Treatment of oseltamivir-resistant influenza A (H1N1) virus infections in mice with antiviral agents

Antiviral Research

Volumn 96, Issue 1, 2012, Pages 13-20

  Smee, Donald F ^a   Julander, Justin G ^a   Bart Tarbet, E ^a   Gross, Matthew ^b   Nguyen, Jack ^b  

^a UTAH STATE UNIVERSITY   (United States)

^b Adamas Pharmaceuticals Inc   (United States)

Author keywords

Amantadine; Oseltamivir; Ribavirin; Rimantadine; Zanamivir

Indexed keywords

4 ACETAMIDO 5 AMINO 3 (1 ETHYLPROPOXY) 1 CYCLOHEXENE 1 CARBOXYLIC ACID; AMANTADINE; ANTIVIRUS AGENT; OSELTAMIVIR; PERAMIVIR; RIBAVIRIN; RIMANTADINE; VIRUS SIALIDASE; ZANAMIVIR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ANTIVIRAL THERAPY; ARTICLE; CELL ASSAY; CELL STRAIN; CONTROLLED STUDY; CYTOTOXICITY; DRUG DOSE COMPARISON; DRUG EFFICACY; ENZYME INHIBITION; FEMALE; GENE MUTATION; IC 50; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL;

AMANTADINE; ANIMALS; ANTIVIRAL AGENTS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, VIRAL; FEMALE; INFLUENZA A VIRUS, H1N1 SUBTYPE; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

INFLUENZA A VIRUS; MUS; ORTHOMYXOVIRIDAE;

EID: 84864930532     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2012.07.002     Document Type: Article

References (50)

1. Bantia S., Kellogg D., Parker C.D., Babu Y.S. Combination of peramivir and rimantadine demonstrate synergistic antiviral effects in sub-lethal influenza A (H3N2) virus mouse model. Antiviral Res. 2010, 88:276-280.
2. Barnard D.L. Animal models for the study of influenza pathogenesis and therapy. Antiviral Res. 2009, 82:A110-122.
3. Baz M., Abed Y., Nehme B., Boivin G. Activity of the oral neuraminidase inhibitor A-322278 against the oseltamivir-resistant H275Y (A/H1N1) influenza virus mutant in mice. Antimicrob. Agents Chemother. 2009, 53:791-793.
4. Baz M., Abed Y., Simon P., Hamelin M.E., Boivin G. Effect of the neuraminidase mutation H275Y conferring resistance to oseltamivir on the replicative capacity and virulence of old and recent human influenza A(H1N1) viruses. J. Infect. Dis. 2010, 201:740-745.
5. Besselaar T.G., Naidoo D., Buys A., Gregory V., McAnerney J., Manamela J.M., Blumberg L., Schoub B.D. Widespread oseltamivir resistance in influenza A viruses (H1N1), South Africa. Emerg. Infect. Dis. 2008, 14:1809-1810.
6. Carr J., Ives J., Kelly L., Lambkin R., Oxford J., Mendel D., Tai L., Roberts N. 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. 2002, 54:79-88.
7. Chen H., Cheung C.L., Tai H., Zhao P., Chan J.F., Cheng V.C., Chan K.H., Yuen K.Y. Oseltamivir-resistant influenza A pandemic (H1N1) 2009 virus, Hong Kong. Chin. Emerg. Infect. Dis. 2009, 15:1970-1972.
8. Dharan N.J., Gubareva L.V., Meyer J.J., Okomo-Adhiambo M., McClinton R.C., Marshall S.A., St George K., Epperson S., Brammer L., Klimov A.I., Bresee J.S., Fry A.M. Infections with oseltamivir-resistant influenza A(H1N1) virus in the United States. JAMA 2009, 301:1034-1041.
9. Eriksson B., Helgstrand E., Johansson N.G., Larsson A., Misiorny A., Noren J.O., Philipson L., Stenberg K., Stening G., Stridh S., Oberg B. Inhibition of influenza virus ribonucleic acid polymerase by ribavirin triphosphate. Antimicrob. Agents Chemother. 1977, 11:946-951.
10. Furuta Y., Takahashi K., Fukuda Y., Kuno M., Kamiyama T., Kozaki K., Nomura N., Egawa H., Minami S., Watanabe Y., Narita H., Shiraki K. In vitro and in vivo activities of anti-influenza virus compound T-705. Antimicrob. Agents Chemother. 2002, 46:977-981.
11. Govorkova E.A., Ilyushina N.A., McClaren J.L., Naipospos T.S., Douangngeun B., Webster R.G. Susceptibility of highly pathogenic H5N1 influenza viruses to the neuraminidase inhibitor oseltamivir differs in vitro and in a mouse model. Antimicrob. Agents Chemother. 2009, 53:3088-3096.
12. Govorkova E.A., Webster R.G. Combination chemotherapy for influenza. Viruses 2010, 2:1510-1529.
13. Gubareva L.V., Trujillo A.A., Okomo-Adhiambo M., Mishin V.P., Deyde V.M., Sleeman K., Nguyen H.T., Sheu T.G., Garten R.J., Shaw M.W., Fry A.M., Klimov A.I. Comprehensive assessment of 2009 pandemic influenza A (H1N1) virus drug susceptibility in vitro. Antiviral Ther. 2010, 15:1151-1159.
14. Hamelin M.E., Baz M., Abed Y., Couture C., Joubert P., Beaulieu E., Bellerose N., Plante M., Mallett C., Schumer G., Kobinger G.P., Boivin G. Oseltamivir-resistant pandemic A/H1N1 virus is as virulent as its wild-type counterpart in mice and ferrets. PLoS Pathog. 2010, 6:e1001015.
15. Herlocher M.L., Carr J., Ives J., Elias S., Truscon R., Roberts N., Monto A.S. Influenza virus carrying an R292K mutation in the neuraminidase gene is not transmitted in ferrets. Antiviral Res. 2002, 54:99-111.
16. Hong S.D., Park S.H., Kang S.J., Kwon Y.S., Kee S.J., Park K.H., Jung S.I., Jang H.C. First fatal oseltamivir-resistant 2009 pandemic influenza A (H1N1) case in an adult in Korea. Chonnam Med. J. 2011, 47:127-129.
17. Ilyushina N.A., Hoffmann E., Salomon R., Webster R.G., Govorkova E.A. Amantadine-oseltamivir combination therapy for H5N1 influenza virus infection in mice. Antiviral Ther. 2007, 12:363-370.
18. Ilyushina N.A., Khalenkov A.M., Seiler J.P., Forrest H.L., Bovin N.V., Marjuki H., Barman S., Webster R.G., Webby R.J. Adaptation of pandemic H1N1 influenza viruses in mice. J. Virol. 2010, 84:8607-8616.
19. Ives J.A., Carr J.A., Mendel D.B., Tai C.Y., Lambkin R., Kelly L., Oxford J.S., Hayden F.G., Roberts N.A. The H275Y 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. 2002, 55:307-317.
20. Leonov H., Astrahan P., Krugliak M., Arkin I.T. How do aminoadamantanes block the influenza M2 channel, and how does resistance develop?. J. Am. Chem. Soc. 2011, 133:9903-9911.
21. Meijer, A., Lackenby, A., Hungnes, O., Lina, B., van-der-Werf, S., Schweiger, B., Opp, M., Paget, J., van-de-Kassteele, J., Hay, A., Zambon, M., 2009. Oseltamivir-resistant influenza virus A (H1N1), Europe, 2007-08 season. Emerg. Infect. Dis. 15, 552-560.
22. Mossad S.B. The resurgence of swine-origin influenza A (H1N1). Cleve. Clin. J. Med. 2009, 76:337-343.
23. Nguyen H.T., Sheu T.G., Mishin V.P., Klimov A.I., Gubareva L.V. Assessment of pandemic and seasonal influenza A (H1N1) virus susceptibility to neuraminidase inhibitors in three enzyme activity inhibition assays. Antimicrob. Agents Chemother. 2010, 54:3671-3677.
24. Nguyen J.T., Hoopes J.D., Le M.H., Smee D.F., Patick A.K., Faix D.J., Blair P.J., de Jong M.D., Prichard M.N., Went G.T. Triple combination of amantadine, ribavirin, and oseltamivir is highly active and synergistic against drug resistant influenza virus strains in vitro. PLoS One 2010, 5:e9332.
25. Nguyen J.T., Smee D.F., Barnard D.L., Julander J.G., Gross M., de Jong M.D., Went G.T. Efficacy of combined therapy with amantadine, oseltamivir, and ribavirin in vivo against susceptigble and amantadine-resistnt influenza A viruses. PLoS One 2012, 7:e31006.
26. Otte A., Sauter M., Alleva L., Baumgarte S., Klingel K., Gabriel G. Differential host determinants contribute to the pathogenesis of 2009 pandemic H1N1 and human H5N1 influenza A viruses in experimental mouse models. Am. J. Pathol. 2011, 179:230-239.
27. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2007, 22:659-661.
28. Reed L.J., Muench H. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 1938, 27:493-498.
29. Saito R., Sato I., Suzuki Y., Baranovich T., Matsuda R., Ishitani N., Dapat C., Dapat I.C., Zaraket H., Oguma T., Suzuki H. Reduced effectiveness of oseltamivir in children infected with oseltamivir-resistant influenza A (H1N1) viruses with His275Tyr mutation. Pediatr. Infect. Dis. J. 2010, 29:898-904.
30. Selvam P., Chandramohan M., Hurst B.L., Smee D.F. Activity of isatine-sulfadimidine derivatives against 2009 pandemic H1N1 influenza virus in cell culture. Antivir. Chem. Chemother. 2010, 20:143-146.
31. Selvam P., Murugesh N., Chandramohan M., Sidwell R.W., Wandersee M.K., Smee D.F. Anti-influenza virus activities of 4-[(1,2-dihydro-2-oxo-3H-indol-3-ylidene)amino]-N-(4,6-dimethyl-2-pyrimidi n-2-yl)benzenesulphonamide and its derivatives. Antivir. Chem. Chemother. 2006, 17:269-274.
32. Sidwell R.W., Bailey K.W., Wong M.H., Barnard D.L., Smee D.F. In vitro and in vivo influenza virus-inhibitory effects of viramidine. Antiviral Res. 2005, 68:10-17.
33. Sidwell R.W., Huffman J.H., Barnard D.L., Bailey K.W., Wong M.H., Morrison A., Syndergaard T., Kim C.U. Inhibition of influenza virus infections in mice by GS4104, an orally effective influenza virus neuraminidase inhibitor. Antiviral Res. 1998, 37:107-120.
34. Sidwell R.W., Smee D.F. In vitro and in vivo assay systems for study of influenza virus inhibitors. Antiviral Res. 2000, 48:1-16.
35. Sidwell R.W., Smee D.F., Huffman J.H., Barnard D.L., Bailey K.W., Morrey J.D., Babu Y.S. In vivo influenza virus-inhibitory effects of the cyclopentane neuraminidase inhibitor RJW-270201. Antimicrob. Agents Chemother. 2001, 45:749-757.
36. Sleeman K., Mishin V.P., Deyde V.M., Furuta Y., Klimov A.I., Gubareva L.V. In vitro antiviral activity of favipiravir (T-705) against drug-resistant influenza and 2009 A(H1N1) viruses. Antimicrob. Agents Chemother. 2010, 54:2517-2524.
37. Smee D.F., Huffman J.H., Morrison A.C., Barnard D.L., Sidwell R.W. Cyclopentane neuraminidase inhibitors with potent in vitro anti-influenza virus activities. Antimicrob. Agents Chemother. 2001, 45:743-748.
38. Smee D.F., Hurst B.L., Wong M.H., Bailey K.W., Morrey J.D. Effects of double combinations of amantadine, oseltamivir, and ribavirin on influenza A (H5N1) virus infections in cell culture and in mice. Antimicrob. Agents Chemother. 2009, 53:2120-2128.
39. Smee D.F., Hurst B.L., Wong M.H., Bailey K.W., Tarbet E.B., Morrey J.D., Furuta Y. Effects of the combination of favipiravir (T-705) and oseltamivir on influenza A virus infections in mice. Antimicrob. Agents Chemother. 2010, 54:126-133.
40. Smee D.F., Hurst B.L., Wong M.H., Tarbet E.B., Babu Y.S., Klumpp K., Morrey J.D. Combinations of oseltamivir and peramivir for the treatment of influenza A (H1N1) virus infections in cell culture and in mice. Antiviral Res. 2010, 88:38-44.
41. Smee D.F., Morrison A.C., Barnard D.L., Sidwell R.W. Comparison of colorimetric, fluorometric, and visual methods for determining anti-influenza (H1N1 and H3N2) virus activities and toxicities of compounds. J. Virol. Methods 2002, 106:71-79.
42. Smee D.F., Wandersee M.K., Wong M.H., Bailey K.W., Sidwell R.W. Treatment of mannan-enhanced influenza B virus infections in mice with oseltamivir, ribavirin and viramidine. Antivir. Chem. Chemother. 2004, 15:261-268.
43. Smee D.F., Wong M.H., Bailey K.W., Sidwell R.W. Activities of oseltamivir and ribavirin used alone and in combination against infections in mice with recent isolates of influenza A (H1N1) and B viruses. Antivir. Chem. Chemother. 2006, 17:185-192.
44. Smith J.R., Rayner C.R., Donner B., Wollenhaupt M., Klumpp K., Dutkowski R. Oseltamivir in seasonal, pandemic, and avian influenza: a comprehensive review of 10-years clinical experience. Adv. Ther. 2011, 28:927-959.
45. Southam D.S., Dolovich M., O'Byrne P.M., Inman M.D. Distribution of intranasal instillations in mice. effects of volume, time, body position, and anesthesia. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 282:L833-839.
46. Thorlund K., Awad T., Boivin G., Thabane L. Systematic review of influenza resistance to the neuraminidase inhibitors. BMC Infect. Dis. 2011, 11:134.
47. Valette M., Allard J.P., Aymard M., Millet V. Susceptibilities to rimantadine of influenza A/H1N1 and A/H3N2 viruses isolated during the epidemics of 1988 to 1989 and 1989 to 1990. Antimicrob. Agents Chemother. 1993, 37:2239-2240.
48. Yen H.L., Ilyushina N.A., Salomon R., Hoffmann E., Webster R.G., Govorkova E.A. Neuraminidase inhibitor-resistant recombinant A/Vietnam/1203/04 (H5N1) influenza viruses retain their replication efficiency and pathogenicity in vitro and in vivo. J. Virol. 2007, 81:12418-12426.
49. Yen H.L., Monto A.S., Webster R.G., Govorkova E.A. Virulence may determine the necessary duration and dosage of oseltamivir treatment for highly pathogenic A/Vietnam/1203/04 influenza virus in mice. J. Infect. Dis. 2005, 192:665-672.
50. Zheng B., Chan K.H., Zhang A.J., Zhou J., Chan C.C., Poon V.K., Zhang K., Leung V.H., Jin D.Y., Woo P.C., Chan J.F., To K.K., Chen H., Yuen K.Y. D225G mutation in hemagglutinin of pandemic influenza H1N1 (2009) virus enhances virulence in mice. Exp. Biol. Med. (Maywood) 2010, 235:981-988.