Virus susceptibility analyses from a phase IV clinical trial of inhaled zanamivir treatment in children infected with influenza

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 4, 2013, Pages 1677-1684

  Yates, Phillip J ^a   Mehta, Nalini ^a   Horton, Joseph ^b   Tisdale, Margaret ^a  

^a GLAXOSMITHKLINE   (United Kingdom)

^b GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; SIALIDASE; ZANAMIVIR;

AMINO ACID ANALYSIS; AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ANTIVIRAL THERAPY; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG RECEPTOR BINDING; HUMAN; IC 50; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA B; INFLUENZA VIRUS A; JAPAN; MAJOR CLINICAL STUDY; MOLECULAR CLONING; NONHUMAN; PHASE 4 CLINICAL TRIAL; PRIORITY JOURNAL; PROTEIN FOLDING; SEASONAL INFLUENZA; SEQUENCE ANALYSIS; THROAT CULTURE; VIRUS CULTURE;

AMINO ACID SUBSTITUTION; DRUG RESISTANCE, VIRAL; HUMANS; INFLUENZA, HUMAN; MOLECULAR SEQUENCE DATA; MUTATION; NEURAMINIDASE; POLYMERASE CHAIN REACTION; VIRAL PROTEINS; ZANAMIVIR;

EID: 84875180043     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02145-12     Document Type: Article

References (47)

1. von Itzstein M, Wu W-Y, Kok GB, Pegg MS, Dyason JC, Jin B, van Phan T, Smythe ML, White HF, Oliver SW, Colman PM, Varghese JN, Ryan DM, Woods JM, Bethell RC, Hotham VJ, Cameron JM, Penn CR. 1993. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363:418-423.
2. Collins PJ, Haire LF, Lin YP, Liu J, Russell RJ, Walker PA, Skehel JJ, Martin SR, Hay AJ, Gamblin SJ. 2008. The mechanism of H5N1 influenza resistance to Tamiflu and implications for drug stockpiles. Nature 453:1258 -1261.
3. Smith BJ, McKimm-Breshkin JL, McDonald M, Fernley RT, Varghese JN, Colman PM. 2002. Structural studies of the resistance of influenza virus neuraminidase to inhibitors. J. Med. Chem. 45:2207-2212.
4. Varghese JN, Smith PW, Sollis SL, Blick TJ, Sahasrabudhe A, McKimm-Breschkin JL, Colman PM. 1998. Drug design against a shifting target: a structural basis for resistance to inhibitors in a variant of influenza virus neuraminidase. Structure 6:735-746.
5. Laforce C, Man CY, Henderson FW, McElhaney JE, Hampel FC, Bettis R, Kudule L, Harris J, Yates P, Tisdale M, Webster A. 2007. Efficacy and safety of inhaled zanamivir in the prevention of influenza in community-dwelling high-risk adult and adolescent subjects: a 28-day, randomized, double-blind, placebo-controlled, multi-center trial. Clin. Ther. 29:1579-1590.
6. Tisdale M. 2000. Monitoring of viral susceptibility: new challenges with the development of influenza NA inhibitors. Rev. Med. Virol. 10:45-55.
7. Gubareva LV, Mastrosovich MN, Brenner MK, Bethell RC, Webster RG. 1998. Evidence for zanamivir resistance in an immunocompromised child infected with influenza B virus. J. Infect. Dis. 178:1557-1562.
8. Nguyen HT, Fry AM, Loveless PA, Klimov AI, Gubareva LV. 2010. Recovery of a multi-drug 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.
9. Rousset D, Goff JL, Abou-Jaoude G, Scemla A, Ribaud P, Mercier-Delaurue S, Caro V, Enouf V, Simon F, Molina JM, van der Werf S. 2010. Emergence of successive mutations in the neuraminidase of the pandemic H1N1 virus, respectively, associated with oseltamivir resistance and reduced susceptibility to both oseltamivir and zanamivir under treatment with neuraminidase inhibitors, abstr. P-198. Abstr. Options for Control of Influenza Congress, Hong Kong.
10. 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.
11. Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, Kimura K, Hayden FG, Sugaya N, Kawaoka Y. 2004. Resistant influenza A viruses in children treated with oseltamivir. Lancet 364:759 -765.
12. Ward P, Small I, Smith J, Suter P, Dutkowski R. 2005. Oseltamivir (Tamiflu) and its potential for use in the event of an influenza pandemic. J. Antimicrob. Chemother. 55(Suppl S1):i5-i21.
13. Interim Risk Assessment ECDC. 2008. Emergence of seasonal influenza viruses type A/H1N1 with oseltamivir resistance in some European countries at the start of the 2007-8 influenza season. European Centre for Disease Prevention and Control, Stockholm, Sweden. Accessed 27 January 2008. http://www.ecdc. europa.eu/en/healthtopics/documents/0801-interim-ecdc-risk-assessment.pdf.
14. World Health Organization. 2008. Influenza A(H1N1) virus resistance to oseltamivir - 2008 influenza season, Southern Hemisphere. World Health Organization, Geneva, Switzerland. Accessed 18 July 2008. http://www.who.int/ csr/disease/influenza/H1N1webupdate18072008.pdf.
15. World Health Organization. 2009. Oseltamivir resistance in immunocompromised hospital patients. Pandemic (H1N1) 2009 briefing note 18. World Health Organization, Geneva, Switzerland. http://www.who.int/csr/disease/ swineflu/notes/briefing-20091202/en/index.html.
16. World Health Organization. 2011. Update on oseltamivir resistance in influenza A (H1N1) 2009 viruses. World Health Organization, Geneva, Switzerland. http://www.who.int/influenza/surveillance-monitoring/updates/2011-09-09-weekly- web-update-oseltamivir-resistance.pdf.
17. Englund J, Zerr D, Heath J, Pergam S, Kuypers J, Yager J, Boeckh M, Mattson D, Whittington N, Whimbey E, Duchin J, Uyeki T, Deyde V, Okomo-Adhiambo M, Sheu T, Trujillo A, Klimov A, Gubareva L, Kay M. 14 August 2009. Oseltamivir-resistant novel influenza A (H1N1) virus infection in two immunosuppressed patients - Seattle, Washington, 2009. MMWR Dispatch 58:1- 4. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm58d0814a1.htm?s-cid-mm58d0814a1-e. Accessed 30 September 2011.
18. Garrison M, Weldon L, Wolf L, Davies M, Maillard J-M, Moore Z, Sheu T, Deyde V, Gubareva L, Fry AM, Fleischauer A, Dailey NJ. 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.
19. Mai LQ, Wertheim HFL, Duong TN, van Doorn HR, Hien NT, Horby P. 2010. A community cluster of oseltamivir-resistant cases of 2009 H1N1 influenza. N. Engl. J. Med. 362:86-87.
20. World Health Organization. 2010. Weekly update on oseltamivir resistance to pandemic influenza A (H1N1) 2009 viruses. World Health Organization, Geneva, Switzerland. http://www.who.int/csr/disease/swineflu/ oseltamivirresistant20100806.pdf.
21. Lackenby A, Moran Gilad J, Pebody R, Miah S, Calatayud L, Bolotin S, Vipond I, Muir P, Guiver M, McMenamin J, Reynolds A, Moore C, Gunson R, Thompson C, Galiano M, Bermingham A, Ellis J, Zambon M. 2011. Continued emergence and changing epidemiology of oseltamivir-resistant influenza A(H1N1)2009 virus, United Kingdom, winter 2010/11. Euro Surveill. 16(5):pii-19784. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId-19784.
22. Hardie K, Hurt A, Wilson N. 2011. Influenza (50): Australia(NewSouth Wales), H275Y mutation cluster. In ProMED Mail. International Society for Infectious Diseases, Brookline, MA. Archive number 20110825.2594. Accessed 30 September 2011.
23. Hurt AC, Hardie K, Wilson NJ, Deng YM, Osbourn M, Gehrig N, Kelso A. 2011. Community transmission of oseltamivir-resistant A(H1N1)pdm09 influenza. N. Engl. J. Med. 365:2541-2542.
24. Saito R, Suzuki K, Okano H, Hasegawa N, Abe H, Inoshira S. 2011. Sensitivity to influenza virus and antipyretic effects of zanamivir (Relenza) in pediatric patients with influenza A and B virus infection: special drug use investigation in emergence of Relenza-resistant influenza viruses in pediatric patients over three influenza seasons from 2006 to 2009. Antibiot. Chem. 27:123-137.
25. Barnett JM, Cadman A, Gor D, Dempsey M, Walters M, Candlin A, Tisdale M, Morley PJ, Owens IJ, Fenton RJ, Lewis AP, Claas ECJ, Rimmelzwaan GF, De Groot R, Osterhaus ADME. 2000. Zanamivir susceptibility monitoring and characterization of influenza virus clinical isolates obtained during phase II clinical efficacy studies. Antimicrob. Agents Chemother. 44:78-87.
26. Barnett JM, Cadman A, Burrell FM, Madar SH, Lewis AP, Tisdale M, Bethel R. 1999. In vitro selection and characterisation of influenza B/Beijing/1/87 isolates with altered susceptibility to zanamivir. Virology 265: 286-295.
27. Monto AS, Macken C, McKimm-Breschkin JL, Hampson AW, Hay A, Klimov A, Tashiro M, Webster RG, Aymard M, Hayden F, Zambon M. 2006. Influenza viruses resistant to the neuraminidase inhibitors detected during the first three years of their use. Antimicrob. Agents Chemother. 50:2395-2402.
28. Le QM, Kiso M, Someya K, Sakai YT, Nguyen TH, Nguyen KHL, Dinh Pham N, Ngyen HH, Yamada S, Muramoto Y, Horimoto T, Takada A, Goto H, Suzuki T, Suzuki Y, Kawaoka Y. 2005. Isolation of drugresistant H5N1 virus. Nature 437:1108.
29. Carr S, Ilyushina NA, Franks J, Adderson EE, Caniza M, Govorkova EA, Webster RG. 2011. Oseltamivir-resistant influenza A and B viruses pre- and postantiviral therapy in children and young adults with cancer. Pediatr. Infect. Dis. J. 30:284 -288.
30. Abed Y, Baz M, Boivin G. 2006. Impact of neuraminidase mutations conferring influenza resistance to neuraminidase inhibitors in the N1 and N2 genetic backgrounds. Antivir. Ther. 11:971-976.
31. Pizzorno A, Bouhy X, 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.
32. Tisdale M. 2009. Influenza M2 ion-channel and neuraminidase inhibitors, p 421-447. In Mayers DL, Lerner SA, Ouellette M, Sobel JD (ed), Antimicrobial drug resistance: mechanisms of drug resistance, vol 1. doi: 10.1007/978-1-59745- 180-2-31.
33. Hatakeyama S, Sugaya N, Ito M, Yamazaki M, Ichikawa M, Kimura K, Kiso M, Shimizu H, Kawakami C, Koike K, Mitamura K, Kawaoka Y. 2007. Emergence of influenza B viruses with reduced sensitivity to neuraminidase inhibitors. JAMA 297:1435-1442.
34. Yen HL, Hoffmann E, Taylor G, Scholtissek C, Monto AS, Webster RG, Govorkova EA. 2006. Importance of neuraminidase active-site residues to the neuraminidase inhibitor resistance of influenza viruses. J. Virol. 80: 8787-8795.
35. Zürcher T, Yates PJ, Daly J, Sahasrabudhe Walyers M, Dash L, Tisdale M, McKimm-Breshkin JL. 2006. Mutations conferring zanamivir resistance in human influenza virus N2 neuraminidase compromise virus fitness and are not stably maintained in vitro. J. Antimicrob. Chemother. 58:723-732.
36. Hurt AC, Holien JK, Parker M, Kelso A, Barr IG. 2009. Zanamivirresistant influenza viruses with a novel neuraminidase mutation. J. Virol. 83:10366 -10373.
37. Hurt AC, Lowther S, Middletonc D, Barr IG. 2010. Assessing the development of oseltamivir and zanamivir resistance in A(H5N1) influenza viruses using a ferret model. Antiviral Res. 87:361-366.
38. Okomo-Adhiambo M, Nguyen HT, Sleeman K, Sheu TG, Deyde VM, Garten RJ, Xu X, Shaw MW, Klimov AI, Gubareva LV. 2009. Host cell selection of influenza neuraminidase variants: implications for drug resistance monitoring in A(H1N1) viruses. Antiviral Res. 85:381-388.
39. Dapat C, Suzuki Y, Saito R, Kyaw Y, Myint YY, Lin N, Oo HN, Oo KY, Win N, Naito M, Hasegawa G, Dapat IC, Zaraket H, Baranovich T, Nishikawa M, Saito T, Suzuki H. 2010. Rare influenza A (H3N2) variants with reduced sensitivity to antiviral drugs. Emerg. Infect. Dis. 16:493- 496.
40. Baz M, Abed Y, Boivin G. 2007. Characterization of drug-resistant recombinant influenza A/H1N1 viruses selected in vitro with peramivir and zanamivir. Antiviral Res. 74:159 -162.
41. McKimm-Breschkin J, Trivedi T, Hampson A, Hay A, Klimov A, Tashiro M, Hayden F, Zambon M. 2003. Neuraminidase sequence analysis and susceptibilities of influenza virus clinical isolates to zanamivir and oseltamivir. Antimicrob. Agents Chemother. 47:2264 -2272.
42. Gubareva LV, Hayden FG. 2006. M2 and neuraminidase inhibitors: anti-influenza activity, mechanisms of resistance, and clinical effectiveness. In Kawaoka Y (ed), Influenza virology: current topics. Caister Academic, Norfolk, United Kingdom.
43. Aoki FY, Boivin G, Roberts N. 2007. Influenza virus susceptibility and resistance to oseltamivir. Antivir. Ther. 12:603- 616.
44. Valinotto LE, Diez RA, Barrero PR, Farias JA, Lopez EL, Mistchenko AS. 2010. Emergence of intratreatment resistance to oseltamivir in pandemic influenza A H1N1 2009 virus. Antivir. Ther. 15:923-927.
45. Lackovich JK, Lee JE, Chang P, Rashtchian A. 2001. Measuring fidelity of PLATINUM® Pfx DNA polymerase. Focus 23:6 -7.
46. Westfall B, Sitaraman K, Lee JE, Borman J, Rashtchian A. 1999. PLATINUM® Pfx DNA polymerase for high-fidelity PCR. Focus 21: 46 - 48.
47. Herlocher ML, Truscon R, Elias S, Yen H-L, Roberts NA, Ohmit SE, Monto AS. 2004. Influenza viruses resistant to the antiviral drug oseltamivir: transmission studies in ferrets. J. Infect. Dis. 190:1627-1630.