Prior population immunity reduces the expected impact of CTL-inducing vaccines for pandemic influenza control

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Bolton, Kirsty J ^a   McCaw, James M ^b,c   Brown, Lorena ^d   Jackson, David ^d   Kedzierska, Katherine ^d   McVernon, Jodie ^b,c  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS REACTING ANTIBODY; INFLUENZA VACCINE;

ARTICLE; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; DISEASE CONTROL; DISEASE TRANSMISSION; DRUG EFFICACY; HUMAN; INFLUENZA VIRUS A; INFLUENZA VIRUS A H7N9; NONHUMAN; PANDEMIC INFLUENZA; VACCINATION; VIRUS STRAIN; ALGORITHM; IMMUNITY; IMMUNOLOGY; INFLUENZA A VIRUS; INFLUENZA, HUMAN; PANDEMIC; STATISTICAL MODEL;

INFLUENZA A VIRUS; SUIDAE;

ALGORITHMS; HUMANS; IMMUNITY; INFLUENZA A VIRUS; INFLUENZA VACCINES; INFLUENZA, HUMAN; MODELS, STATISTICAL; PANDEMICS; T-LYMPHOCYTES, CYTOTOXIC; VACCINATION;

EID: 84926299762     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120138     Document Type: Article

References (86)

1. Osterholm MT, Kelley NS, Sommer A, Belongia EA. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis. 2012 Jan; 12(1):36-44. Available from: http://dx.doi.org/10.1016/S1473-3099(11)70295-X
2. Manzoli L, Ioannidis JPA, Flacco ME, De Vito C, Villari P. Effectiveness and harms of seasonal and pandemic influenza vaccines in children, adults and elderly: a critical review and re-analysis of 15 meta-analyses. Hum Vaccin Immunother. 2012 Jul; 8(7):851-862. Available from: 10.4161/hv.19917 PMID: 22777099
3. Neuzil KM, Jackson LA, Nelson J, Klimov A, Cox N, Bridges CB, et al. Immunogenicity and reactogenicity of 1 versus 2 doses of trivalent inactivated influenza vaccine in vaccine-naive 5-8-year-old children. J Infect Dis. 2006 Oct; 194(8):1032-1039. Available from: http://dx.doi.org/10.1086/507309 PMID: 16991077
4. Skowronski DM, De Serres G, Crowcroft NS, Janjua NZ, Boulianne N, Hottes TS, et al. Association between the 2008-09 seasonal influenza vaccine and pandemic H1N1 illness during Spring-Summer 2009: four observational studies from Canada. PLoS Med. 2010 Apr; 7(4):e1000258. Available from: http://dx.doi.org/10.1371/journal.pmed.1000258 PMID: 20386731
5. Cowling BJ, Ng S, Ma ESK, Cheng CKY, Wai W, Fang VJ, et al. Protective efficacy of seasonal influenza vaccination against seasonal and pandemic influenza virus infection during 2009 in Hong Kong. Clin Infect Dis. 2010 Dec; 51(12):1370-1379. Available from: http://dx.doi.org/10.1086/657311 PMID: 21067351
6. McVernon J, Laurie K, Barr I, Kelso A, Skeljo M, Nolan T. Absence of cross-reactive antibodies to influenza A (H1N1) 2009 before and after vaccination with 2009 Southern Hemisphere seasonal trivalent influenza vaccine in children aged 6 months-9 years: a prospective study. Influenza Other Respi Viruses. 2011 Jan; 5(1):7-11. Available from: http://dx.doi.org/10.1111/j.1750-2659.2010.00172.x
7. Hardelid P, Fleming DM, McMenamin J, Andrews N, Robertson C, SebastianPillai P, et al. Effectiveness of pandemic and seasonal influenza vaccine in preventing pandemic influenza A(H1N1)2009 infection in England and Scotland 2009-2010. Euro Surveill. 2011; 16(2).
8. Leung GM, Nicoll A. Reflections on pandemic (H1N1) 2009 and the international response. PLoS Med. 2010; 7(10). Available from: 10.1371/journal.pmed.1000346
9. Maines TR, Chen LM, Matsuoka Y, Chen H, Rowe T, Ortin J, et al. Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci U S A. 2006 Aug; 103 (32):12121-12126. Available from: 10.1073/pnas.0605134103 PMID: 16880383.
10. Steel J, Staeheli P, Mubareka S, García-Sastre A, Palese P, Lowen AC. Transmission of pandemic H1N1 influenza virus and impact of prior exposure to seasonal strains or interferon treatment. J Virol. 2010 Jan; 84(1):21-26. Available from: 10.1128/JVI.01732-09 PMID: 19828604
11. McMichael A, Gotch F, Noble G, Beare P. Cytotoxic T-cell immunity to influenza. N Engl J Med. 1983 Jul; 309(1):13-7. Available from: 10.1056/NEJM198307073090103 PMID: 6602294
12. Wilkinson TM, Li CKF, Chui CSC, Huang AKY, Perkins M, Liebner JC, et al. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med. 2012 Feb; 18(2):274-280. Available from: 10.1038/nm.2612 PMID: 22286307
13. Groot ASD, Ardito M, McClaine EM, Moise L, Martin WD. Immunoinformatic comparison of T-cell epitopes contained in novel swine-origin influenza A (H1N1) virus with epitopes in 2008-2009 conventional influenza vaccine. Vaccine. 2009 Sep; 27(42):5740-5747. Available from: 10.1016/j.vaccine.2009.07.040 PMID: 19660593
14. Gras S, Kedzierski L, Valkenburg SA, Laurie K, Liu YC, Denholm JT, et al. Cross-reactive CD8+ T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proc Natl Acad Sci U S A. 2010 Jul; 107(28):12599-12604. Available from: 10.1073/pnas.1007270107 PMID: 20616031
15. Tu W, Mao H, Zheng J, Liu Y, Chiu SS, Qin G, et al. Cytotoxic T lymphocytes established by seasonal human influenza cross-react against 2009 pandemic H1N1 influenza virus. J Virol. 2010 Jul; 84 (13):6527-6535. Available from: 10.1128/JVI.00519-10 PMID: 20410263
16. McMichael AJ, Gotch FM, Dongworth DW, Clark A, Potter CW. Declining T-cell immunity to influenza, 1977-82. Lancet. 1983 Oct; 2(8353):762-764. doi: 10.1016/S0140-6736(83)92297-3 PMID: 6137602
17. Sridhar S, Begom S, Bermingham A, Hoschler K, Adamson W, Carman W, et al. Cellular immune correlates of protection against symptomatic pandemic influenza. Nat Med. 2013 Sep; 19:1305-1312. Available from: 10.1038/nm.3350 PMID: 24056771
18. Epstein SL. Prior H1N1 influenza infection and susceptibility of Cleveland Family Study participants during the H2N2 pandemic of 1957: an experiment of nature. J Infect Dis. 2006 Jan; 193(1):49-53. Available from: 10.1086/498980 PMID: 16323131
19. McElhaney JE, Xie D, Hager WD, Barry MB, Wang Y, Kleppinger A, et al. T cell responses are better correlates of vaccine protection in the elderly. J Immunol. 2006 May; 176(10):6333-6339. doi: 10.4049/jimmunol.176.10.6333 PMID: 16670345
20. Brown LE, Kelso A. Prospects for an influenza vaccine that induces cross-protective cytotoxic T lymphocytes. Immunol Cell Biol. 2009; 87(4):300-308. Available from: 10.1038/icb.2009.16 PMID: 19308073
21. Lee LYH, Ha DLA, Simmons C, de Jong MD, Chau NVV, Schumacher R, et al. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J Clin Invest. 2008 Oct; 118(10):3478-3490. Available from: 10.1172/JCI32460 PMID: 18802496
22. Scheible K, Zhang G, Baer J, Azadniv M, Lambert K, Pryhuber G, et al. CD8+ T cell immunity to 2009 pandemic and seasonal H1N1 influenza viruses. Vaccine. 2011 Mar; 29(11):2159-2168. Available from: 10.1016/j.vaccine.2010.12.073 PMID: 21211588
23. Wagar LE, Rosella L, Crowcroft N, Lowcock B, Drohomyrecky PC, Foisy J, et al. Humoral and cell-mediated immunity to pandemic H1N1 influenza in a Canadian cohort one year post-pandemic: implications for vaccination. PLoS One. 2011; 6(11):e28063. Available from: 10.1371/journal.pone.0028063 PMID: 22132212
24. Skowronski DM, Hottes TS, McElhaney JE, Janjua NZ, Sabaiduc S, Chan T, 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 Jan; 203(2):158-167. Available from: 10.1093/infdis/jiq039 PMID: 21288814
25. Valkenburg SA, Gras S, Guillonneau C, Gruta NLL, Thomas PG, Purcell AW, et al. Protective efficacy of cross-reactive CD8+ T cells recognising mutant viral epitopes depends on peptide-MHC-I structural interactions and T cell activation threshold. PLoS Pathog. 2010; 6(8):e1001039. Available from: 10.1371/journal.ppat.1001039 PMID: 20711359
26. Berkhoff EGM, de Wit E, Geelhoed-Mieras MM, Boon ACM, Symons J, Fouchier RAM, et al. Functional constraints of influenza A virus epitopes limit escape from cytotoxic T lymphocytes. J Virol. 2005 Sep; 79(17):11239-11246. Available from: 10.1128/JVI.79.17.11239-11246.2005 PMID: 16103176
27. Valkenburg SA, Venturi V, Dang THY, Bird NL, Doherty PC, Turner SJ, et al. Early priming minimizes the age-related immune compromise of CD8 T cell diversity and function. PLoS Pathog. 2012 Feb; 8 (2):e1002544. Available from: 10.1371/journal.ppat.1002544 PMID: 22383879
28. He XS, Holmes TH, Mahmood K, Kemble GW, Dekker CL, Arvin AM, et al. Phenotypic changes in influenza-specific CD8+ T cells after immunization of children and adults with influenza vaccines. J Infect Dis. 2008 Mar; 197(6):803-811. Available from: 10.1086/528804 PMID: 18279048
29. Gruta NLL, Kedzierska K, Pang K, Webby R, Davenport M, Chen W, et al. A virus-specific CD8+ T cell immunodominance hierarchy determined by antigen dose and precursor frequencies. Proc Natl Acad Sci U S A. 2006 Jan; 103(4):994-999. Available from: 10.1073/pnas.0510429103 PMID: 16418289
30. Deliyannis G, Jackson D, Ede N, Zeng W, Hourdakis I, Sakabetis E, et al. Induction of long-term memory CD8(+) T cells for recall of viral clearing responses against influenza virus. J Virol. 2002 May; 76 (9):4212-21. 0022-538X (Print) Journal Article Available from: 10.1128/JVI.76.9.4212-4221.2002 PMID: 11932386
31. Laidlaw BJ, Decman V, Ali MAA, Abt MC, Wolf AI, Monticelli LA, et al. Cooperativity Between CD8+ T Cells, Non-Neutralizing Antibodies, and Alveolar Macrophages Is Important for Heterosubtypic Influenza Virus Immunity. PLoS Pathog.2013 Mar; 9(3):e1003207. Available from: 10.1371/journal.ppat.1003207 PMID: 23516357
32. Kedzierska K, Gruta NLL, Turner SJ, Doherty PC. Establishment and recall of CD8+ T-cell memory in a model of localized transient infection. Immunol Rev. 2006 Jun; 211:133-145. Available from: 10.1111/j.0105-2896.2006.00386.x PMID: 16824123
33. Christensen JP, Doherty PC, Branum KC, Riberdy JM. Profound protection against respiratory challenge with a lethal H7N7 influenza A virus by increasing the magnitude of CD8(+) T-cell memory. J Virol. 2000 Dec; 74(24):11690-11696. doi: 10.1128/JVI.74.24.11690-11696.2000 PMID: 11090168
34. Ng WC, Gilbertson B, Lim B, Zeng W, Jackson DC, Brown LE. Lipopeptide vaccines illustrate the potential role of subtype-crossreactive T cells in the control of highly virulent influenza. Influenza Other Respi Viruses. 2009 Jul; 3(4):177-182. Available from: 10.1111/j.1750-2659.2009.00087.x
35. Tan ACL, Deliyannis G, Bharadwaj M, Brown LE, Zeng W, Jackson DC. The design and proof of concept for a CD8(+) T cell-based vaccine inducing cross-subtype protection against influenza A virus. Immunol Cell Biol. 2013 Jan; 91(1):96-104. Available from: 10.1038/icb.2012.54 PMID: 23146941
36. Tan ACL, Mifsud EJ, Zeng W, Edenborough K, McVernon J, Brown LE, et al. Intranasal administration of the TLR2 agonist Pam2Cys provides rapid protection against influenza in mice. Mol Pharm. 2012 Sep; 9(9):2710-2718. Available from: 10.1021/mp300257x PMID: 22823162
37. Ulmer JB, Donnelly JJ, Parker SE, Rhodes GH, Felgner PL, Dwarki VJ, et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science. 1993 Mar; 259(5102):1745-1749. doi: 10.1126/science.8456302 PMID: 8456302
38. Fu TM, Friedman A, Ulmer JB, Liu MA, Donnelly JJ. Protective cellular immunity: cytotoxic T-lymphocyte responses against dominant and recessive epitopes of influenza virus nucleoprotein induced by DNA immunization. J Virol. 1997 Apr; 71(4):2715-2721. PMID: 9060624
39. He XS, Holmes TH, Zhang C, Mahmood K, Kemble GW, Lewis DB, et al. Cellular immune responses in children and adults receiving inactivated or live attenuated influenza vaccines. J Virol. 2006 Dec; 80 (23):11756-11766. Available from: 10.1128/JVI.01460-06 PMID: 16971435
40. Nguyen HH, Moldoveanu Z, Novak MJ, van Ginkel FW, Ban E, Kiyono H, et al. Heterosubtypic Immunity to Lethal Influenza A Virus Infection Is Associated with Virus-Specific CD8+Cytotoxic T Lymphocyte Responses Induced in Mucosa-Associated Tissues. Virology. 1999; 254(1):50-60. Available from: 10.1006/viro.1998.9521 PMID: 9927573
41. Zhu FC, Wang H, Fang HH, Yang JG, Lin XJ, Liang XF, et al. A Novel Influenza A (H1N1) Vaccine in Various Age Groups. N Engl J Med. 2009 Oct;Available from: 10.1056/NEJMoa0908535
42. Berthoud TK, Hamill M, Lillie PJ, Hwenda L, Collins KA, Ewer KJ, et al. Potent CD8+ T-cell immunogenicity in humans of a novel heterosubtypic influenza A vaccine, MVA-NP+M1. Clin Infect Dis. 2011 Jan; 52(1):1-7. Available from: 10.1093/cid/ciq015 PMID: 21148512
43. Antrobus RD, Lillie PJ, Berthoud TK, Spencer AJ, McLaren JE, Ladell K, et al. A T Cell-Inducing Influenza Vaccine for the Elderly: Safety and Immunogenicity of MVA-NP+M1 in Adults Aged over 50 Years. PLoS One. 2012; 7(10):e48322. Available from: 10.1371/journal.pone.0048322 PMID: 23118984
44. Lillie PJ, Berthoud TK, Powell TJ, Lambe T, Mullarkey C, Spencer AJ, et al. Preliminary assessment of the efficacy of a T-cell-based influenza vaccine, MVA-NP+M1, in humans. Clin Infect Dis. 2012 Jul; 55 (1):19-25. Available from: 10.1093/cid/cis327 PMID: 22441650
45. Price GE, Soboleski MR, Lo CY, Misplon JA, Quirion MR, Houser KV, et al. Single-dose mucosal immunization with a candidate universal influenza vaccine provides rapid protection from virulent H5N1, H3N2 and H1N1 viruses. PLoS One. 2010; 5(10):e13162. Available from: 10.1371/journal.pone.0013162 PMID: 20976273
46. Arinaminpathy N, Ratmann O, Koelle K, Epstein SL, Price GE, Viboud C, et al. Impact of cross-protective vaccines on epidemiological and evolutionary dynamics of influenza. Proc Natl Acad Sci U S A. 2012 Feb; 109(8):3173-3177. Available from: 10.1073/pnas.1113342109 PMID: 22323589
47. Koelle K, Khatri P, Kamradt M, Kepler TB. A two-tiered model for simulating the ecological and evolutionary dynamics of rapidly evolving viruses, with an application to influenza. J R Soc Interface. 2010 Sep; 7(50):1257-1274. Available from: 10.1098/rsif.2010.0007 PMID: 20335193
48. Booy R, Khandaker G, Heron LG, Yin J, Doyle B, Tudo KK, et al. Cross-reacting antibodies against the pandemic (H1N1) 2009 influenza virus in older Australians. Med J Aust. 2011 Jan; 194(1):19-23. PMID: 21449863
49. Wong KK, Greenbaum A, Moll ME, Lando J, Moore EL, Ganatra R, et al. Outbreak of Influenza A (H3N2) Variant Virus Infection among Attendees of an Agricultural Fair, Pennsylvania, USA, 2011. Emerg Infect Dis. 2012 Dec; 18(12):1937-1944. Available from: 10.3201/eid1812.121097 PMID: 23171635
50. Skowronski DM, Janjua NZ, Serres GD, Purych D, Gilca V, Scheifele DW, et al. Cross-reactive and vaccine-induced antibody to emerging swine influenza A(H3N2)v. J Infect Dis. 2012 Aug;Available from: 10.1093/infdis/jis500
51. Kreijtz JHCM, de Mutsert G, van Baalen CA, Fouchier RAM, Osterhaus ADME, Rimmelzwaan GF. Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J Virol. 2008 Jun; 82(11):5161-5166. Available from: 10.1128/JVI.02694-07 PMID: 18353950
52. Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, et al. Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. The Lancet. 2013; 381:1926-1932. doi: 10.1016/S0140-6736(13)60938-1
53. Wearing HJ, Rohani P, Keeling MJ. Appropriate models for the management of infectious diseases. PLoS Med. 2005 Jul; 2(7):e174. Available from: 10.1371/journal.pmed.0020174 PMID: 16013892
54. Lloyd AL. The dependence of viral parameter estimates on the assumed viral life cycle: limitations of studies of viral load data. Proc Biol Sci. 2001 Apr; 268(1469):847-854. Available from: 10.1098/rspb.2000.1572 PMID: 11345331
55. Baguelin M, Hoek AJV, Jit M, Flasche S, White PJ, Edmunds WJ. Vaccination against pandemic influenza A/H1N1v in England: a real-time economic evaluation. Vaccine. 2010 Mar; 28(12):2370-2384. Available from: 10.1016/j.vaccine.2010.01.002 PMID: 20096762
56. Cori A, Valleron AJ, Carrat F, Scalia Tomba G, Thomas G, Boëelle PY. Estimating influenza latency and infectious period durations using viral excretion data. Epidemics. 2012 Aug; 4(3):132-138. Available from: 10.1016/j.epidem.2012.06.001 PMID: 22939310
57. White LF, Wallinga J, Finelli L, Reed C, Riley S, Lipsitch M, et al. Estimation of the reproductive number and the serial interval in early phase of the 2009 influenza A/H1N1 pandemic in the USA. Influenza Other Respi Viruses. 2009 Nov; 3(6):267-276. Available from: 10.1111/j.1750-2659.2009.00106.x
58. Boëelle PY, Ansart S, Cori A, Valleron AJ. Transmission parameters of the A/H1N1 (2009) influenza virus pandemic: a review. Influenza Other Respi Viruses. 2011 Sep; 5(5):306-316. Available from: 10.1111/j.1750-2659.2011.00234.x
59. Levy JW, Cowling BJ, Simmerman JM, Olsen SJ, Fang VJ, Suntarattiwong P, et al. The serial intervals of seasonal and pandemic influenza viruses in households in Bangkok, Thailand. Am J Epidemiol. 2013 Jun; 177(12):1443-1451. Available from: 10.1093/aje/kws402 PMID: 23629874
60. Mossong J, Hens N, Jit M, Beutels P, Auranen K, Mikolajczyk R, et al. Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med. 2008 Mar; 5(3):e74. Available from: 10.1371/journal.pmed.0050074 PMID: 18366252
61. Eames KTD, Tilston NL, Brooks-Pollock E, Edmunds WJ. Measured dynamic social contact patterns explain the spread of H1N1v influenza. PLoS Comput Biol. 2012; 8(3):e1002425. Available from: 10.1371/journal.pcbi.1002425 PMID: 22412366
62. Mathews JD, McCaw CT, McVernon J, McBryde ES, McCaw JM. A biological model for influenza transmission: pandemic planning implications of asymptomatic infection and immunity. PLoS ONE. 2007; 2: e1220. Available from: 10.1371/journal.pone.0001220 PMID: 18043733
63. White LF, Pagano M. Transmissibility of the influenza virus in the 1918 pandemic. PLoS One. 2008; 3 (1):e1498. Available from: 10.1371/journal.pone.0001498 PMID: 18231585
64. Glass K, Kelly H, Mercer GN. Pandemic influenza H1N1: reconciling serosurvey data with estimates of the reproduction number. Epidemiology. 2012 Jan; 23(1):86-94. Available from: 10.1097/EDE.0b013e31823a44a5 PMID: 22089631
65. Jackson C, Vynnycky E, Mangtani P. Estimates of the transmissibility of the 1968 (Hong Kong) influenza pandemic: evidence of increased transmissibility between successive waves. Am J Epidemiol. 2010 Feb; 171(4):465-478. Available from: 10.1093/aje/kwp394 PMID: 20007674
66. McCaw JM, McVernon J, McBryde ES, Mathews JD. Influenza: accounting for prior immunity. Science. 2009 Aug; 325(5944):1071; author reply 1072-1071; author reply 1073 Available from: 10.1126/science.325-1071a PMID: 19713508
67. Viboud C, Grais RF, Lafont BAP, Miller MA, Simonsen L, Group MISMS. Multinational impact of the 1968 Hong Kong influenza pandemic: evidence for a smoldering pandemic. J Infect Dis. 2005 Jul; 192 (2):233-248. doi: 10.1086/431150 PMID: 15962218
68. Yang JR, Huang YP, Chang FY, Hsu LC, Lin YC, Su CH, et al. New variants and age shift to high fatality groups contribute to severe successive waves in the 2009 influenza pandemic in Taiwan. PLoS One. 2011; 6(11):e28288. Available from: 10.1371/journal.pone.0028288 PMID: 22140569
69. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC. The genomic and epidemiological dynamics of human influenza A virus. Nature. 2008 May; 453(7195):615-619. Available from: 10.1038/nature06945 PMID: 18418375
70. Boni M, Gog J, Andreasen V, Feldman M. Epidemic dynamics and antigenic evolution in a single season of influenza As. Proc Biol Sci. 2006 Jun; 273(1592):1307-16. Available from: 10.1098/rspb.2006.3466 PMID: 16777717
71. Koelle K, Cobey S, Grenfell B, Pascual M. Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science. 2006 Dec; 314(5807):1898-903. Available from: 10.1126/science.1132745 PMID: 17185596
72. Volkov I, Pepin KM, Lloyd-Smith JO, Banavar JR, Grenfell BT. Synthesizing within-host and population-level selective pressures on viral populations: the impact of adaptive immunity on viral immune escape. J R Soc Interface. 2010 Sep; 7(50):1311-1318. Available from: 10.1098/rsif.2009.0560 PMID: 20335194
73. Guarnaccia T, Carolan LA, Maurer-Stroh S, Lee RTC, Job E, Reading PC, et al. Antigenic Drift of the Pandemic 2009 A(H1N1) Influenza Virus in a Ferret Model. PLoS Pathog. 2013 May; 9(5):e1003354. Available from: 10.1371/journal.ppat.1003354 PMID: 23671418
74. Weinfurter JT, Brunner K, Capuano SV, Li C, Broman KW, Kawaoka Y, et al. Cross-reactive T cells are involved in rapid clearance of 2009 pandemic H1N1 influenza virus in nonhuman primates. PLoS Pathog. 2011 Nov; 7(11):e1002381. Available from: 10.1371/journal.ppat.1002381 PMID: 22102819
75. Gilligan CA, van den Bosch F. Epidemiological models for invasion and persistence of pathogens. Annu Rev Phytopathol. 2008; 46:385-418. Available from: 10.1146/annurev.phyto.45.062806.094357 PMID: 18680429
76. Goldstein E, Apolloni A, Lewis B, Miller JC, Macauley M, Eubank S, et al. Distribution of vaccine/antivirals and the 'least spread line' in a stratified population. J R Soc Interface. 2009 Oct;Available from: http://dx.doi.org/10.1098/rsif.2009.0393
77. McVernon J, Laurie K, Faddy H, Irving D, Nolan T, Barr I, et al. Seroprevalence of antibody to influenza A(H1N1)pdm09 attributed to vaccination or infection, before and after the second (2010) pandemic wave in Australia. Influenza Other Respir Viruses. 2014 Mar; 8(2):194-200. Available from: 10.1111/irv.12225 PMID: 24382379
78. Miller E, Hoschler K, Hardelid P, Stanford E, Andrews N, Zambon M. Incidence of 2009 pandemic influenza A H1N1 infection in England: a cross-sectional serological study. Lancet. 2010 Mar; 375 (9720):1100-1108. Available from: 10.1016/S0140-6736(09)62126-7 PMID: 20096450
79. Luo S, Reed M, Mattingly JC, Koelle K. The impact of host immune status on the within-host and population dynamics of antigenic immune escape. J R Soc Interface. 2012 Oct; 9(75):2603-2613. Available from: 10.1098/rsif.2012.0180 PMID: 22572027
80. Pepin KM, Riley S, Grenfell BT. Effects of influenza antivirals on individual and population immunity over many epidemic waves. Epidemiol Infect. 2012 Mar;p. 1-11. Available from: http://dx.doi.org/10.1017/S0950268812000477
81. Matrajt L, Halloran ME, Longini IM Jr. Optimal vaccine allocation for the early mitigation of pandemic influenza. PLoS Comput Biol. 2013; 9(3):e1002964. Available from: 10.1371/journal.pcbi.1002964 PMID: 23555207
82. Webby RJ, Webster RG. Emergence of influenza A viruses. Philos Trans R Soc Lond B Biol Sci. 2001 Dec; 356(1416):1817-1828. Available from: 10.1098/rstb.2001.0997 PMID: 11779380
83. Ducatez MF, Webster RG, Webby RJ. Animal influenza epidemiology. Vaccine. 2008 Sep; 26 Suppl 4: D67-D69. doi: 10.1016/j.vaccine.2008.07.064 PMID: 19230163
84. Ellebedy AH, Ahmed R. Re-engaging cross-reactive memory B cells: the influenza puzzle. Front Immunol. 2012; 3:53. Available from: 10.3389/fimmu.2012.00053 PMID: 22566934
85. Alexander DJ. Summary of avian influenza activity in Europe, Asia, Africa, and Australasia, 2002-2006. Avian Dis. 2007 Mar; 51(1 Suppl):161-166. doi: 10.1637/7602-041306R.1 PMID: 17494548
86. Thomas PG, Handel A, Doherty PC, La Gruta NL. Ecological analysis of antigen-specific CTL repertoires defines the relationship between naive and immune T-cell populations. Proc Natl Acad Sci U S A. 2013 Jan; 110(5):1839-1844. Available from: 10.1073/pnas.1222149110 PMID: 23319654