The global spread of drug-resistant influenza

Journal of the Royal Society Interface

Volumn 9, Issue 69, 2012, Pages 648-656

  Chao, Dennis L ^a   Bloom, Jesse D ^a   Kochin, Beth F ^b   Antia, Rustom ^b   Longini, Ira M ^a,c  

^a Fred Hutchinson Cancer Research Center   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Antiviral agents; Influenza; Mathematical model

Indexed keywords

ANTIVIRAL AGENTS; STOCHASTIC MODELS; STOCHASTIC SYSTEMS;

ANTI-VIRAL DRUGS; ANTIVIRAL TREATMENTS; ANTIVIRALS; DETERMINISTIC APPROXIMATION; INFLUENZA; INFLUENZA A; MODEL APPROXIMATIONS; OSELTAMIVIR; RESISTANT STRAINS; STOCHASTIC SIMULATION MODEL;

VIRUSES;

OSELTAMIVIR;

ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; DRUG EXPOSURE; GENE MUTATION; HUMAN; INFECTION CONTROL; INFLUENZA; INFLUENZA A (H1N1); NONHUMAN; REVIEW; SEASONAL INFLUENZA; SEASONAL VARIATION; SELECTIVE SWEEP; STOCHASTIC MODEL; VIRAL GENETICS; VIRUS TRANSMISSION;

EID: 84856559560     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2011.0427     Document Type: Review

References (40)

1. Ferguson, N. M., Cummings, D. A. T., Cauchemez, S., Fraser, C., Riley, S., Meeyai, A., Iamsirithaworn, S. & Burke, D. S. 2005 Strategies for containing an emerging influenza pandemic in Southeast Asia. Nature 437, 209-214. (doi:10.1038/nature04017)
2. Longini Jr, I. M., Nizam, A., Xu, S., Ungchusak, K., Hanshaoworakul, W., Cummings, D. A. T. & Halloran, M. E. 2005 Containing pandemic influenza at the source. Science 309, 1083-1087. (doi:10.1126/science.1115717)
3. Ortiz, J. R., Kamimoto, L., Aubert, R. E., Yao, J., Shay, D. K., Bresee, J. S. & Epstein, R. S. 2008 Oseltamivir prescribing in pharmacy-benefits database, United States, 2004-2005. Emerg. Infect. Dis. 14, 1280-1283. (doi:10.3201/eid1408.080074)
4. Gubareva, L. V., Kaiser, L., Matrosvich, M. N., Soo-Hoo, Y. & Hayden, F. G. 2001 Selection of influenza virus mutants in experimentally infected volunteers treated with oseltamivir. J. Infect. Dis. 183, 523-531. (doi:10.1086/318537)
5. Whitley, R. J., Hayden, F. G., Reisinger, K. S., Young, N., Dutkowski, R., Ipe, D., Mills, R. G. & Ward, P. 2001 Oral oseltamivir treatment of influenza in children. Pediatric Infect. Dis. J. 20, 127-133. (doi:10.1097/00006454-200102000-00002)
6. Bouvier, N. M., Lowen, A. C. & Palese, P. 2008 Oseltamivir-resistant influenza A viruses are transmitted efficiently among guinea pigs by direct contact but not by aerosol. J. Virol. 82, 10 052-10 058. (doi:10.1128/JVI.01226- 08)
7. Carr, J., Ives, J., Kelly, L., Lambkin, R., Oxford, J., Mendel, D., Tai, L. & Roberts, N. 2002 Influenza virus carrying neuraminidase with reduced sensitivity to oseltamivir carboxylate has altered properties in vitro and is compromised for infectivity and replicative ability in vivo. Antivir. Res. 54, 79-88. (doi:10.1016/S0166-3542(01)00215-7)
8. Herlocher, M. L., Carr, J., Ives, J., Elias, S., Truscon, R., Roberts, N. & Monto, A. S. 2002 Influenza virus carrying an R292K mutation in the neuraminidase gene is not transmitted in ferrets. Antivir. Res. 54, 99-111. (doi:10.1016/S0166-3542(01)00214-5)
9. Abed, Y., Goyette, N. & Bovin, G. 2004 A reverse genetics study of resistance to neuraminidase inhibitors in an influenza A/H1N1 virus. Antivir. Therapy 9, 577-581. (Pubitemid 39150215)
10. Herlocher, M. L., Truscon, R., Elias, S., Yen, H. L., Roberts, N. A., Ohmit, S. E. & Monto, A. S. 2004 Influenza viruses resistant to the antiviral drug oseltamivir: transmission studies in ferrets. J. Infect. Dis. 190, 1627-1630. (doi:10.1086/424572)
11. Ives, J. A. L., Carr, J. A., Mendel, D. B., Tai, C. Y., Lambkin, R., Kelly, L., Oxford, J. S., Hayden, F. G. & Roberts, N. A. 2002 The H274Y mutation in the influenza A/H1N1 neuraminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo. Antivir. Res. 55, 307-317. (doi:10.1016/S0166-3542(02)00053-0)
12. Baranovich, T. et al. 2010 Emergence of H274Y oseltamivir-resistant A(H1N1) influenza viruses in Japan during the 2008-2009 season. J. Clin. Virol. 47, 23-28. (doi:10.1016/j.jcv.2009.11.003)
13. Moscona, A. 2009 Global transmission of oseltamivir-resistant influenza. N Engl. J. Med. 360, 953-956. (doi:10.1056/NEJMp0900648)
14. Baz, M., Abed, Y., Simon, P., Hamelin, M. E. & Boivin, G. Effect of neuraminidase mutation H274Y conferring resistance to oseltamivir on the replicative capacity and virulence of old and recent human influenza A(H1N1) viruses. J. Infect. Dis. 201, 740-745. (doi:10.1086/650464)
15. Matsuzaki, Y. et al. 2010 A two-year survey of the oseltamivir-resistant influenza A(H1N1) virus in Yamagata, Japan and the clinical effectiveness of oseltamivir and zanamavir. Virol. J. 7, 53. (doi:10.1186/1743-422X-7-53)
16. Rameix-Welti, M.-A., Enouf, V., Cuvelier, F., Jeannin, P. & van der Werf, S. 2008 Enzymatic properties of the neuraminidase of seasonal H1N1 influenza viruses provide insights for the emergence of natural resistance to oseltamivir. PLoS Pathog. 4, e1000103. (doi:10.1371/journal.ppat.1000103)
17. Bloom, J. D., Gong, L. I. & Baltimore, D. 2010 Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328, 1272-1275. (doi:10.1126/science.1187816)
18. Kramarz, P., Monnet, D., Nicoll, A., Yilmaz, C. & Ciancio, B. 2009 Use of oseltamivir in 12 European countries between 2002 and 2007-lack of association with the appearance of oseltamivir-resistant influenza A(H1N1) viruses. Euro. Surveill. 14, 19112.
19. Kenah, E., Chao, D. L., Matrajt, L., Halloran, M. E. & Longini Jr, I. M. 2011 The global transmission and control of influenza. PLoS ONE 6, e19515. (doi:10.1371/journal.pone.0019515)
20. Halloran, M. E., Hayden, F. G., Yang, Y., Longini Jr, I. M. & Monto, A. S. 2007 Antiviral effects on influenza viral transmission and pathogenicity: observations from household-based trials. Am. J. Epidemiol. 165, 212-21. (doi:10.1093/aje/kwj362)
21. Collins, P. J. et al. 2009 Structural basis for oseltamivir resistance of influenza viruses. Vaccine 27, 6317-6323. (doi:10.1016/j.vaccine.2009.07.017)
22. Wagner, R., Matrosovich, M. & Klenk, H. D. 2002 Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev. Med. Virol. 12, 159-166. (doi:10.1002/rmv.352)
23. Zaraket, H., Saito, R., Suzuki, Y., Baranovich, T., Dapta, C., Caperig-Dapat, I. & Suzuki, H. 2010 Genetic make-up of amantadine-resistant and oseltamivir-resistant human influenza A/H1N1 viruses. J. Clin. Microbiol. 48, 1085-1092. (doi:10.1128/JCM.01532-09)
24. Simonsen, L. et al. 2007 The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol. Biol. Evol. 24, 1811-1820. (doi:10.1093/molbev/msm103)
25. Niman, H. L. 2009 Emergence and fixing of antiviral resistance in influenza A via recombination and hitch hiking. Nat. Precedings. See http://hdl.handle.net/10101/npre.2009.2832.1.
26. Boni, M. F., Zhou, Y., Taubenberger, J. K. & Holmes, E. C. Homologous recombination is very rare or absent in human influenza A virus. J. Virol. 82, 4807-4811. (doi:10.1128/JVI.02683-07)
27. Meijer, A. et al. 2009 Oseltamivir-resistant influenza virus A (H1N1), Europe, 2007-08 season. Emerg. Infect. Dis. 15, 552-560. (doi:10.3201/eid1504. 081280)
28. zur Wiesch, P. A., Kouyos, R., Engelstädter, J., Regoes, R. R. & Bonhoeffer, S. 2011 Population biological principles of drug-resistance evolution in infectious diseases. Lancet Infect.Dis. 11, 236-47. (doi:10.1016/S1473-3099(10)70264-4)
29. Nelson, M. I., Simonsen, L., Viboud, C., Miller, M. A. & Holmes, E. C. 2007 Phylogenetic analysis reveals the global migration of seasonal influenza A viruses. PLoS Pathog. 3, e0030131. (doi:10.1371/journal.ppat.0030131)
30. Bedford, T., Cobey, S., Beerli, P. & Pascual, M. 2010 Global migration dynamics underlie evolution and persistence of human influenza A (H3N2). PLoS Pathog. 6, e1000918. (doi:10.1371/journal.ppat.1000918)
31. Rambaut, A., Pybus, O. G., Nelson, M. I., Viboud, C., Taubenberger, J. K. & Holmes, E. C. 2008 The genomic and epidemiological dynamics of human influenza A virus. Nature 453, 615-619. (doi:10.1038/nature06945)
32. Plotkin, J. B., Dushoff, J. & Levin, S. A. 2002 Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc. Natl Acad. Sci. USA 99, 6263-6268. (doi:10.1073/pnas.082110799)
33. Smith, D. J., Lapedes, A. S., de Jong, J. C., Bestebroer, T. M., Rimmelzwaan, G. F., Osterhaus, A. D. M. E. & Fouchier, R. A. M. 2004 Mapping the antigenic and genetic evolution of influenza virus. Science 305, 371-376. (doi:10.1126/science.1097211)
34. World Health Organization. 2011 Update on oseltamivir resistance in influenza A(H1N1) 2009 viruses: 15 June 2011. See http://www.who.int/entity/csr/ disease/influ enza/2011-06-17-weekly-web-update-oseltamivir-resistance.pdf (accessed on June 19 2011).
35. Brookes, D. W., Miah, S., Lackenby, A., Hartgroves, L. & Barclay, W. S. 2011 Pandemic H1N1 2009 influenza virus with the H275Y oseltamivir resistance neuraminidase mutation shows a small compromise in enzyme activity and viral fitness. J. Antimicrob. Chemother. 66, 466-70. (doi:10.1093/jac/dkq486)
36. Duan, S., Boltz, D. A., Seiler, P., Li, J., Bragstad, K., Nielsen, L. P.,Webby, R. J.,Webster, R. G. & Govorkova, E. A. 2010 Oseltamivir-resistant pandemic H1N1/2009 influenza virus possesses lower transmissibility and fitness in ferrets. PLoS Pathog. 6, e1001022. (doi:10.1371/journal.ppat.1001022)
37. Hamelin, M.-È. et al. 2010 Oseltamivir-resistant pandemic A/H1N1 virus is as virulent as its wild-type counterpart in mice and ferrets. PLoS Pathog. 6, e1001015. (doi:10.1371/journal.ppat.1001015)
38. Pizzorno, A., Bouhy, Z., Abed, Y. & Boivin, G. 2011 Generation and characterization of recombinant pandemic influenza A(H1N1) viruses resistant to neuraminidase inhibitors. J. Infect. Dis. 203, 25-31. (doi:10.1093/infdis/ jiq010)
39. Seibert, C. W. et al. 2010 Oseltamivir-resistant variants of the 2009 pandemic H1N1 influenza A virus are not attenuated in the guinea pig and ferret transmission models. J. Virol. 84, 11 219-11 226. (doi:10.1128/JVI.01424-10)
40. Kiso, M. et al. 2010 Characterization of oseltamivir-resistant 2009 H1N1 pandemic influenza A viruses. PLoS Pathog. 6, e1001079. (doi:10.1371/journal. ppat.1001079)