Utilising animal models to evaluate oseltamivir efficacy against influenza A and B viruses with reduced in vitro susceptibility


Autoři: Rubaiyea Farrukee aff001;  Celeste Ming-Kay Tai aff001;  Ding Yuan Oh aff001;  Danielle E. Anderson aff004;  Vithiagaran Gunalan aff005;  Martin Hibberd aff006;  Gary Yuk-Fai Lau aff004;  Ian G. Barr aff001;  Veronika von Messling aff004;  Sebastian Maurer-Stroh aff005;  Aeron C. Hurt aff001
Působiště autorů: WHO Collaborating Centre for Reference and Research on Influenza, VIDRL, at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia aff001;  Department of Microbiology and Immunology, The University of Melbourne, at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia aff002;  School of Health and Life Sciences, Federation University, Churchill, Victoria, Australia aff003;  Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore aff004;  Bioinformatics Institute, Agency for Science, Technology and Research, Singapore, Singapore aff005;  Genome Institute of Singapore, Agency for Science, Technology and Research, Singapore, Singapore aff006;  Veterinary Medicine Division, Paul-Ehrlich-Institute, Federal Institute for Vaccines and Biomedicines, Langen, Germany aff007;  National Public Health Laboratories, National Centre for Infectious Diseases, Ministry of Health, Singapore aff008;  Department of Biological Sciences, National University Singapore, Singapore aff009
Vyšlo v časopise: Utilising animal models to evaluate oseltamivir efficacy against influenza A and B viruses with reduced in vitro susceptibility. PLoS Pathog 16(6): e32767. doi:10.1371/journal.ppat.1008592
Kategorie: Research Article
doi: 10.1371/journal.ppat.1008592

Souhrn

The neuraminidase (NA) inhibitor (NAI) oseltamivir (OST) is the most widely used influenza antiviral drug. Several NA amino acid substitutions are reported to reduce viral susceptibility to OST in in vitro assays. However, whether there is a correlation between the level of reduction in susceptibility in vitro and the efficacy of OST against these viruses in vivo is not well understood. In this study, a ferret model was utilised to evaluate OST efficacy against circulating influenza A and B viruses with a range of in vitro generated 50% inhibitory concentrations (IC50) values for OST. OST efficacy against an A(H1N1)pdm09 and an A(H1N1)pdm09 virus with the H275Y substitution in neuraminidase was also tested in the macaque model. The results from this study showed that OST had a significant impact on virological parameters compared to placebo treatment of ferrets infected with wild-type influenza A viruses with normal IC50 values (~1 nM). However, this efficacy was lower against wild-type influenza B and other viruses with higher IC50 values. Differing pathogenicity of the viruses made evaluation of clinical parameters difficult, although some effect of OST in reducing clinical signs was observed with influenza A(H1N1) and A(H1N1)pdm09 (H275Y) viruses. Viral titres in macaques were too low to draw conclusive results. Analysis of the ferret data revealed a correlation between IC50 and OST efficacy in reducing viral shedding but highlighted that the current WHO guidelines/criteria for defining normal, reduced or highly reduced inhibition in influenza B viruses based on in vitro data are not well aligned with the low in vivo OST efficacy observed for both wild-type influenza B viruses and those with reduced OST susceptibility.

Klíčová slova:

Ferrets – H1N1 – Influenza – Influenza A virus – Influenza B virus – Influenza viruses – Macaque – Viral release


Zdroje

1. Lowen AC, Mubareka S, Tumpey TM, Garcia-Sastre A, Palese P. The guinea pig as a transmission model for human influenza viruses. Proc Natl Acad Sci U S A. 2006;103(26):9988–92. Epub 2006/06/21. doi: 10.1073/pnas.0604157103 16785447; PubMed Central PMCID: PMC1502566.

2. Zaraket H, Saito R. Japanese Surveillance Systems and Treatment for Influenza. Curr Treat Options Infect Dis. 2016;8(4):311–28. doi: 10.1007/s40506-016-0085-5 28035195

3. Koszalka P, Tilmanis D, Hurt AC. Influenza antivirals currently in late-phase clinical trial. Influenza Other Respir Viruses. 2017;11(3):240–6. doi: 10.1111/irv.12446 28146320

4. Itzstein Mv, Wen-Yang W, Kok GB, Pegg MS, Dyason JC, Jin B, et al. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature. 1993;(6428):418. edsgcl.14138960. doi: 10.1038/363418a0 8502295

5. von Itzstein M. The war against influenza: discovery and development of sialidase inhibitors. Nat Rev Drug Discov. 2007;6(12):967–74. doi: 10.1038/nrd2400 18049471

6. ChinaBioToday. China’s SFDA Ready to Fast-Track Approvals of Peramivir, a Flu Treatment http://www.chinabiotoday.com/articles/20130408_1.2013 [updated 08/04/2013; cited 2014 13/04/2014]. Available from: http://www.chinabiotoday.com/articles/20130408_1.

7. Chairat K, Tarning J, White NJ, Lindegardh N. Pharmacokinetic properties of anti-influenza neuraminidase inhibitors. J Clin Pharmacol. 2013;53(2):119–39. Epub 2013/02/26. doi: 10.1177/0091270012440280 23436258.

8. Ikematsu H, Kawai N. Laninamivir octanoate: a new long-acting neuraminidase inhibitor for the treatment of influenza. Expert Rev Anti Infect Ther. 2011;9(10):851–7. doi: 10.1586/eri.11.112 21973296

9. Hurt AC, Kelly H. Debate Regarding Oseltamivir Use for Seasonal and Pandemic Influenza. Emerging infectious diseases. 2016;22(6):949–55. Epub 2016/05/19. doi: 10.3201/eid2206.151037 27191818; PubMed Central PMCID: PMC4880079.

10. Gubareva LV, Besselaar TG, Daniels RS, Fry A, Gregory V, Huang W, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2015–2016. Antiviral research. 2017;146:12–20. doi: 10.1016/j.antiviral.2017.08.004 PMC5667636. 28802866

11. Hurt AC, Besselaar TG, Daniels RS, Ermetal B, Fry A, Gubareva L, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2014–2015. Antiviral Res. 2016;132:178–85. doi: 10.1016/j.antiviral.2016.06.001 27265623

12. Meijer A, Rebelo-de-Andrade H, Correia V, Besselaar T, Drager-Dayal R, Fry A, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2012–2013. Antiviral Res. 2014;110:31–41. doi: 10.1016/j.antiviral.2014.07.001 25043638

13. Takashita E, Meijer A, Lackenby A, Gubareva L, Rebelo-de-Andrade H, Besselaar T, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013–2014. Antiviral Res. 2015;117:27–38. doi: 10.1016/j.antiviral.2015.02.003 25721488

14. McKimm-Breschkin J, Trivedi T, Hampson A, Hay A, Klimov A, Tashiro M, et al. Neuraminidase sequence analysis and susceptibilities of influenza virus clinical isolates to zanamivir and oseltamivir. Antimicrob Agents Chemother. 2003;47(7):2264–72. doi: 10.1128/aac.47.7.2264-2272.2003 12821478

15. Okomo-Adhiambo M, Sleeman K, Lysen C, Nguyen HT, Xu X, Li Y, et al. Neuraminidase inhibitor susceptibility surveillance of influenza viruses circulating worldwide during the 2011 Southern Hemisphere season. Influenza Other Respir Viruses. 2013;7(5):645–58. doi: 10.1111/irv.12113 23575174

16. Sheu TG, Deyde VM, Okomo-Adhiambo M, Garten RJ, Xu X, Bright RA, et al. Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from 2004 to 2008. Antimicrob Agents Chemother. 2008;52(9):3284–92. doi: 10.1128/AAC.00555-08 18625765

17. Gubareva LV. Molecular mechanisms of influenza virus resistance to neuraminidase inhibitors. Virus Res. 2004;103(1–2):199–203. doi: 10.1016/j.virusres.2004.02.034 15163510

18. Lackenby A, Hungnes O, Dudman SG, Meijer A, Paget WJ, Hay AJ, et al. Emergence of resistance to oseltamivir among influenza A(H1N1) viruses in Europe. Euro Surveill. 2008;13(5). Epub 2008/05/01. doi: 10.2807/ese.13.05.08026-en 18445375.

19. Moscona A. Global Transmission of Oseltamivir-Resistant Influenza. New England Journal of Medicine. 2009;360(10):953–6. doi: 10.1056/NEJMp0900648 19258250.

20. Lackenby A, Besselaar TG, Daniels RS, Fry A, Gregory V, Gubareva LV, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors and status of novel antivirals, 2016–2017. Antiviral Res. 2018;157:38–46. Epub 2018/07/10. doi: 10.1016/j.antiviral.2018.07.001 29981793; PubMed Central PMCID: PMC6094047.

21. Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, Garten RJ, et al. Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med. 2009;360(25):2605–15. doi: 10.1056/NEJMoa0903810 19423869

22. Gubareva LV, Trujillo AA, Okomo-Adhiambo M, Mishin VP, Deyde VM, Sleeman K, et al. Comprehensive assessment of 2009 pandemic influenza A (H1N1) virus drug susceptibility in vitro. Antivir Ther. 2010;15(8):1151–9. doi: 10.3851/IMP1678 21149922

23. Hurt AC, Hardie K, Wilson NJ, Deng YM, Osbourn M, Leang SK, et al. Characteristics of a widespread community cluster of H275Y oseltamivir-resistant A(H1N1)pdm09 influenza in Australia. J Infect Dis. 2012;206(2):148–57. doi: 10.1093/infdis/jis337 22561367

24. Takashita E, Kiso M, Fujisaki S, Yokoyama M, Nakamura K, Shirakura M, et al. Characterization of a large cluster of influenza A(H1N1)pdm09 viruses cross-resistant to oseltamivir and peramivir during the 2013–2014 influenza season in Japan. Antimicrob Agents Chemother. 2015;59(5):2607–17. doi: 10.1128/AAC.04836-14 25691635

25. Okomo-Adhiambo M, Mishin VP, Sleeman K, Saguar E, Guevara H, Reisdorf E, et al. Standardizing the influenza neuraminidase inhibition assay among United States public health laboratories conducting virological surveillance. Antiviral Res. 2016;128:28–35. doi: 10.1016/j.antiviral.2016.01.009 26808479

26. Hurt AC, Okomo-Adhiambo M, Gubareva LV. The fluorescence neuraminidase inhibition assay: a functional method for detection of influenza virus resistance to the neuraminidase inhibitors. Methods Mol Biol. 2012;865:115–25. doi: 10.1007/978-1-61779-621-0_7 22528156

27. Okomo-Adhiambo M, Sleeman K, Ballenger K, Nguyen HT, Mishin VP, Sheu TG, et al. Neuraminidase inhibitor susceptibility testing in human influenza viruses: a laboratory surveillance perspective. Viruses. 2010;2(10):2269–89. doi: 10.3390/v2102269 21994620

28. Meetings of the WHO working group on surveillance of influenza antiviral susceptibility—Geneva, November 2011 and June 2012. Wkly Epidemiol Rec. 2012;87(39):369–74. 23061103

29. Kawai N, Ikematsu H, Hirotsu N, Maeda T, Kawashima T, Tanaka O, et al. Clinical effectiveness of oseltamivir and zanamivir for treatment of influenza A virus subtype H1N1 with the H274Y mutation: a Japanese, multicenter study of the 2007–2008 and 2008–2009 influenza seasons. Clin Infect Dis. 2009;49(12):1828–35. Epub 2009/11/17. doi: 10.1086/648424 19911968.

30. Saito R, Sato I, Suzuki Y, Baranovich T, Matsuda R, Ishitani N, et al. Reduced effectiveness of oseltamivir in children infected with oseltamivir-resistant influenza A (H1N1) viruses with His275Tyr mutation. Pediatr Infect Dis J. 2010;29(10):898–904. doi: 10.1097/INF.0b013e3181de9d24 20442686

31. Matsuzaki Y, Mizuta K, Aoki Y, Suto A, Abiko C, Sanjoh K, et al. A two-year survey of the oseltamivir-resistant influenza A(H1N1) virus in Yamagata, Japan and the clinical effectiveness of oseltamivir and zanamivir. Virology journal. 2010;7:53–. doi: 10.1186/1743-422X-7-7 PubMed PMID: 20202225.

32. Piralla A, Gozalo-Marguello M, Fiorina L, Rovida F, Muzzi A, Colombo AA, et al. Different drug-resistant influenza A(H3N2) variants in two immunocompromised patients treated with oseltamivir during the 2011–2012 influenza season in Italy. J Clin Virol. 2013;58(1):132–7. doi: 10.1016/j.jcv.2013.06.003 23810646

33. Hurt AC, Leang SK, Tiedemann K, Butler J, Mechinaud F, Kelso A, et al. Progressive emergence of an oseltamivir-resistant A(H3N2) virus over two courses of oseltamivir treatment in an immunocompromised paediatric patient. Influenza Other Respir Viruses. 2013;7(6):904–8. doi: 10.1111/irv.12108 23551973

34. Sugaya N, Mitamura K, Yamazaki M, Tamura D, Ichikawa M, Kimura K, et al. Lower clinical effectiveness of oseltamivir against influenza B contrasted with influenza A infection in children. Clin Infect Dis. 2007;44(2):197–202. doi: 10.1086/509925 17173216

35. Suzuki E, Ichihara K. The course of fever following influenza virus infection in children treated with oseltamivir. J Med Virol. 2008;80(6):1065–71. doi: 10.1002/jmv.21144 18428131

36. Kawai N, Ikematsu H, Iwaki N, Maeda T, Kanazawa H, Kawashima T, et al. A comparison of the effectiveness of zanamivir and oseltamivir for the treatment of influenza A and B. The Journal of infection. 2008;56(1):51–7. Epub 10/15. doi: 10.1016/j.jinf.2007.09.002 17936910.

37. Sugaya N, Tamura D, Yamazaki M, Ichikawa M, Kawakami C, Kawaoka Y, et al. Comparison of the clinical effectiveness of oseltamivir and zanamivir against influenza virus infection in children. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 2008;47(3):339–45. doi: 10.1086/589748 18582202.

38. Heinonen S, Silvennoinen H, Lehtinen P, Vainionpää R, Vahlberg T, Ziegler T, et al. Early oseltamivir treatment of influenza in children 1–3 years of age: a randomized controlled trial. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 2010;51(8):887–94. doi: 10.1086/656408 20815736.

39. Kawai N, Ikematsu H, Iwaki N, Maeda T, Satoh I, Hirotsu N, et al. A comparison of the effectiveness of oseltamivir for the treatment of influenza A and influenza B: a Japanese multicenter study of the 2003–2004 and 2004–2005 influenza seasons. Clin Infect Dis. 2006;43(4):439–44. doi: 10.1086/505868 16838232

40. Belser JA, Katz JM, Tumpey TM. The ferret as a model organism to study influenza A virus infection. Disease models & mechanisms. 2011;4(5):575–9. Epub 2011/08/04. doi: 10.1242/dmm.007823 21810904; PubMed Central PMCID: PMC3180220.

41. Bouvier NM, Lowen AC. Animal Models for Influenza Virus Pathogenesis and Transmission. Viruses. 2010;2(8):1530–63. Epub 2010/01/01. doi: 10.3390/v20801530 21442033; PubMed Central PMCID: PMC3063653.

42. Margine I, Krammer F. Animal models for influenza viruses: implications for universal vaccine development. Pathogens (Basel, Switzerland). 2014;3(4):845–74. Epub 2014/12/02. doi: 10.3390/pathogens3040845 25436508; PubMed Central PMCID: PMC4282889.

43. Oh DY, Hurt AC. Using the ferret as an animal model for investigating influenza antiviral effectiveness. Frontiers in Microbiology. 2016;7. doi: 10.3389/fmicb.2016.00080 26870031

44. Radigan KA, Misharin AV, Chi M, Budinger GS. Modeling human influenza infection in the laboratory. Infection and drug resistance. 2015;8:311–20. Epub 2015/09/12. doi: 10.2147/IDR.S58551 26357484; PubMed Central PMCID: PMC4560508.

45. Govorkova EA, Marathe BM, Prevost A, Rehg JE, Webster RG. Assessment of the efficacy of the neuraminidase inhibitor oseltamivir against 2009 pandemic H1N1 influenza virus in ferrets. Antiviral Res. 2011;91(2):81–8. Epub 2011/06/04. doi: 10.1016/j.antiviral.2011.05.008 21635924; PubMed Central PMCID: PMC3148604.

46. Huang SS, Banner D, Fang Y, Ng DC, Kanagasabai T, Kelvin DJ, et al. Comparative analyses of pandemic H1N1 and seasonal H1N1, H3N2, and influenza B infections depict distinct clinical pictures in ferrets. PLoS ONE. 2011;6(11):16.

47. Oh DY, Lowther S, McCaw JM, Sullivan SG, Leang SK, Haining J, et al. Evaluation of oseltamivir prophylaxis regimens for reducing influenza virus infection, transmission and disease severity in a ferret model of household contact. J Antimicrob Chemother. 2014;69(9):2458–69. doi: 10.1093/jac/dku146 24840623

48. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. The American Journal of Epidemiology. 1938;27(3):493–7.

49. Reddy MB, Yang KH, Rao G, Rayner CR, Nie J, Pamulapati C, et al. Oseltamivir Population Pharmacokinetics in the Ferret: Model Application for Pharmacokinetic/Pharmacodynamic Study Design. PLoS ONE. 2015;10(10).

50. Oh DY, Barr IG, Hurt AC. A novel video tracking method to evaluate the effect of influenza infection and antiviral treatment on ferret activity. PLoS ONE. 2015;10(3).

51. Farrukee R, Zarebski AE, McCaw JM, Bloom JD, Reading PC, Hurt AC. Characterization of Influenza B Virus Variants with Reduced Neuraminidase Inhibitor Susceptibility. Antimicrob Agents Chemother. 2018;62(11):01081–18.

52. Zhou B, Lin X, Wang W, Halpin RA, Bera J, Stockwell TB, et al. Universal influenza B virus genomic amplification facilitates sequencing, diagnostics, and reverse genetics. J Clin Microbiol. 2014;52(5):1330–7. doi: 10.1128/JCM.03265-13 24501036

53. Zhou B, Donnelly ME, Scholes DT, St George K, Hatta M, Kawaoka Y, et al. Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and Swine origin human influenza a viruses. Journal of virology. 2009;83(19):10309–13. Epub 07/15. doi: 10.1128/JVI.01109-09 19605485.

54. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9. doi: 10.1038/nmeth.1923 22388286.

55. Koboldt DC, Larson DE, Wilson RK. Using VarScan 2 for Germline Variant Calling and Somatic Mutation Detection. Curr Protoc Bioinformatics. 2013;44:15.4.1–.4.7. doi: 10.1002/0471250953.bi1504s44 25553206.

56. Direksin K, Joo H, Goyal SM. An immunoperoxidase monolayer assay for the detection of antibodies against swine influenza virus. J Vet Diagn Invest. 2002;14(2):169–71. doi: 10.1177/104063870201400215 11939342

57. Team RDC. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.; 2008.

58. Uno Y, Uehara S, Yamazaki H. Utility of non-human primates in drug development: Comparison of non-human primate and human drug-metabolizing cytochrome P450 enzymes. Biochem Pharmacol. 2016;121:1–7. doi: 10.1016/j.bcp.2016.06.008 27318253

59. Baskin CR, Garcia-Sastre A, Tumpey TM, Bielefeldt-Ohmann H, Carter VS, Nistal-Villan E, et al. Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J Virol. 2004;78(19):10420–32. doi: 10.1128/JVI.78.19.10420-10432.2004 15367608

60. Safronetz D, Rockx B, Feldmann F, Belisle SE, Palermo RE, Brining D, et al. Pandemic swine-origin H1N1 influenza A virus isolates show heterogeneous virulence in macaques. J Virol. 2011;85(3):1214–23. Epub 2010/11/19. doi: 10.1128/JVI.01848-10 21084481; PubMed Central PMCID: PMC3020514.

61. Josset L, Engelmann F, Haberthur K, Kelly S, Park B, Kawoaka Y, et al. Increased viral loads and exacerbated innate host responses in aged macaques infected with the 2009 pandemic H1N1 influenza A virus. J Virol. 2012;86(20):11115–27. Epub 2012/08/03. doi: 10.1128/JVI.01571-12 22855494; PubMed Central PMCID: PMC3457171.

62. Marriott AC, Dennis M, Kane JA, Gooch KE, Hatch G, Sharpe S, et al. Influenza A Virus Challenge Models in Cynomolgus Macaques Using the Authentic Inhaled Aerosol and Intra-Nasal Routes of Infection. PLoS One. 2016;11(6):e0157887. Epub 2016/06/17. doi: 10.1371/journal.pone.0157887 27311020; PubMed Central PMCID: PMC4911124.

63. Kitano M, Itoh Y, Kodama M, Ishigaki H, Nakayama M, Ishida H, et al. Efficacy of single intravenous injection of peramivir against influenza B virus infection in ferrets and cynomolgus macaques. Antimicrobial agents and chemotherapy. 2011;55(11):4961–70. Epub 08/15. doi: 10.1128/AAC.00412-11 21844317.

64. Itoh Y, Shichinohe S, Nakayama M, Igarashi M, Ishii A, Ishigaki H, et al. Emergence of H7N9 Influenza A Virus Resistant to Neuraminidase Inhibitors in Nonhuman Primates. Antimicrob Agents Chemother. 2015;59(8):4962–73. doi: 10.1128/AAC.00793-15 26055368

65. Kiso M, Iwatsuki-Horimoto K, Yamayoshi S, Uraki R, Ito M, Nakajima N, et al. Emergence of Oseltamivir-Resistant H7N9 Influenza Viruses in Immunosuppressed Cynomolgus Macaques. The Journal of Infectious Diseases. 2017;216(5):582–93. doi: 10.1093/infdis/jix296 28931216

66. Stittelaar KJ, Tisdale M, van Amerongen G, van Lavieren RF, Pistoor F, Simon J, et al. Evaluation of intravenous zanamivir against experimental influenza A (H5N1) virus infection in cynomolgus macaques. Antiviral research. 2008;80(2):225–8. Epub 07/21. doi: 10.1016/j.antiviral.2008.06.014 18647621.

67. Kitano M, Itoh Y, Ishigaki H, Nakayama M, Ishida H, Pham VL, et al. Efficacy of repeated intravenous administration of peramivir against highly pathogenic avian influenza A (H5N1) virus in cynomolgus macaques. Antimicrobial agents and chemotherapy. 2014;58(8):4795–803. Epub 06/09. doi: 10.1128/AAC.02817-14 24913156.

68. Ison MG, Portsmouth S, Yoshida Y, Shishido T, Hayden F, Uehara T, editors. Phase 3 Trial of Baloxavir Marboxil in High Risk Influenza Patients (CAPSTONE-2 Study). ID week advancing science week; 2018; San Francisco

69. Baz M, Abed Y, Simon P, Hamelin ME, Boivin G. 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. 2010;201(5):740–5. doi: 10.1086/650464 20100088

70. Govorkova EA, Ilyushina NA, Boltz DA, Douglas A, Yilmaz N, Webster RG. Efficacy of oseltamivir therapy in ferrets inoculated with different clades of H5N1 influenza virus. Antimicrob Agents Chemother. 2007;51(4):1414–24. doi: 10.1128/AAC.01312-06 17296744

71. Hamelin M-È, Baz M, Abed Y, Couture C, Joubert P, Beaulieu É, et al. Oseltamivir-Resistant Pandemic A/H1N1 Virus Is as Virulent as Its Wild-Type Counterpart in Mice and Ferrets. PLoS Pathogens. 2010;6(7):e1001015. doi: 10.1371/journal.ppat.1001015 PMC2908621. 20661429

72. Hurt AC, Nor'e SS, McCaw JM, Fryer HR, Mosse J, McLean AR, et al. Assessing the Viral Fitness of Oseltamivir-Resistant Influenza Viruses in Ferrets, Using a Competitive-Mixtures Model. Journal of Virology. 2010;84(18):9427–38. doi: 10.1128/JVI.00373-10 PMC2937593. 20631138

73. Marriott AC, Dove BK, Whittaker CJ, Bruce C, Ryan KA, Bean TJ, et al. Low dose influenza virus challenge in the ferret leads to increased virus shedding and greater sensitivity to oseltamivir. PLoS ONE. 2014;9(4).

74. Wong DDY, Choy K-T, Chan RWY, Sia SF, Chiu H-P, Cheung PPH, et al. Comparable Fitness and Transmissibility between Oseltamivir-Resistant Pandemic 2009 and Seasonal H1N1 Influenza Viruses with the H275Y Neuraminidase Mutation. Journal of Virology. 2012;86(19):10558–70. doi: 10.1128/JVI.00985-12 PMC3457312. 22811535

75. Yen H-L, Zhou J, Choy K-T, Sia SF, Teng O, Ng IH, et al. The R292K mutation that confers resistance to neuraminidase inhibitors leads to competitive fitness loss of A/Shanghai/1/2013 (H7N9) influenza virus in ferrets. The Journal Of Infectious Diseases. 2014;210(12):1900–8. doi: 10.1093/infdis/jiu353 (24951824). Cites: Science. 2013 Jul 26;341(6144):410–4. (PMID: 23868922). Cites: Emerg Infect Dis. 2013;19(9):1521–4. (PMID: 23965618). Cites: Nature. 2013 Sep 26;501(7468):551–5. (PMID: 23842494). Cites: Nature. 2013 Sep 26;501(7468):556–9. (PMID: 23842497). Cites: Nature. 2013 Sep 26;501(7468):560–3. (PMID: 23925116). Cites: Am J Pathol. 2013 Oct;183(4):1137–43. (PMID: 24029490). Cites: Nat Commun. 2013;4:2854. (PMID: 24326875). Cites: Clin Infect Dis. 2014 Jan;58(2):242–6. (PMID: 24076969). Cites: J Virol. 2014 Feb;88(3):1502–12. (PMID: 24227867). Cites: Lancet Respir Med. 2013 Sep;1(7):534–42. (PMID: 24461614). Cites: J Infect Dis. 2014 Feb 15;209(4):551–6. (PMID: 23990570). Linking ISSN: 00221899. Subset: AIM; IM; Grant Information: HHSN27220140006C United States PHS HHS Date of Electronic Publication: 2014 Jun 20. Current Imprints: Publication: Jan. 2011-: Oxford: Oxford University Press; Original Imprints: Publication: 1904–2010: Chicago, IL: University of Chicago Press 10.1093/infdis/jiu353.

76. Thangavel RR, Bouvier NM. Review: Animal models for influenza virus pathogenesis, transmission, and immunology. Journal of Immunological Methods. 2014;410:60–9. Epub 2014, April 4. doi: 10.1016/j.jim.2014.03.023 S0022175914001124. 24709389

77. Singh S, Barghoorn J, Bagdonas A, Adler J, Treanor J, Kinnersley N, et al. Clinical benefits with oseltamivir in treating influenza in adult populations. Clinical drug investigation. 2003;23(9):561–9. doi: 10.2165/00044011-200323090-00002 17535069


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