Oseltamivir-ribavirin combination therapy for highly pathogenic H5N1 influenza virus infection in mice

Antimicrobial Agents and Chemotherapy

Volumn 52, Issue 11, 2008, Pages 3889-3897

  Ilyushina, Natalia A ^a,b   Hay, Alan ^c   Yilmaz, Neziha ^d   Boon, Adrianus C M ^a   Webster, Robert G ^a,e   Govorkova, Elena A ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b D I IVANOVSKY INSTITUTE OF VIROLOGY   (Russian Federation)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d Refik Saydam Hygiene Center   (Turkey)

^e UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 ACETAMIDO 5 AMINO 3 (1 ETHYLPROPOXY) 1 CYCLOHEXENE 1 CARBOXYLIC ACID; OSELTAMIVIR; RIBAVIRIN; ZANAMIVIR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; DRUG ANTAGONISM; DRUG DOSE ESCALATION; DRUG DOSE TITRATION; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; IC 50; INFLUENZA; INFLUENZA VIRUS A H5N1; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYSTEM; THREE DIMENSIONAL IMAGING; TURKEY (REPUBLIC); VIET NAM; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; ANTIVIRAL AGENTS; CHEMOKINES; CYTOKINES; DRUG INTERACTIONS; DRUG THERAPY, COMBINATION; FEMALE; INFLUENZA A VIRUS, H5N1 SUBTYPE; LUNG; MICE; MICE, INBRED BALB C; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; RIBAVIRIN; VIRUS REPLICATION;

EID: 55849102109     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01579-07     Document Type: Article

References (50)

1. Beigel, J. H., J. Farrar, A. M. Han, F. G. Hayden, R. Hyer, M. D. de Jong, S. Lochindarat, T. K. Nguyen, T. H. Nguyen, T. H. Tran, A. Nicoll, S. Touch, and K. Y. Yuen. 2005. Avian influenza A (H5N1) infection in humans. N. Engl. J. Med. 353:1374-1385.
2. Cheung, C. L., J. M. Rayner, G. J. Smith, P. Wang, T. S. Naipospos, J. Zhang, K. Y. Yuen, R. G. Webster, J. S. Peiris, Y. Guan, and H. Chen. 2006. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J. Infect. Dis. 193:1626-1629.
3. Cox, D. R. 1972. Regression models and life-tables. J. R. Stat. Soc. B 34:187-220.
4. de Clercq, E. 2006. Antiviral agents active against influenza A viruses. Nat. Rev. 5:1015-1025.
5. de Jong, M. D., T. T. Tran, H. K. Truong, M. H. Vo, G. J. Smith, V. C. Nguyen, V. C. Bach, T. Q. Phan, Q. H. Do, Y. Guan, J. S. Peiris, T. H. Tran, and J. Farrar. 2005. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N. Engl. J. Med. 353:2667-2672.
6. Eriksson, B., B. Helgstrand, N. G. Johansson, A. Larsson, A. Misiorny, J. O. Noren, L. Phillipson, K. Stenberg, G. Stening, S. Stridh, and B. Oberg. 1977. Inhibition of influenza virus ribonucleic acid polymerase by ribavirin triphosphate. Antimicrob. Agents Chemother. 11:946-951.
7. Gilbert, B. E., and V. Knight. 1986. Biochemistry and clinical applications of ribavirin. Antimicrob. Agents Chemother. 30:201-205.
8. Govorkova, E. A., H. B. Fang, M. Tan, and R. G. Webster. 2004. Neuraminidase inhibitor-rimantadine combinations exert additive and synergistic antiinfluenza virus effects in MDCK cells. Antimicrob. Agents Chemother. 48:4855-4863.
9. Govorkova, E. A., N. A. Ilyushina, D. A. Boltz, A. Douglas, N. Yilmaz, and R. G. Webster. 2007. Efficacy of oseltamivir therapy in ferrets inoculated with different clades of H5N1 influenza virus. Antimicrob. Agents Chemother. 51:1414-1424.
10. Hayden, F. G. 2006. Antiviral resistance in influenza viruses - implications for management and pandemic response. N. Engl. J. Med. 354:785-788.
11. Hayden, F. G., and A. J. Hay. 1992. Emergence and transmission of influenza A viruses resistant to amantadine and rimantadine. Curr. Top. Microbiol. Immunol. 176:119-130.
12. Hayden, F. G., C. A. Sable, J. D. Connor, and J. Lane. 1996. Intravenous ribavirin by constant infusion for serious influenza and parainfluenza virus infection. Antivir. Ther. 1:51-56.
13. Hayden, F. G., K. M. Cote, and R. G. Douglas. 1980. Plaque inhibition assay for drug susceptibility testing of influenza viruses. Antimicrob. Agents Chemother. 17:865-870.
14. Hayden, F. G., R. G. Douglas, Jr., and R. Simons. 1980. Enhancement of activity against influenza viruses by combinations of antiviral agents. Antimicrob. Agents Chemother. 18:536-541.
15. Ilyushina, N. A., E. A. Govorkova, and R. G. Webster. 2005. Detection of amantadine-resistant variants among avian influenza viruses isolated in North America and Asia. Virology 341:102-106.
16. Ilyushina, N. A., E. Hoffmann, R. Salomon, R. G. Webster, and E. A. Govorkova. 2007. Amantadine-oseltamivir combination therapy for H5N1 influenza virus infection in mice. Antivir. Ther. 12:363-370.
17. Ilyushina, N. A., N. V. Bovin, R. G. Webster, and E. A. Govorkova. 2006. Combination chemotherapy, a potential strategy for reducing the emergence of drug-resistant influenza A variants. Antivir. Res. 70:121-131.
18. Khare, G. P., R. W. Sidwell, J. T. Witkowski, L. N. Simon, and R. K. Robins. 1973. Suppression by 1-β-D-ribofuranosyl-1,2,4- triazole-3-carboxamine (virazole, ICN 1229) of influenza virus-induced infections in mice. Antimicrob. Agents Chemother. 3:517-522.
19. Kiso, M., K. Mitamura, Y. Sakai-Tagawa, K. Shiraishi, C. Kawakami, K. Kimura, F. G. Hayden, N. Sugaya, and Y. Kawaoka. 2004. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364:759-765.
20. Knight, V., and B. E. Gilbert. 1987. Ribavirin aerosol treatment of influenza. Infect. Dis. Clin. N. Am. 1:441-457.
21. Le, Q. M., M. Kiso, K. Someya, Y. T. Sakai, T. H. Nguyen, K. H. Nguyen, N. D. Pham, H. H. Ngyen, S. Yamada, Y. Muramoto, T. Horimoto, A. Takada, H. Goto, T. Suzuki, Y. Suzuki, and Y. Kawaoka. 2005. Avian flu: isolation of drug-resistant H5N1 virus. Nature 437:1108.
22. Leneva, I. A., N. Roberts, E. A. Govorkova, O. G. Goloubeva, and R. G. Webster. 2001. The neuraminidase inhibitor GS4104 (oseltamivir phosphate) is efficacious against A/Hong Kong/156/97 (H5N1) and A/Hong Kong/1074/99 (H9N2) influenza viruses. Antivir. Res. 48:101-115.
23. Madren, L. K., C. Shipman, and F. G. Hayden. 1995. In vitro inhibitory effects of combinations of anti-influenza agents. Antivir. Chem. Chemother. 6:109-113.
24. McKimm-Breschkin, J. L. 2000. Resistance of influenza viruses to neuraminidase inhibitors - a review. Antivir. Res. 47:1-17.
25. McKimm-Breschkin, J. L. 2005. Management of influenza virus infections with neuraminidase inhibitors: detection, incidence, and implications of drug resistance. Treat. Respir. Med. 4:107-116.
26. McKimm-Breschkin, J. L., P. Selleck, T. Usman, and M. Johnson. 2007. Reduced sensitivity of influenza A (H5N1) to oseltamivir. Emerg. Infect. Dis. 13:1354-1357.
27. Monto, A. S. 2003. The role of antivirals in the control of influenza. Vaccine 21:1796-1800.
28. Peiris, J. S. M., M. D. de Jong, and Y. Guan. 2007. Avian influenza virus (H5N1): a threat to human health. Clin. Mircobiol. Rev. 20:243-267.
29. Potier, M., L. Mameli, M. Belislem, L. Dallaire, and S. B. Melanxon. 1979. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-α-D-N-acetylneuraminate) substrate. Anal. Biochem. 94:287-296.
30. Prichard, M. N., and C. Shipman, Jr. 1990. A three-dimensional model to analyze drug-drug combinations. Antivir. Res. 14:181-206.
31. Prichard, M. N., K. R. Aseltine, and C. Shipman, Jr. 1992. MacSynergy™ II. University of Michigan, Ann Arbor.
32. Reed, L. J., and H. Muench. 1938. A simple method for estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
33. Russell, R. J., L. F. Haire, D. J. Stevens, P. J. Collins, Y. P. Lin, G. M. Blackburn, A. J. Hay, S. J. Gamblin, and J. J. Skehel. 2006. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443:45-49.
34. Saad, M. D., B. R. Boynton, K. C. Earhart, M. M. Mansour, H. L. Niman, N. M. Elsayed, A. L. Nayel, A. S. Abdelghani, H. M. Essmat, E. M. Labib, E. A. Ayoub, and M. R. Monteville. 2007. Detection of oseltamivir resistance mutation N294S in humans with influenza A H5N1, p. 228. Abstr. Options Control Influenza VI, Toronto, Ontario, Canada.
35. Salomon, R., E. Hoffmann, and R. G. Webster. 2007. Inhibition of the cytokine response does not protect against lethal H5N1 influenza infection. Proc. Natl. Acad. Sci. USA 30:12479-12481.
36. Salomon, R., J. Franks, E. A. Govorkova, N. A. Ilyushina, H.-L. Yen, D. Post, J. Humberd, M. Trichet, J. E. Rehg, R. Webby, R. G. Webster, and E. Hoffmann. 2006. The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J. Exp. Med. 203:689-697.
37. Sidwell, R. W., J. H. Huffman, G. P. Khare, L. B. Allen, J. T. Witkowski, and R. K. Robins. 1972. Broad-spectrum antiviral activity of virazole: 1-β-D-ribofuranosyl-1,2,4-triazole-3-carboxamine. Science 177:705-706.
38. Sidwell, R. W., K. W. Bailey, M. H. Wong, D. L. Barnard, and D. F. Smee. 2005. In vitro and in vivo influenza virus - inhibitory effects of viramidine. Antivir. Res. 68:10-17.
39. Smee, D. F., M. H. Wong, K. W. Bailey, and R. W. Sidwell. 2006. 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. 17:185-192.
40. Smee, D. F., K. W. Bailey, A. C. Morrison, and R. W. Sidwell. 2002. Combination treatment of influenza A virus infections in cell culture and in mice with the cyclopentane neuraminidase inhibitor RWJ-270201 and ribavirin. Chemotherapy 48:88-93.
41. Sweeny, D. J., G. Lynch, A. M. Bidgood, W. Lew, K. Y. Wang, and K. C. Cundy. 2000. Metabolism of the influenza neuraminidase inhibitor prodrug oseltamivir in the rat. Drug Metab. Dispos. 28:737-741.
42. Szretter, K. J., S. Gandappa, X. Lu, C. Smith, W. J. Shieh, S. R. Saki, S. Sambhara, T. M. Tumpey, and J. M. Katz. 2007. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J. Virol. 81:2736-2744.
43. Venables, W. N., and B. D. Ripley. 1997. Modern applied statistics, p. 223-242, 297-321, 345-350. Springer, New York, NY.
44. Webster, R. G., and E. A. Govorkova. 2006. H5N1 influenza-continuing evolution and spread. N. Engl. J. Med. 355:2174- 2177.
45. Wilson, S. Z., V. Knight, P. R. Wyde, S. Drake, and R. B. Couch. 1980. Amantadine and ribavirin aerosol treatment of influenza A and B infection in mice. Antimicrob. Agents Chemother. 17:642-648.
46. World Health Organization. 2007. Towards a unified nomenclature system for the highly pathogenic H5N1 avian influenza viruses (EPR). World Health Organization, Geneva, Switzerland. http://www.who.int/csr/disease/ avian_influenza/guidelines/nomenclature/en/index.html.
47. World Health Organization. 2008. H5N1 avian influenza: timeline of major events. World Health Organization, Geneva, Switzerland. http://www.who.int/csr/disease/ avian_influenza/ai_timeline/en/index.html.
48. Wray, S. K., B. E. Gilbert, and V. Knight. 1985. Effect of ribavirin triphosphate on primer generation and elongation during influenza virus transcription in vitro. Antivir. Res. 5:39-48.
49. Yen, H.-L., A. S. Monto, R. G. Webster, and E. A. Govorkova. 2005. 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. 192:665-672.
50. Zambon, M., and F. G. Hayden. 2001. Position statement: global neuraminidase inhibitor susceptibility network. Antivir. Res. 49:147-156.