Multidrug resistant 2009 a/h1n1 influenza clinical isolate with a neuraminidase i223r mutation retains its virulence and transmissibility in ferrets

PLoS Pathogens

Volumn 7, Issue 9, 2011, Pages

  van der Vries, Erhard ^a   Kroeze, Edwin J ^b   Stittelaar, Koert J ^a,b   Linster, Martin ^a   van der Linden, Anne ^a   Schrauwen, Eefje J A ^a   Leijten, Lonneke M ^a   van Amerongen, Geert ^a   Schutten, Martin ^a   Kuiken, Thijs ^a   Osterhaus, Albert D M E ^a,b   Fouchier, Ron A M ^a   Boucher, Charles A B ^a   Herfst, Sander ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b Viroclinics Biosciences BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; ISOLEUCINE; OSELTAMIVIR; PERAMIVIR; ZANAMIVIR; SIALIDASE;

2009 H1N1 INFLUENZA; AEROSOL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRAIN; CROSS RESISTANCE; FERRET; IN VITRO STUDY; INFLUENZA VIRUS A H1N1; INOCULATION; LUNG ALVEOLITIS; LUNG LESION; MULTIDRUG RESISTANCE; MUTATION; NONHUMAN; PATHOGENESIS; VIRUS ISOLATION; VIRUS MUTANT; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION; VIRUS VIRULENCE; WEIGHT REDUCTION; ANIMAL; CELL LINE; DISEASE MODEL; DISEASE TRANSMISSION; DOG; ENZYMOLOGY; GENETICS; HUMAN; INFLUENZA; METABOLISM; ORTHOMYXOVIRUS INFECTION; PANDEMIC; PATHOGENICITY;

ANIMALIA; MUSTELA; ORTHOMYXOVIRIDAE;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DOGS; DRUG RESISTANCE, MULTIPLE, VIRAL; FERRETS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; MUTATION; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; PANDEMICS;

EID: 80053440951     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002276     Document Type: Article

References (38)

1. Monto AS, (2003) The role of antivirals in the control of influenza. Vaccine 21: 1796-1800.
2. Bautista E, Chotpitayasunondh T, Gao Z, Harper SA, Shaw M, et al. (2010) Clinical aspects of pandemic 2009 influenza A (H1N1) virus infection. N Engl J Med 362: 1708-1719.
3. Lee VJ, Yap J, Cook AR, Chen MI, Tay JK, et al. (2010) Oseltamivir ring prophylaxis for containment of 2009 H1N1 influenza outbreaks. N Engl J Med 362: 2166-2174.
4. Dominguez-Cherit G, Lapinsky SE, Macias AE, Pinto R, Espinosa-Perez L, et al. (2009) Critically Ill patients with 2009 influenza A(H1N1) in Mexico. JAMA 302: 1880-1887.
5. WHO, (2011) Update on oseltamivir resistance to influenza H1N1 (2009) viruses. Geneva World Health Organisation http://www.who.int/csr/disease/influenza/2011_07_15_weekly_web_update_oseltamivir_resistance.pdf.
6. Harvala H, Gunson R, Simmonds P, Hardie A, Bennett S, et al. (2010) The emergence of oseltamivir-resistant pandemic influenza A (H1N1) 2009 virus amongst hospitalised immunocompromised patients in Scotland, November-December, 2009. Euro Surveill 15: pii: 19536.
7. Gaur AH, Bagga B, Barman S, Hayden R, Lamptey A, et al. (2010) Intravenous zanamivir for oseltamivir-resistant 2009 H1N1 influenza. N Engl J Med 362: 88-89.
8. Monto AS, McKimm-Breschkin JL, Macken C, Hampson AW, Hay A, et al. (2006) Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3 years of their use. Antimicrob Agents Chemother 50: 2395-2402.
9. Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, et al. (2004) Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364: 759-765.
10. Hauge SH, Dudman S, Borgen K, Lackenby A, Hungnes O, (2009) Oseltamivir-resistant influenza viruses A (H1N1), Norway, 2007-08. Emerg Infect Dis 15: 155-162.
11. Meijer A, Lackenby A, Hungnes O, Lina B, van-der-Werf S, et al. (2009) Oseltamivir-resistant influenza virus A (H1N1), Europe, 2007-08 season. Emerg Infect Dis 15: 552-560.
12. Ives JA, Carr JA, Mendel DB, Tai CY, Lambkin R, et al. (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. Antiviral Res 55: 307-317.
13. Herlocher ML, Carr J, Ives J, Elias S, Truscon R, et al. (2002) Influenza virus carrying an R292K mutation in the neuraminidase gene is not transmitted in ferrets. Antiviral Res 54: 99-111.
14. Carr J, Ives J, Kelly L, Lambkin R, Oxford J, et al. (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. Antiviral Res 54: 79-88.
15. van der Vries E, van den Berg B, Schutten M, (2008) Fatal oseltamivir-resistant influenza virus infection. N Engl J Med 359: 1074-1076.
16. Baz M, Abed Y, Simon P, Hamelin ME, Boivin G, (2010) Effect of the 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.
17. Bouvier NM, Lowen AC, Palese P, (2008) Oseltamivir-resistant influenza A viruses are transmitted efficiently among guinea pigs by direct contact but not by aerosol. J Virol 82: 10052-10058.
18. Bloom JD, Gong LI, Baltimore D, (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272-1275.
19. Collins PJ, Haire LF, Lin YP, Liu J, Russell RJ, et al. (2009) Structural basis for oseltamivir resistance of influenza viruses. Vaccine 27: 6317-6323.
20. Duan S, Boltz DA, Seiler P, Li J, Bragstad K, et al. (2010) Oseltamivir-resistant pandemic H1N1/2009 influenza virus possesses lower transmissibility and fitness in ferrets. PLoS Pathog 6: e1001022.
21. Hamelin ME, Baz M, Abed Y, Couture C, Joubert P, 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.
22. Kiso M, Shinya K, Shimojima M, Takano R, Takahashi K, et al. (2010) Characterization of oseltamivir-resistant 2009 H1N1 pandemic influenza A viruses. PLoS Pathog 6: e1001079.
23. Memoli MJ, Davis AS, Proudfoot K, Chertow DS, Hrabal RJ, et al. (2011) Multidrug-resistant 2009 pandemic influenza A(H1N1) viruses maintain fitness and transmissibility in ferrets. J Infect Dis 203: 348-357.
24. Seibert CW, Kaminski M, Philipp J, Rubbenstroth D, Albrecht RA, 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: 11219-11226.
25. van der Vries E, Stelma FF, Boucher CA, (2010) Emergence of a multidrug-resistant pandemic influenza A (H1N1) virus. N Engl J Med 363: 1381-1382.
26. Nguyen HT, Fry AM, Loveless PA, Klimov AI, Gubareva LV, (2010) Recovery of a multidrug-resistant strain of pandemic influenza A 2009 (H1N1) virus carrying a dual H275Y/I223R mutation from a child after prolonged treatment with oseltamivir. Clin Infect Dis 51: 983-984.
27. Munster VJ, de Wit E, van den Brand JM, Herfst S, Schrauwen EJ, et al. (2009) Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 325: 481-483.
28. Squires B, Macken C, Garcia-Sastre A, Godbole S, Noronha J, et al. (2008) BioHealthBase: informatics support in the elucidation of influenza virus host pathogen interactions and virulence. Nucleic Acids Res 36: D497-503.
29. van den Brand JM, Stittelaar KJ, van Amerongen G, Rimmelzwaan GF, Simon J, et al. (2010) Severity of pneumonia due to new H1N1 influenza virus in ferrets is intermediate between that due to seasonal H1N1 virus and highly pathogenic avian influenza H5N1 virus. J Infect Dis 201: 993-999.
30. Centers for Disease C, Prevention (2009) Oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infection in two summer campers receiving prophylaxis--North Carolina, 2009. MMWR Morb Mortal Wkly Rep 58: 969-972.
31. Hurt A, Lee R, Leang S, Cui L, Deng Y, et al. (2011) Increased detection in Australia and Singapore of a novel influenza A(H1N1)2009 variant with reduced oseltamivir and zanamivir sensitivity due to a S247N neuraminidase mutation. Euro Surveill 16: pii: 19884.
32. Herfst S, Chutinimitkul S, Ye J, de Wit E, Munster VJ, et al. (2010) Introduction of virulence markers in PB2 of pandemic swine-origin influenza virus does not result in enhanced virulence or transmission. J Virol 84: 3752-3758.
33. McCaw JM, Arinaminpathy N, Hurt AC, McVernon J, McLean AR, (2011) A mathematical framework for estimating pathogen transmission fitness and inoculum size using data from a competitive mixtures animal model. PLoS Comput Biol 7: e1002026.
34. Schrauwen EJ, Herfst S, Chutinimitkul S, Bestebroer TM, Rimmelzwaan GF, et al. (2011) Possible increased pathogenicity of pandemic (H1N1) 2009 influenza virus upon reassortment. Emerg Infect Dis 17: 200-208.
35. Matrosovich M, Matrosovich T, Carr J, Roberts NA, Klenk HD, (2003) Overexpression of the alpha-2,6-sialyltransferase in MDCK cells increases influenza virus sensitivity to neuraminidase inhibitors. J Virol 77: 8418-8425.
36. de Wit E, Spronken MI, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, et al. (2004) Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res 103: 155-161.
37. Karber G, (1931) Beitrag zur kollektiven behandlung pharmakologischer reihenversuche. Exp Pathol Pharmakol 162: 480-483.
38. Fouchier RA, Bestebroer TM, Herfst S, Van Der Kemp L, Rimmelzwaan GF, et al. (2000) Detection of influenza A viruses from different species by PCR amplification of conserved sequences in the matrix gene. J Clin Microbiol 38: 4096-4101.