Selection of multi-drug resistant influenza A and B viruses under zanamivir pressure and their replication fitness in ferrets

Antiviral Therapy

Volumn 23, Issue 4, 2018, Pages 295-306

  Oh, Ding Yuan ^a,b   Panozzo, Jacqueline ^a,b   Vitesnik, Sophie ^a   Farrukee, Rubaiyea ^a   Piedrafita, David ^b   Mosse, Jennifer ^b   Hurt, Aeron C ^a,c  

^a VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

^b UNIVERSITY OF BALLARAT   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; VIRUS RNA; ZANAMIVIR;

ANIMAL; ANTIVIRAL RESISTANCE; CLASSIFICATION; DISEASE PREDISPOSITION; DNA SEQUENCE; DRUG EFFECT; GENETIC RECOMBINATION; INFLUENZA A VIRUS; INFLUENZA B VIRUS; MICROBIAL SENSITIVITY TEST; MUSTELA PUTORIUS FURO; MUTATION; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; REPRODUCTIVE FITNESS; VIROLOGY; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; DISEASE SUSCEPTIBILITY; DRUG RESISTANCE, VIRAL; FERRETS; GENETIC FITNESS; INFLUENZA A VIRUS; INFLUENZA B VIRUS; MICROBIAL SENSITIVITY TESTS; MUTATION; ORTHOMYXOVIRIDAE INFECTIONS; RECOMBINATION, GENETIC; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VIRUS REPLICATION; ZANAMIVIR;

EID: 85046398440     PISSN: 13596535     EISSN: 20402058     Source Type: Journal    
DOI: 10.3851/imp3135     Document Type: Article

References (39)

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; 103:9988-9992.
2. China's SFDA ready to fast-track approvals of peramivir, a flu treatment. ChinaBioToday. (Updated 8 April 2013. Accessed 13 April 2014.) Available from http://www.chinabiotoday.com/articles/20130408_1
3. Chairat K, Tarning J, White NJ, Lindegardh N. Pharmacokinetic properties of anti-influenza neuraminidase inhibitors. J Clin Pharmacol 2013; 53:119-139.
4. Ikematsu H, Kawai N. Laninamivir octanoate: a new long-acting neuraminidase inhibitor for the treatment of influenza. Expert Rev Anti Infect Ther 2011; 9:851-857.
5. Wijaya L, Chua YY, Cui L, Chan K, Tan BH. Intravenous zanamivir in critically ill patients due to pandemic 2009 (H1N1) influenza A virus. Singapore Med J 2011; 52:481-485.
6. Marty FM, Man CY, van der Horst C, et al. Safety and pharmacokinetics of intravenous zanamivir treatment in hospitalized adults with influenza: an open-label, multicenter, single-arm, Phase II study. J Infect Dis 2014; 209:542-550.
7. Chan-Tack KM, Kim C, Moruf A, Birnkrant DB. Clinical experience with intravenous zanamivir under an Emergency IND program in the United States (2011-2014). Antivir Ther 2015; 20:561-564.
8. Kidd IM, Down J, Nastouli E, et al. H1N1 pneumonitis treated with intravenous zanamivir. Lancet 2009; 374:1036.
9. GlaxoSmithKline. A Phase III international, randomized, double-blind, double-dummy study to evaluate the efficacy and safety of 300 mg or 600 mg of intravenous zanamivir twice daily compared to 75 mg of oral oseltamivir twice daily in the treatment of hospitalized adults and adolescents with influenza. (Updated 18 July 2016. Accessed 5 December 2016.) Available from http://www.gskclinicalstudyregister.com/study/114373#ps
10. Chan-Tack KM, Gao A, Himaya AC, et al. Clinical experience with intravenous zanamivir under an emergency investigational new drug program in the United States. J Infect Dis 2013; 207:196-198.
11. L'Huillier AG, Abed Y, Petty TJ, et al. E119D neuraminidase mutation conferring pan-resistance to neuraminidase inhibitors in an A(H1N1)pdm09 isolate from a stem-cell transplant recipient. J Infect Dis 2015; 212:1726-1734.
12. Abed Y, Bouhy X, L'Huillier AG, et al. The E119D neuraminidase mutation identified in a multidrug-resistant influenza A(H1N1)pdm09 isolate severely alters viral fitness in vitro and in animal models. Antiviral Res 2016; 132:6-12.
13. Baek YH, Song MS, Lee EY, et al. Profiling and characterization of influenza virus N1 strains potentially resistant to multiple neuraminidase inhibitors. J Virol 2015; 89:287-299.
14. Burnham AJ, Armstrong J, Lowen AC, Webster RG, Govorkova EA. Competitive fitness of influenza B viruses with neuraminidase inhibitor-resistant substitutions in a coinfection model of the human airway epithelium. J Virol 2015; 89:4575-4587.
15. Burnham AJ, Baranovich T, Marathe BM, Armstrong J, Webster RG, Govorkova EA. Fitness costs for influenza B viruses carrying neuraminidase inhibitor-resistant substitutions: underscoring the importance of E119A and H274Y. Antimicrob Agents Chemother 2014; 58:2718-2730.
16. Pascua PN, Marathe BM, Burnham AJ, et al. Competitive fitness of influenza B viruses possessing E119A and H274Y neuraminidase inhibitor resistance-associated substitutions in ferrets. PLoS One 2016; 11:e0159847.
17. Gubareva LV, Bethell R, Hart GJ, Murti KG, Penn CR, Webster RG. Characterization of mutants of influenza A virus selected with the neuraminidase inhibitor 4-guanidino-Neu5Ac2en. J Virol 1996; 70:1818-1827.
18. McKimm-Breschkin JL, Sahasrabudhe A, Blick TJ, et al. Mutations in a conserved residue in the influenza virus neuraminidase active site decreases sensitivity to Neu5Ac2en-derived inhibitors. J Virol 1998; 72:2456-2462.
19. Tai CY, Escarpe PA, Sidwell RW, et al. Characterization of human influenza virus variants selected in vitro in the presence of the neuraminidase inhibitor GS 4071. Antimicrob Agents Chemother 1998; 42:3234-3241.
20. Barnett JM, Cadman A, Burrell FM, et al. In vitro selection and characterisation of influenza B/Beijing/1/87 isolates with altered susceptibility to zanamivir. Virology 1999; 265:286-295.
21. Chaudhry A, Bastien N, Li Y, et al. Oseltamivir resistance in an influenza A (H3N2) virus isolated from an immunocompromised patient during the 2014-2015 influenza season in Alberta, Canada. Influenza Other Respir Viruses 2016; 10:532-535.
22. Tamura D, DeBiasi RL, Okomo-Adhiambo M, et al. Emergence of multidrug-resistant influenza A(H1N1) pdm09 virus variants in an immunocompromised child treated with oseltamivir and zanamivir. J Infect Dis 2015; 212:1209-1213.
23. Recommended composition of influenza virus vaccines for use in the 2016-2017 northern hemisphere influenza season. WHO. (Updated 25 February 2016. Accessed 11 January 2017.) Available from http://www.who.int/influenza/vaccines/virus/recommendations/2016_17_ north/en/
24. 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; 865:115-125.
25. Marathe BM, Leveque V, Klumpp K, Webster RG, Govorkova EA. Determination of neuraminidase kinetic constants using whole influenza virus preparations and correction for spectroscopic interference by a fluorogenic substrate. PLoS One 2013; 8:e71401.
26. Hoffmann E, Krauss S, Perez D, Webby R, Webster RG. Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 2002; 20:3165-3170.
27. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 2000; 97:6108-6113.
28. Hoffmann E, Mahmood K, Yang CF, Webster RG, Greenberg HB, Kemble G. Rescue of influenza B virus from eight plasmids. Proc Natl Acad Sci U S A 2002; 99:11411-11416.
29. 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:e0118780.
30. Monto AS, Maassab HF. Ether treatment of type B influenza virus antigen for the hemagglutination inhibition test. J Clin Microbiol 1981; 13:54-57.
31. Takashita E, Meijer A, Lackenby A, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013-2014. Antiviral Res 2015; 117:27-38.
32. Hurt AC, Besselaar TG, Daniels RS, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2014-2015. Antiviral Res 2016; 132:178-185.
33. Meijer A, Rebelo-de-Andrade H, Correia V, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2012-2013. Antiviral Res 2014; 110:31-41.
34. Gubareva LV, Matrosovich MN, Brenner MK, Bethell RC, Webster RG. Evidence for zanamivir resistance in an immunocompromised child infected with influenza B virus. J Infect Dis 1998; 178:1257-1262.
35. Sheu TG, Deyde VM, Garten RJ, Klimov AI, Gubareva LV. Detection of antiviral resistance and genetic lineage markers in influenza B virus neuraminidase using pyrosequencing. Antiviral Res 2010; 85:354-360.
36. Mishin VP, Hayden FG, Gubareva LV. Susceptibilities of antiviral-resistant influenza viruses to novel neuraminidase inhibitors. Antimicrob Agents Chemother 2005; 49:4515-4520.
37. Butler J, Hooper KA, Petrie S, et al. Estimating the fitness advantage conferred by permissive neuraminidase mutations in recent oseltamivir-resistant A(H1N1)pdm09 influenza viruses. PLoS Pathog 2014; 10:e1004065.
38. Pizzorno A, Bouhy X, Abed Y, Boivin G. Generation and characterization of recombinant pandemic influenza A(H1N1) viruses resistant to neuraminidase inhibitors. J Infect Dis 2011; 203:25-31.
39. ClinicalTrials.gov. A study of intravenous zanamivir versus oral oseltamivir in adults and adolescents hospitalized with influenza (ZORO). GlaxoSmithKline. (Updated 2 December 2016. Accessed 5 December 2016.) Available from https://www.clinicaltrials.gov/ct2/show/NCT01231620?term=A+study+of+intravenous+zanamivir+versus+oral+oseltamivir&a mp;rank=1