, Flynn PM. 2010. Recipients of vaccine against the 1976 “swine flu” have enhanced neutralization responses to the 2009 novel H1N1 influenza virus. Clin Infect Dis 50:1487–1492. https://doi.org/10.1086/652441.
12. Xie H, Li X, Gao J, Lin Z, Jing X, Plant E, Zoueva O, Eichelberger MC, Ye Z. 2011. Revisiting the 1976 “swine flu” vaccine clinical trials: cross-reactive hemagglutinin and neuraminidase antibodies and their role in protection against the 2009 H1N1 pandemic virus in mice. Clin Infect Dis 53:1179–1187. https://doi.org/10.1093/cid/cir693.
13. Miller MS, Tsibane T, Krammer F, Hai R, Rahmat S, Basler CF, Palese P. 2013. 1976 and 2009 H1N1 influenza virus vaccines boost anti-hemagglutinin stalk antibodies in humans. J Infect Dis 207:98–105. https://doi.org/10.1093/infdis/jis652.
14. Ellebedy AH, Krammer F, Li G-M, Miller MS, Chiu C, Wrammert J, Chang CY, Davis CW, McCausland M, Elbein R, Edupuganti S, Spearman P, Andrews SF, Wilson PC, García-Sastre A, Mulligan MJ, Mehta AK, Palese P, Ahmed R. 2014. Induction of broadly cross-reactive antibody responses to the influenza HA stem region following H5N1 vaccination in humans. Proc Natl Acad Sci U S A 111:13133–13138. https://doi.org/10.1073/pnas.1414070111.
15. Miller MS, Gardner TJ, Krammer F, Aguado LC, Tortorella D, Basler CF, Palese P. 2013. Neutralizing antibodies against previously encountered influenza virus strains increase over time: a longitudinal analysis. Sci Transl Med 5:198ra107. https://doi.org/10.1126/scitranslmed.3006637.
16. Nachbagauer R, Wohlbold TJ, Hirsh A, Hai R, Sjursen H, Palese P, Cox RJ, Krammer F. 2014. Induction of broadly reactive anti-hemagglutinin stalk antibodies by an H5N1 vaccine in humans. J Virol 88:13260–13268. https://doi.org/10.1128/JVI.02133-14.
17. Borja-Aburto VH, Chowell G, Viboud C, Simonsen L, Miller MA, Grajales-Muñiz C, González-Bonilla CR, Diaz-Quiñonez JA, Echevarría-Zuno S. 2012. Epidemiological characterization of a fourth wave of pandemic A/H1N1 influenza in Mexico, winter 2011-2012: age shift and severity. Arch Med Res 43:563–570. https://doi.org/10.1016/j.arcmed.2012.09.005.
18. Dávila-Torres J, Chowell G, Borja-Aburto VH, Viboud C, Grajalez-Muñiz C, Miller MA. 2015. Intense seasonal A/H1N1 influenza in Mexico, winter 2013-2014. Arch Med Res 46:63–70. https://doi.org/10.1016/j.arcmed.2014.11.005.
19. Worobey M, Han G-Z, Rambaut A. 2014. Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus. Proc Natl Acad Sci U S A 111:8107– 8112. https://doi.org/10.1073/pnas.1324197111.
20. Shanks GD, Brundage JF. 2012. Pathogenic responses among young adults during the 1918 influenza pandemic. Emerg Infect Dis 18: 201–207. https://doi.org/10.3201/eid1802.102042.
21. Ma J, Dushoff J, Earn DJD. 2011. Age-specific mortality risk from pandemic influenza. J Theor Biol 288:29–34. https://doi.org/10.1016/j.jtbi.2011.08.003.
22. Almond D. 2006. Is the 1918 influenza pandemic over? Long-term effects of in utero influenza exposure in the post-1940 U.S. population. J Polit Econ 114:672–712. https://doi.org/10.1086/507154.
23. Shrestha SS, Swerdlow DL, Borse RH, Prabhu VS, Finelli L, Atkins CY, Owusu-Edusei K, Bell B, Mead PS, Biggerstaff M, Brammer L, Davidson H, Jernigan D, Jhung MA, Kamimoto LA, Merlin TL, Nowell M, Redd SC, Reed C, Schuchat A, Meltzer MI. 2011. Estimating the burden of 2009 pandemic influenza A (H1N1) in the United States (April 2009-April 2010). Clin Infect Dis 52(Suppl 1):S75–S82. https://doi.org/10.1093/cid/ciq012.
24. Serfling RE. 1963. Methods for current statistical analysis of excess pneumonia-influenza deaths. Public Health Rep 78:494–506. https://doi.org/10.2307/4591848.
25. Nguyen AM, Noymer A. 2013. Influenza mortality in the United States, 2009 pandemic: burden, timing and age distribution. PLoS One 8:e64198. https://doi.org/10.1371/journal.pone.0064198.
26. Li Y, Myers JL, Bostick DL, Sullivan CB, Madara J, Linderman SL, Liu Q, Carter DM, Wrammert J, Esposito S, Principi N, Plotkin JB, Ross TM, Ahmed R, Wilson PC, Hensley SE. 2013. Immune history shapes specificity of pandemic H1N1 influenza antibody responses. J Exp Med 210: 1493–1500. https://doi.org/10.1084/jem.20130212.
27. Linderman SL, Chambers BS, Zost SJ, Parkhouse K, Li Y, Herrmann C, Ellebedy AH, Carter DM, Andrews SF, Zheng N-Y, Huang M, Huang Y, Strauss D, Shaz BH, Hodinka RL, Reyes-Terán G, Ross TM, Wilson PC, Ahmed R, Bloom JD, Hensley SE. 2014. Potential antigenic explanation for atypical H1N1 infections among middle-aged adults during the 2013-2014 influenza season. Proc Natl Acad Sci U S A 111:15798–15803. https://doi.org/10.1073/pnas.1409171111.
28. Simonsen L, Spreeuwenberg P, Lustig R, Taylor RJ, Fleming DM, Krone-man M, Van Kerkhove MD, Mounts AW, Paget WJ, GLaMOR Collaborating Teams. 2013. Global mortality estimates for the 2009 influenza pandemic from the GLaMOR project: a modeling study. PLoS Med 10: e1001558. https://doi.org/10.1371/journal.pmed.1001558.
29. Kilbourne ED. 2006. Influenza pandemics of the 20th century. Emerg Infect Dis 12:9–14. https://doi.org/10.3201/eid1201.051254.
30. Cox CM, Goodin K, Fisher E, Dawood FS, Hamilton JJ, Leparc GF, Gray M, Nelson L, Borse RH, Singleton JA, Reed C, Balish AL, Katz JM, Hopkins RS, Fry AM. 2011. Prevalence of 2009 pandemic influenza A (H1N1) virus antibodies, Tampa Bay Florida—November-December, 2009. PLoS One 6:e29301. https://doi.org/10.1371/journal.pone.0029301.
31. Earn DJD, He D, Loeb MB, Fonseca K, Lee BE, Dushoff J. 2012. Effects of school closure on incidence of pandemic influenza in Alberta, Canada. Ann Intern Med 156:173–181. https://doi.org/10.7326/0003-4819-156-3 -201202070-00005.
32. Ikonen N, Strengell M, Kinnunen L, Osterlund P, Pirhonen J, Broman M, Davidkin I, Ziegler T, Julkunen I. 2010. High frequency of cross-reacting antibodies against 2009 pandemic influenza A(H1N1) virus among the elderly in Finland. Euro Surveill 15(5):pii<19478.
33. Fisman DN, Savage R, Gubbay J, Achonu C, Akwar H, Farrell DJ, Crow-croft NS, Jackson P. 2009. Older age and a reduced likelihood of 2009 H1N1 virus infection. N Engl J Med 361:2000–2001. https://doi.org/10.1056/NEJMc0907256.
34. Jacobs JH, Archer BN, Baker MG, Cowling BJ, Heffernan RT, Mercer G, Uez O, Hanshaoworakul W, Viboud C, Schwartz J, Tchetgen Tchetgen E, Lipsitch M. 2012. Searching for sharp drops in the incidence of pandemic A/H1N1 influenza by single year of age. PLoS One 7:e42328. https://doi.org/10.1371/journal.pone.0042328.
35. Medina RA, Stertz S, Manicassamy B, Zimmermann P, Sun X, Albrecht RA, Uusi-Kerttula H, Zagordi O, Belshe RB, Frey SE, Tumpey TM, García-Sastre A. 2013. Glycosylations in the globular head of the hemagglutinin protein modulate the virulence and antigenic properties of the H1N1 influenza viruses. Sci Transl Med 5:187ra70. https://doi.org/10.1126/scitranslmed.3005996.
36. Cobey S, Hensley SE. 2017. Immune history and influenza virus susceptibility. Curr Opin Virol 22:105–111. https://doi.org/10.1016/j.coviro.2016.12.004.
37. Reber A, Katz J. 2013. Immunological assessment of influenza vaccines and immune correlates of protection. Expert Rev Vaccines 12:519–536. https://doi.org/10.1586/erv.13.35.
38. Girard MP, Tam JS, Assossou OM, Kieny MP. 2010. The 2009 A (H1N1) influenza virus pandemic: a review. Vaccine 28:4895– 4902. https://doi.org/10.1016/j.vaccine.2010.05.031.
39. Krammer F, Palese P. 2015. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 14:167–182. https://doi.org/10.1038/nrd4529.
40. Gostic KM, Ambrose M, Worobey M, Lloyd-Smith JO. 2016. Potent protection against H5N1 and H7N9 influenza via childhood hemagglutinin imprinting. Science 354:722–726. https://doi.org/10.1126/science.aag1322.
41. Rau R, Bohk C, Muszynska M, Vaupel J. 2013. Rates of mortality improvement on the Lexis surface: visualizing age-, period-, and cohort-effects. Population Association of America, Washington, DC.
42. Acosta E, Miller M, Hallman S, Bourbeau R, Herring DA, Dillon L, Earn D, Madrenas J, Gagnon A. 2016. Determinants of influenza mortality trends: early-life exposure to influenza and age-period-cohort analysis of influenza mortality in U.S. 1959–2012. Population Association of America, Washington, DC.
43. Lemaitre M, Carrat F, Rey G, Miller M, Simonsen L, Viboud C. 2012. Mortality burden of the 2009 A/H1N1 influenza pandemic in France: comparison to seasonal influenza and the A/H3N2 pandemic. PLoS One 7:e45051. https://doi.org/10.1371/journal.pone.0045051.
44. Thompson WW, Weintraub E, Dhankhar P, Cheng P-Y, Brammer L, Meltzer MI, Bresee JS, Shay DK. 2009. Estimates of US influenza-associated deaths made using four different methods. Influenza Other Respir Viruses 3:37–49. https://doi.org/10.1111/j.1750-2659.2009.00073.x.
45. Hilbe JM. 2011. Negative binomial regression, 2nd ed. Cambridge University Press, Cambridge, United Kingdom.
46. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K. 2003. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289:179–186. https://doi.org/10.1001/jama.289.2.179.
47. Simonsen L, Viboud C, Taylor RJ, Miller MA. 2011. The epidemiology of influenza and its control, p 27–54. In Rappuoli R, Del Giudice G (ed), Influenza vaccines for the future. Springer, Basel, Switzerland.
48. Jayasundara K, Soobiah C, Thommes E, Tricco AC, Chit A. 2014. Natural attack rate of influenza in unvaccinated children and adults: a meta-regression analysis. BMC Infect Dis 14:670. https://doi.org/10.1186/s12879-014-0670-5.
49. Van Kerkhove MD, Hirve S, Koukounari A, Mounts AW, H1N1pdm Serol-ogy Working Group. 2013. Estimating age-specific cumulative incidence for the 2009 influenza pandemic: a meta-analysis of A(H1N1)pdm09 serological studies from 19 countries. Influenza Other Respir Viruses 7:872–886. https://doi.org/10.1111/irv.12074.
50. Mossong J, Hens N, Jit M, Beutels P, Auranen K, Mikolajczyk R, Massari M, Salmaso S, Tomba GS, Wallinga J, Heijne J, Sadkowska-Todys M, Rosinska M, Edmunds WJ. 2008. Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med 5:e74. https://doi.org/10.1371/journal.pmed.0050074.
51. Skowronski DM, Moser FS, Janjua NZ, Davoudi B, English KM, Purych D, Petric M, Pourbohloul B. 2013. H3N2v and other influenza epidemic risk based on age-specific estimates of sero-protection and contact network interactions. PLoS One 8:e54015. https://doi.org/10.1371/journal.pone.0054015.
52. Gambhir M, Swerdlow DL, Finelli L, Van Kerkhove MD, Biggerstaff M, Cauchemez S, Ferguson NM. 2013. Multiple contributory factors to the age distribution of disease cases: a modeling study in the context of influenza A(H3N2v). Clin Infect Dis 57(Suppl 1):S23–S27. https://doi.org/10.1093/cid/cit298.
53. Molinari N-AM, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM, Weintraub E, Bridges CB. 2007. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25:5086–5096. https://doi.org/10.1016/j.vaccine.2007.03.046.
54. Johnson BF, Wilson LE, Ellis J, Elliot AJ, Barclay WS, Pebody RG, McMenamin J, Fleming DM, Zambon MC. 2009. Fatal cases of influenza A in childhood. PLoS One 4:e7671. https://doi.org/10.1371/journal.pone.0007671.
55. Reed C, Katz JM, Hancock K, Balish A, Fry AM, H1N1 Serosurvey Working Group. 2012. Prevalence of seropositivity to pandemic influenza A/H1N1 virus in the United States following the 2009 pandemic. PLoS One 7:e48187. https://doi.org/10.1371/journal.pone.0048187.