Oseltamivir inhibits influenza virus replication and transmission following ocular-only aerosol inoculation of ferrets

Virology

Volumn 484, Issue , 2015, Pages 305-312

  Belser, Jessica A ^a   Maines, Taronna R ^a   Creager, Hannah M ^a,b   Katz, Jacqueline M ^a   Tumpey, Terrence M ^a  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Aerosol; Antiviral; Ferret model; Influenza virus; Oseltamivir (Tamiflu); Transmission

Indexed keywords

4 ACETAMIDO 5 AMINO 3 (1 ETHYLPROPOXY) 1 CYCLOHEXENE 1 CARBOXYLIC ACID; OSELTAMIVIR; ANTIVIRUS AGENT;

2009 H1N1 INFLUENZA; AEROSOL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CORNEA EPITHELIUM; DRUG EFFICACY; FERRET; HUMAN; HUMAN CELL; INFLUENZA A; INFLUENZA A (H1N1); INFLUENZA A VIRUS; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H7N3); INFLUENZA A VIRUS (H7N9); INOCULATION; MALE; NONHUMAN; PRIORITY JOURNAL; SEROCONVERSION; VIRUS DETECTION; VIRUS ENTRY; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS TRANSMISSION; ANIMAL; DISEASE MODEL; DRUG EFFECTS; ORAL DRUG ADMINISTRATION; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; PHYSIOLOGY; SURVIVAL; VIROLOGY;

ADMINISTRATION, ORAL; ANIMALS; ANTIVIRAL AGENTS; DISEASE MODELS, ANIMAL; FERRETS; MALE; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; SURVIVAL ANALYSIS; VIRUS REPLICATION;

EID: 84947245038     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.06.020     Document Type: Article

References (41)

1. Avian influenza Outbreak in the United Kingdom. Euro Surveill. 2007, 12(E070531):070532.
2. Aamir U.B., Naeem K., Ahmed Z., Obert C.A., Franks J., Krauss S., Seiler P., Webster R.G. Zoonotic potential of highly pathogenic avian H7N3 influenza viruses from Pakistan. Virology 2009, 390:212-220.
3. Belser J.A., Davis C.T., Balish A., Edwards L.E., Zeng H., Maines T.R., Gustin K.M., Martinez I.L., Fasce R., Cox N.J., Katz J.M., Tumpey T.M. Pathogenesis, transmissibility, and ocular tropism of a highly pathogenic avian influenza A (H7N3) virus associated with human conjunctivitis. J. Virol. 2013, 87:5746-5754.
4. Belser J.A., Gustin K.M., Katz J.M., Maines T.R., Tumpey T.M. Influenza virus infectivity and virulence following ocular-only aerosol inoculation of ferrets. J. Virol. 2014, 88:9647-9654.
5. Belser J.A., Gustin K.M., Maines T.R., Pantin-Jackwood M.J., Katz J.M., Tumpey T.M. Influenza virus respiratory infection and transmission following ocular inoculation in ferrets. PLoS Pathog. 2012, 8:e1002569.
6. Belser J.A., Katz J.M., Tumpey T.M. The ferret as a model organism to study influenza A virus infection. Dis. Models & Mech. 2011, 4:575-579.
7. Belser J.A., Rota P.A., Tumpey T.M. Ocular tropism of respiratory viruses. Microbiol. Mol. Biol. Rev. 2013, 77:144-156.
8. Belser J.A., Sleeman K., Pearce M.B., Katz J.M., Gubareva L.V., Tumpey T.M. Oseltamivir inhibits H7 influenza virus replication in mice inoculated by the ocular route. Antimicrob. Agents Chemother. 2012, 56:1616-1618.
9. Belser J.A., Wadford D.A., Xu J., Katz J.M., Tumpey T.M. Ocular infection of mice with influenza A (H7) viruses: a site of primary replication and spread to the respiratory tract. J. Virol. 2009, 83:7075-7084.
10. Belser J.A., Zeng H., Katz J.M., Tumpey T.M. Ocular tropism of influenza A viruses: identification of H7 subtype-specific host responses in human respiratory and ocular cells. J. Virol. 2011, 85:10117-10125.
11. Boltz D.A., Rehg J.E., McClaren J., Webster R.G., Govorkova E.A. Oseltamivir prophylactic regimens prevent H5N1 influenza morbidity and mortality in a ferret model. J. Infect. Dis. 2008, 197:1315-1323.
12. Chan M.C., Chan R.W., Yu W.C., Ho C.C., Yuen K.M., Fong J.H., Tang L.L., Lai W.W., Lo A.C., Chui W.H., Sihoe A.D., Kwong D.L., Wong D.S., Tsao G.S., Poon L.L., Guan Y., Nicholls J.M., Peiris J.S. Tropism and innate host responses of the 2009 pandemic H1N1 influenza virus in ex vivo and in vitro cultures of human conjunctiva and respiratory tract. Am. J. Pathol. 2010, 176:1828-1840.
13. Chosewood, L.C., Wilson, D.E., Centers for Disease Control and Prevention (U.S.), National Institutes of Health (U.S.), 2009Biosafety in microbiological and biomedical laboratories, 5th ed. U.S. Dept. of Health and Human Services, Public Health Service, Centers for Disease Control and Prevention, National Institutes of Health, Washington, D.C.
14. Davies B.E. Pharmacokinetics of oseltamivir: an oral antiviral for the treatment and prophylaxis of influenza in diverse populations. J. Antimicrob. Chemother. 2010, 65(Suppl 2). ii5-ii10.
15. Gao R., Cao B., Hu Y., Feng Z., Wang D., Hu W., Chen J., Jie Z., Qiu H., Xu K., Xu X., Lu H., Zhu W., Gao Z., Xiang N., Shen Y., He Z., Gu Y., Zhang Z., Yang Y., Zhao X., Zhou L., Li X., Zou S., Zhang Y., Li X., Yang L., Guo J., Dong J., Li Q., Dong L., Zhu Y., Bai T., Wang S., Hao P., Yang W., Zhang Y., Han J., Yu H., Li D., Gao G.F., Wu G., Wang Y., Yuan Z., Shu Y. Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 2013, 368:1888-1897.
16. Govorkova E.A., Ilyushina N.A., Boltz D.A., Douglas A., Yilmaz N., Webster R.G. Efficacy of oseltamivir therapy in ferrets inoculated with different clades of H5N1 influenza virus. Antimicrob. Agents Chemother. 2007, 51:1414-1424.
17. Govorkova E.A., Marathe B.M., Prevost A., Rehg J.E., Webster R.G. Assessment of the efficacy of the neuraminidase inhibitor oseltamivir against 2009 pandemic H1N1 influenza virus in ferrets. Antivir. Res. 2011, 91:81-88.
18. Gustin K.M., Belser J.A., Katz J.M., Tumpey T.M., Maines T.R. Innovations in modeling influenza virus infections in the laboratory. Trends Microbiol. 2012, 20:275-281.
19. Gustin K.M., Katz J.M., Tumpey T.M., Maines T.R. Comparison of the levels of infectious virus in respirable aerosols exhaled by ferrets infected with influenza viruses exhibiting diverse transmissibility phenotypes. J. Virol. 2013, 87:7864-7873.
20. Ilyushina N.A., Bovin N.V., Webster R.G., Govorkova E.A. Combination chemotherapy, a potential strategy for reducing the emergence of drug-resistant influenza A variants. Antivir. Res. 2006, 70:121-131.
21. Ison M.G. Optimizing antiviral therapy for influenza: understanding the evidence. Expert Rev. Anti-Infect. Ther. 2015, 13:417-425.
22. Kirkeby S., Martel C.J., Aasted B., Vorum H. Carbohydrate determinants in ferret conjunctiva are affected by infection with influenza H1N1 virus. Curr. Eye Res. 2013, 38:1027-1035.
23. Koopmans M., Wilbrink B., Conyn M., Natrop G., van der Nat H., Vennema H., Meijer A., van Steenbergen J., Fouchier R., Osterhaus A., Bosman A. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 2004, 363:587-593.
24. Lopez-Martinez I., Balish A., Barrera-Badillo G., Jones J., Nunez-Garcia T.E., Jang Y., Aparicio-Antonio R., Azziz-Baumgartner E., Belser J.A., Ramirez-Gonzalez J.E., Pedersen J.C., Ortiz-Alcantara J., Gonzalez-Duran E., Shu B., Emery S.L., Poh M.K., Reyes-Teran G., Vazquez-Perez J.A., Avila-Rios S., Uyeki T., Lindstrom S., Villanueva J., Tokars J., Ruiz-Matus C., Gonzalez-Roldan J.F., Schmitt B., Klimov A., Cox N., Kuri-Morales P., Davis C.T., Diaz-Quinonez J.A. Highly pathogenic avian influenza A(H7N3) virus in poultry workers, Mexico, 2012. Emerg. Infect. Dis. 2013, 19:1531-1534.
25. Maines T.R., Chen L.M., Matsuoka Y., Chen H., Rowe T., Ortin J., Falcon A., Nguyen T.H., Mai le Q., Sedyaningsih E.R., Harun S., Tumpey T.M., Donis R.O., Cox N.J., Subbarao K., Katz J.M. Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc. Natl. Acad. Sci. USA 2006, 103:12121-12126.
26. Maines T.R., Jayaraman A., Belser J.A., Wadford D.A., Pappas C., Zeng H., Gustin K.M., Pearce M.B., Viswanathan K., Shriver Z.H., Raman R., Cox N.J., Sasisekharan R., Katz J.M., Tumpey T.M. Transmission and pathogenesis of swine-origin 2009A(H1N1) influenza viruses in ferrets and mice. Science 2009, 325:484-487.
27. Maines T.R., Lu X.H., Erb S.M., Edwards L., Guarner J., Greer P.W., Nguyen D.C., Szretter K.J., Chen L.M., Thawatsupha P., Chittaganpitch M., Waicharoen S., Nguyen D.T., Nguyen T., Nguyen H.H., Kim J.H., Hoang L.T., Kang C., Phuong L.S., Lim W., Zaki S., Donis R.O., Cox N.J., Katz J.M., Tumpey T.M. Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J. Virol. 2005, 79:11788-11800.
28. Mansour D.E., El-Shazly A.A., Elawamry A.I., Ismail A.T. Comparison of ocular findings in patients with H1N1 influenza infection versus patients receiving influenza vaccine during a pandemic. Ophthalmic Res. 2012, 48:134-138.
29. Marriott A.C., Dove B.K., Whittaker C.J., Bruce C., Ryan K.A., Bean T.J., Rayner E., Pearson G., Taylor I., Dowall S., Plank J., Newman E., Barclay W.S., Dimmock N.J., Easton A.J., Hallis B., Silman N.J., Carroll M.W. Low dose influenza virus challenge in the ferret leads to increased virus shedding and greater sensitivity to oseltamivir. PloS One 2014, 9:e94090.
30. Michaelis M., Geiler J., Klassert D., Doerr H.W., Cinatl J. Infection of human retinal pigment epithelial cells with influenza A viruses. Investig. Ophthalmol. Vis. Sci. 2009, 50:5419-5425.
31. Milton D.K., Fabian M.P., Cowling B.J., Grantham M.L., McDevitt J.J. Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks. PLoS Pathog. 2013, 9:e1003205.
32. Oh D.Y., Lowther S., McCaw J.M., Sullivan S.G., Leang S.K., Haining J., Arkinstall R., Kelso A., McVernon J., Barr I.G., Middleton D., Hurt A.C. 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, 69:2458-2469.
33. Skevaki C.L., Galani I.E., Pararas M.V., Giannopoulou K.P., Tsakris A. Treatment of viral conjunctivitis with antiviral drugs. Drugs 2011, 71:331-347.
34. Sun R., Luo J., Gao Y., He H. Different infection routes of avian influenza A (H5N1) virus in mice. Integr. Zool. 2009, 4:402-408.
35. Tam J.S. Influenza A (H5N1) in Hong Kong: an overview. Vaccine 2002, 20(Suppl 2):S77-S81.
36. Tellier R. Aerosol transmission of influenza A virus: a review of new studies. J. R. Soc. Interface 2009, 6(Suppl 6):S783-S790.
37. Tweed S.A., Skowronski D.M., David S.T., Larder A., Petric M., Lees W., Li Y., Katz J., Krajden M., Tellier R., Halpert C., Hirst M., Astell C., Lawrence D., Mak A. Human illness from avian influenza H7N3, British Columbia. Emerg. Infect. Dis. 2004, 10:2196-2199.
38. Watanabe T., Kiso M., Fukuyama S., Nakajima N., Imai M., Yamada S., Murakami S., Yamayoshi S., Iwatsuki-Horimoto K., Sakoda Y., Takashita E., McBride R., Noda T., Hatta M., Imai H., Zhao D., Kishida N., Shirakura M., de Vries R.P., Shichinohe S., Okamatsu M., Tamura T., Tomita Y., Fujimoto N., Goto K., Katsura H., Kawakami E., Ishikawa I., Watanabe S., Ito M., Sakai-Tagawa Y., Sugita Y., Uraki R., Yamaji R., Eisfeld A.J., Zhong G., Fan S., Ping J., Maher E.A., Hanson A., Uchida Y., Saito T., Ozawa M., Neumann G., Kida H., Odagiri T., Paulson J.C., Hasegawa H., Tashiro M., Kawaoka Y. Characterization of H7N9 influenza A viruses isolated from humans. Nature 2013, 501:551-555.
39. Wattanagoon Y., Stepniewska K., Lindegardh N., Pukrittayakamee S., Silachamroon U., Piyaphanee W., Singtoroj T., Hanpithakpong W., Davies G., Tarning J., Pongtavornpinyo W., Fukuda C., Singhasivanon P., Day N.P., White N.J. Pharmacokinetics of high-dose oseltamivir in healthy volunteers. Antimicrob. Agents Chemother. 2009, 53:945-952.
40. Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza, A.V., Abdel-Ghafar A.N., Chotpitayasunondh T., Gao Z., Hayden F.G., Nguyen D.H., de Jong M.D., Naghdaliyev A., Peiris J.S., Shindo N., Soeroso S., Uyeki T.M. Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med. 2008, 358:261-273.
41. Zeng H., Goldsmith C., Thawatsupha P., Chittaganpitch M., Waicharoen S., Zaki S., Tumpey T.M., Katz J.M. Highly pathogenic avian influenza H5N1 viruses elicit an attenuated type i interferon response in polarized human bronchial epithelial cells. J. Virol. 2007, 81:12439-12449.