Animal models for influenza virus pathogenesis, transmission, and immunology

Journal of Immunological Methods

Volumn 410, Issue , 2014, Pages 60-79

  Thangavel, Rajagowthamee R ^a   Bouvier, Nicole M ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Animal model; Ferret; Guinea pig; Immunology; Influenza; Mouse

Indexed keywords

2009 H1N1 INFLUENZA; ADAPTIVE IMMUNITY; ANIMAL MODEL; ANOREXIA; AVIAN INFLUENZA; BACTERIAL PNEUMONIA; CELLULAR IMMUNITY; CHILL; COUGHING; FERRET; FEVER; GUINEA PIG; HEADACHE; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA A; INFLUENZA B; INFLUENZA VIRUS; INNATE IMMUNITY; LETHARGY; MOUSE; MYALGIA; NONHUMAN; NOSE OBSTRUCTION; NOSE SECRETION; PANDEMIC INFLUENZA; PHARYNGITIS; REVIEW; VIRUS ENTRY; VIRUS PATHOGENESIS; VIRUS PNEUMONIA; VIRUS REPLICATION; VIRUS SHEDDING; VIRUS TRANSMISSION; ANIMAL; DISEASE MODEL; DISEASE TRANSMISSION; FEMALE; INFLUENZA VIRUS A; MALE; METABOLISM; PATHOGENICITY; PATHOLOGY; SEVERITY OF ILLNESS INDEX;

ANIMAL MODEL; FERRET; GUINEA PIG; IMMUNOLOGY; INFLUENZA; MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FERRETS; GUINEA PIGS; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MALE; MICE; SEVERITY OF ILLNESS INDEX;

EID: 84908511240     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2014.03.023     Document Type: Review

References (228)

1. Abed Y., Pizzorno A., Bouhy X., Boivin G. Role of permissive neuraminidase mutations in influenza A/Brisbane/59/2007-like (H1N1) viruses. PLoS Pathog. 2011, 7:e1002431.
2. Alford R.H., Kasel J.A., Gerone P.J., Knight V. Human influenza resulting from aerosol inhalation. Proc. Soc. Exp. Biol. Med. 1966, 122:800.
3. Andrewes C.H., Glover R.E. Spread of infection from the respiratory tract of the ferret: I. Transmission of influenza A virus. Br. J. Exp. Pathol. 1941, 22:91.
4. Animal Research Review Panel Animal Welfare Branch NSW Department of Primary Industries. ARRP Guideline 21: Guidelines for the housing of guinea pigs in scientific institutions 2006, Orange, NSW, (http://www.animalethics.org.au/__data/assets/pdf_file/0012/222510/housing-guinea-pigs-scientific-institutions.pdf).
5. Animals (Scientific Procedures) Act 1986c. 14, Her Majesty's Stationery Office, London http://www.legislation.gov.uk/ukpga/1986/14/enacted.
6. Azoulay-Dupuis E., Lambre C.R., Soler P., Moreau J., Thibon M. Lung alterations in guinea-pigs infected with influenza virus. J. Comp. Pathol. 1984, 94:273.
7. Banks R. The Guinea Pig: Biology, Care, Identification, Nomenclature, Breeding, and Genetics. USAMRIID Seminar Series 1989, (http://netvet.wustl.edu/species/guinea/guinpig.txt).
8. Barnard D.L. Animal models for the study of influenza pathogenesis and therapy. Antiviral Res. 2009, 82:A110.
9. Belser J.A., Blixt O., Chen L.M., Pappas C., Maines T.R., Van Hoeven N., Donis R., Busch J., McBride R., Paulson J.C., Katz J.M., Tumpey T.M. Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7558.
10. Belser J.A., Szretter K.J., Katz J.M., Tumpey T.M. Use of animal models to understand the pandemic potential of highly pathogenic avian influenza viruses. Adv. Virus Res. 2009, 73:55.
11. Belser J.A., Katz J.M., Tumpey T.M. The ferret as a model organism to study influenza A virus infection. Dis. Model. Mech. 2011, 4:575.
12. Belser J.A., Gustin K.M., Pearce M.B., Maines T.R., Zeng H., Pappas C., Sun X., Carney P.J., Villanueva J.M., Stevens J., Katz J.M., Tumpey T.M. Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice. Nature 2013, 501:556.
13. Belser J.A., Maines T.R., Katz J.M., Tumpey T.M. Considerations regarding appropriate sample size for conducting ferret transmission experiments. Future Microbiol 2013, 8:961.
14. Berryman J.C. Guinea-pig vocalizations: their structure, causation and function. Z. Tierpsychol. 1976, 41:80.
15. Bodewes R., Rimmelzwaan G.F., Osterhaus A.D. Animal models for the preclinical evaluation of candidate influenza vaccines. Expert Rev. Vaccines 2010, 9:59.
16. Bodewes R., Kreijtz J.H., van Amerongen G., Fouchier R.A., Osterhaus A.D., Rimmelzwaan G.F., Kuiken T. Pathogenesis of Influenza A/H5N1 virus infection in ferrets differs between intranasal and intratracheal routes of inoculation. Am. J. Pathol. 2011, 179:30.
17. Bodewes R., Geelhoed-Mieras M.M., Wrammert J., Ahmed R., Wilson P.C., Fouchier R.A., Osterhaus A.D., Rimmelzwaan G.F. In vitro assessment of the immunological significance of a human monoclonal antibody directed to the influenza a virus nucleoprotein. Clin. Vaccine Immunol. 2013, 20:1333.
18. Bouvier N.M., Lowen A.C. Animal models for influenza virus pathogenesis and transmission. Viruses 2010, 2:1530.
19. Bouvier N.M., Lowen A.C., Palese P. Oseltamivir-resistant influenza A viruses are transmitted efficiently among guinea pigs by direct contact but not by aerosol. J. Virol. 2008, 82:10052.
20. Bouvier N.M., Rahmat S., Pica N. Enhanced mammalian transmissibility of seasonal influenza A/H1N1 viruses encoding an oseltamivir-resistant neuraminidase. J. Virol. 2012, 86:7268.
21. Bowen L.E., Rivers K., Trombley J.E., Bohannon J.K., Li S.X., Boydston J.A., Eichelberger M.C. Development of a murine nose-only inhalation model of influenza: comparison of disease caused by instilled and inhaled A/PR/8/34. Front. Cell Infect. Microbiol. 2012, 2:74.
22. Brankston G., Gitterman L., Hirji Z., Lemieux C., Gardam M. Transmission of influenza A in human beings. Lancet Infect. Dis. 2007, 7:257.
23. Bushnell R.V., Tobin J.K., Long J., Schultz-Cherry S., Chaudhuri A.R., Nara P.L., Tobin G.J. Serological characterization of guinea pigs infected with H3N2 human influenza or immunized with hemagglutinin protein. Virol. J. 2010, 7:200.
24. Buxton Bridges C., Kuehnert M.J., Hall C.B. Transmission of influenza: implications for control in health care settings. Clin. Infect. Dis. 2003, 37:1094.
25. Call S.A., Vollenweider M.A., Hornung C.A., Simel D.L., McKinney W.P. Does this patient have influenza?. JAMA 2005, 293:987.
26. Cameron C.M., Cameron M.J., Bermejo-Martin J.F., Ran L., Xu L., Turner P.V., Ran R., Danesh A., Fang Y., Chan P.K., Mytle N., Sullivan T.J., Collins T.L., Johnson M.G., Medina J.C., Rowe T., Kelvin D.J. Gene expression analysis of host innate immune responses during lethal H5N1 infection in ferrets. J. Virol. 2008, 82:11308.
27. Canning B.J., Chou Y. Using guinea pigs in studies relevant to asthma and COPD. Pulm. Pharmacol. Ther. 2008, 21:702.
28. Carcione D., Giele C.M., Goggin L.S., Kwan K.S., Smith D.W., Dowse G.K., Mak D.B., Effler P. Secondary attack rate of pandemic influenza A(H1N1) 2009 in Western Australian households, 29 May-7 August 2009. Euro Surveill. 2011, 16.
29. Carrat F., Vergu E., Ferguson N.M., Lemaitre M., Cauchemez S., Leach S., Valleron A.J. Time lines of infection and disease in human influenza: a review of volunteer challenge studies. Am. J. Epidemiol. 2008, 167:775.
30. Cauchemez S., Donnelly C.A., Reed C., Ghani A.C., Fraser C., Kent C.K., Finelli L., Ferguson N.M. Household transmission of 2009 pandemic influenza A (H1N1) virus in the United States. N. Engl. J. Med. 2009, 361:2619.
31. Chao D.L., Bloom J.D., Kochin B.F., Antia R., Longini I.M. The global spread of drug-resistant influenza. J. R. Soc. Interface 2012, 9:648.
32. Chia R., Achilli F., Festing M.F., Fisher E.M. The origins and uses of mouse outbred stocks. Nat. Genet. 2005, 37:1181.
33. Cohen J. Avian influenza. The limits of avian flu studies in ferrets. Science 2012, 335:512.
34. Conenello G.M., Zamarin D., Perrone L.A., Tumpey T., Palese P. A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog. 2007, 3:1414.
35. D'Aoust M.A., Couture M.M., Charland N., Trepanier S., Landry N., Ors F., Vezina L.P. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol. J. 2010, 8:607.
36. de Jong M.D., Simmons C.P., Thanh T.T., Hien V.M., Smith G.J., Chau T.N., Hoang D.M., Chau N.V., Khanh T.H., Dong V.C., Qui P.T., Cam B.V., Ha do Q., Guan Y., Peiris J.S., Chinh N.T., Hien T.T., Farrar J. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 2006, 12:1203.
37. Di Palma F., Gnerre S., Mauceli E., Grabherr M., Johnson J., Chang J., Lander E.S., Lindblad-Toh K., The Genome Sequencing Platform and the Genome Assembly Team Version 3 of the genome sequence of Cavia porcellus (guinea pig). GenBank: AAKN00000000.2 2008, Broad Institute of MIT and Harvard, Cambridge, MA, (http://0-www.ncbi.nlm.nih.gov.elis.tmu.edu.tw/nuccore/AAKN00000000.2).
38. DiLillo D.J., Tan G.S., Palese P., Ravetch J.V. Broadly neutralizing hemagglutinin stalk-specific antibodies require Fc gamma R interactions for protection against influenza virus in vivo. Nat. Med. 2014, 20:143.
39. Donnelly C.A., Finelli L., Cauchemez S., Olsen S.J., Doshi S., Jackson M.L., Kennedy E.D., Kamimoto L., Marchbanks T.L., Morgan O.W., Patel M., Swerdlow D.L., Ferguson N.M. Serial intervals and the temporal distribution of secondary infections within households of 2009 pandemic influenza A (H1N1): implications for influenza control recommendations. Clin. Infect. Dis. 2011, 52(Suppl. 1):S123.
40. Duan S., Boltz D.A., Seiler P., Li J., Bragstad K., Nielsen L.P., Webby R.J., Webster R.G., Govorkova E.A. Oseltamivir-resistant pandemic H1N1/2009 influenza virus possesses lower transmissibility and fitness in ferrets. PLoS Pathog. 2010, 6:e1001022.
41. Eaton M.D. Transmission of epidemic influenza virus in mice by contact. J. Bacteriol. 1940, 39:229.
42. Eichelberger M.C., Green M.D. Animal models to assess the toxicity, immunogenicity and effectiveness of candidate influenza vaccines. Expert Opin. Drug Metab. Toxicol. 2011, 7:1117.
43. Eisenlohr L.C., Luckashenak N., Apcher S., Miller M.A., Sinnathamby G. Beyond the classical: influenza virus and the elucidation of alternative MHC class II-restricted antigen processing pathways. Immunol. Res. 2011, 51:237.
44. Evans D.G. Wilson Smith. 1897-1965. Biogr. Mem. Fellows R. Soc. 1966, 12:478.
45. Fehlmann H.U., Gasser M., Jegge S. Comparison of cellular and humoral immunity to influenza virus in the guinea pig. Pathol. Microbiol. (Basel) 1974, 40:231.
46. Fonseca K., Lavoie M. Avian influenza, human (13): Canada ex China (Beijing), H5N1, fatal, case report. ProMED Mail 2014, International Society for Infectious Diseases, Brookline, MA, (http://www.promedmail.org/direct.php?id=20140112.2167282).
47. Fornek J.L., Korth M.J., Katze M.G. Use of functional genomics to understand influenza-host interactions. Adv. Virus Res. 2007, 70:81.
48. France A.M., Jackson M., Schrag S., Lynch M., Zimmerman C., Biggerstaff M., Hadler J. Household transmission of 2009 influenza A(H1N1) virus after a school-based outbreak in New York City, April- May 2009. J. Infect. Dis. 2010, 201:984.
49. Francis T. Transmission of Influenza by a filterable virus. Science 1934, 80:457.
50. Francis T., Magill T.P. Immunological studies with the virus of influenza. J. Exp. Med. 1935, 62:505.
51. Francis T., Stuart-Harris C.H. Studies on the nasal histology of epidemic influenza virus infection in the ferret: I. The development and repair of the nasal lesion. J. Exp. Med. 1938, 68:789.
52. Frank A.L., Taber L.H., Wells C.R., Wells J.M., Glezen W.P., Paredes A. Patterns of shedding of myxoviruses and paramyxoviruses in children. J. Infect. Dis. 1981, 144:433.
53. Fukushi M., Ito T., Oka T., Kitazawa T., Miyoshi-Akiyama T., Kirikae T., Yamashita M., Kudo K. Serial histopathological examination of the lungs of mice infected with influenza A virus PR8 strain. PLoS ONE 2011, 6:e21207.
54. Gabbard J.D., Dlugolenski D., Van Riel D., Marshall N., Galloway S.E., Howerth E.W., Campbell P.J., Jones C., Johnson S., Byrd-Leotis L., Steinhauer D.A., Kuiken T., Tompkins S.M., Tripp R., Lowen A.C., Steel J. Novel H7N9 influenza virus shows low infectious dose, high growth rate, and efficient contact transmission in the guinea pig model. J. Virol. 2013, 88:1502.
55. Gambotto A., Barratt-Boyes S.M., de Jong M.D., Neumann G., Kawaoka Y. Human infection with highly pathogenic H5N1 influenza virus. Lancet 2007, 371:1464.
56. Gao Y., Zhang Y., Shinya K., Deng G., Jiang Y., Li Z., Guan Y., Tian G., Li Y., Shi J., Liu L., Zeng X., Bu Z., Xia X., Kawaoka Y., Chen H. Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLoS Pathog. 2009, 5:e1000709.
57. Glatman-Freedman A., Portelli I., Jacobs S.K., Mathew J.I., Slutzman J.E., Goldfrank L.R., Smith S.W. Attack rates assessment of the 2009 pandemic H1N1 influenza A in children and their contacts: a systematic review and meta-analysis. PLoS ONE 2012, 7:e50228.
58. Glezen W.P. Influenza control. N. Engl. J. Med. 2006, 355:79.
59. Gocnikova H., Russ G. Influenza A virus PB1-F2 protein. Acta Virol. 2007, 51:101.
60. Goto H., Wells K., Takada A., Kawaoka Y. Plasminogen-binding activity of neuraminidase determines the pathogenicity of influenza A virus. J. Virol. 2001, 75:9297.
61. Govorkova E.A. Consequences of resistance: In vitro fitness, in vivo infectivity, and transmissibility of oseltamivir-resistant influenza A viruses. Influenza Other Respir. Viruses 2013, 7(Suppl. 1):50.
62. Govorkova E.A., Rehg J.E., Krauss S., Yen H.L., Guan Y., Peiris M., Nguyen T.D., Hanh T.H., Puthavathana P., Long H.T., Buranathai C., Lim W., Webster R.G., Hoffmann E. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J. Virol. 2005, 79:2191.
63. Gumbel E.J. The limiting form of Poisson's distribution. Phys. Rev. Lett. 1941, 60:689.
64. Gustin K.M., Belser J.A., Wadford D.A., Pearce M.B., Katz J.M., Tumpey T.M., Maines T.R. Influenza virus aerosol exposure and analytical system for ferrets. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8432.
65. 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.
66. Haas L.E., Thijsen S.F., van Elden L., Heemstra K.A. Human metapneumovirus in adults. Viruses 2013, 5:87.
67. Hai R., Schmolke M., Leyva-Grado V.H., Thangavel R.R., Margine I., Jaffe E.L., Krammer F., Solorzano A., Garcia-Sastre A., Palese P., Bouvier N.M. Influenza A(H7N9) virus gains neuraminidase inhibitor resistance without loss of in vivo virulence or transmissibility. Nat. Commun. 2013, 4:2854.
68. Hale B.G., Albrecht R.A., Garcia-Sastre A. Innate immune evasion strategies of influenza viruses. Future Microbiol 2010, 5:23.
69. Hall C.B. Nosocomial viral respiratory infections: perennial weeds on pediatric wards. Am. J. Med. 1981, 70:670.
70. Hall C.B., Douglas R.G., Geiman J.M., Meagher M.P. Viral shedding patterns of children with influenza B infection. J. Infect. Dis. 1979, 140:610.
71. Hamouda T., Sutcliffe J.A., Ciotti S., Baker J.R. Intranasal immunization of ferrets with commercial trivalent influenza vaccines formulated in a nanoemulsion-based adjuvant. Clin. Vaccine Immunol. 2011, 18:1167.
72. Hashimoto G., Wright P.F., Karzon D.T. Ability of human cord blood lymphocytes to mediate antibody-dependent cellular cytotoxicity against influenza virus-infected cells. Infect. Immun. 1983, 42:214.
73. Hashimoto G., Wright P.F., Karzon D.T. Antibody-dependent cell-mediated cytotoxicity against influenza virus-infected cells. J. Infect. Dis. 1983, 148:785.
74. Herfst S., Schrauwen E.J., Linster M., Chutinimitkul S., de Wit E., Munster V.J., Sorrell E.M., Bestebroer T.M., Burke D.F., Smith D.J., Rimmelzwaan G.F., Osterhaus A.D., Fouchier R.A. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012, 336:1534.
75. Herlocher M.L., Elias S., Truscon R., Harrison S., Mindell D., Simon C., Monto A.S. Ferrets as a transmission model for influenza: sequence changes in HA1 of type A (H3N2) virus. J. Infect. Dis. 2001, 184:542.
76. 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. Antivir. Res. 2002, 54:99.
77. Herlocher M.L., Truscon R., Elias S., Yen H.L., Roberts N.A., Ohmit S.E., Monto A.S. Influenza viruses resistant to the antiviral drug oseltamivir: transmission studies in ferrets. J. Infect. Dis. 2004, 190:1627.
78. Home Office of the Government of the United Kingdom ASPA draft code of practice for all licensed establishments for the care and accommodation of animals. London 2013, (https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/148568/aspa-draft-code-of-practice.pdf).
79. Houser K.V., Pearce M.B., Katz J.M., Tumpey T.M. Impact of prior seasonal H3N2 influenza vaccination or infection on protection and transmission of emerging variants of influenza A(H3N2)v virus in ferrets. J. Virol. 2013, 87:13480.
80. Huang S.S., Banner D., Fang Y., Ng D.C., Kanagasabai T., Kelvin D.J., Kelvin A.A. Comparative analyses of pandemic H1N1 and seasonal H1N1, H3N2, and influenza B infections depict distinct clinical pictures in ferrets. PLoS ONE 2011, 6:e27512.
81. Huang Y., Zaas A.K., Rao A., Dobigeon N., Woolf P.J., Veldman T., Oien N.C., McClain M.T., Varkey J.B., Nicholson B., Carin L., Kingsmore S., Woods C.W., Ginsburg G.S., Hero A.O. Temporal dynamics of host molecular responses differentiate symptomatic and asymptomatic influenza A infection. PLoS Genet. 2011, 7:e1002234.
82. Huang S.S., Banner D., Degousee N., Leon A.J., Xu L., Paquette S.G., Kanagasabai T., Fang Y., Rubino S., Rubin B., Kelvin D.J., Kelvin A.A. Differential pathological and immune responses in newly weaned ferrets are associated with a mild clinical outcome of pandemic 2009 H1N1 infection. J. Virol. 2012, 86:13187.
83. Hurt A.C., Nor'e S.S., McCaw J.M., Fryer H.R., Mosse J., McLean A.R., Barr I.G. Assessing the viral fitness of oseltamivir-resistant influenza viruses in ferrets, using a competitive-mixtures model. J. Virol. 2010, 84:9427.
84. Imai M., Watanabe T., Hatta M., Das S.C., Ozawa M., Shinya K., Zhong G., Hanson A., Katsura H., Watanabe S., Li C., Kawakami E., Yamada S., Kiso M., Suzuki Y., Maher E.A., Neumann G., Kawaoka Y. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012, 486:420.
85. Institute of Laboratory Animal Resources Laboratory animals, Part II: Animals for research. a directory of sources of laboratory animals, tissues and fluids, equipment, and materials 1966, National Academy of Sciences - National Research Council, Washington, DC.
86. IOM (Institute of Medicine) Preventing transmission of pandemic influenza and other viral respiratory diseases: Personal protective equipment for healthcare personnel. 2011, The National Academies Press, Washington, DC.
87. Itoh Y., Shinya K., Kiso M., Watanabe T., Sakoda Y., Hatta M., Muramoto Y., Tamura D., Sakai-Tagawa Y., Noda T., Sakabe S., Imai M., Hatta Y., Watanabe S., Li C., Yamada S., Fujii K., Murakami S., Imai H., Kakugawa S., Ito M., Takano R., Iwatsuki-Horimoto K., Shimojima M., Horimoto T., Goto H., Takahashi K., Makino A., Ishigaki H., Nakayama M., Okamatsu M., Takahashi K., Warshauer D., Shult P.A., Saito R., Suzuki H., Furuta Y., Yamashita M., Mitamura K., Nakano K., Nakamura M., Brockman-Schneider R., Mitamura H., Yamazaki M., Sugaya N., Suresh M., Ozawa M., Neumann G., Gern J., Kida H., Ogasawara K., Kawaoka Y. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 2009, 460:1021.
88. Janssen R.J., Chappell W.A., Gerone P.J. Synergistic activity between Pr8 influenza virus and Staphylococcus aureus in the guinea pig. Am. J. Hyg. 1963, 78:275.
89. Jegaskanda S., Job E.R., Kramski M., Laurie K., Isitman G., de Rose R., Winnall W.R., Stratov I., Brooks A.G., Reading P.C., Kent S.J. Cross-reactive influenza-specific antibody-dependent cellular cytotoxicity antibodies in the absence of neutralizing antibodies. J. Immunol. 2013, 190:1837.
90. Jiang J., Fisher E.M., Murasko D.M. CD8 T cell responses to influenza virus infection in aged mice. Ageing Res. Rev. 2011, 10:422.
91. Kanekiyo M., Wei C.J., Yassine H.M., McTamney P.M., Boyington J.C., Whittle J.R., Rao S.S., Kong W.P., Wang L., Nabel G.J. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 2013, 499:102.
92. Kang Y.M., Song B.M., Lee J.S., Kim H.S., Seo S.H. Pandemic H1N1 influenza virus causes a stronger inflammatory response than seasonal H1N1 influenza virus in ferrets. Arch. Virol. 2011, 156:759.
93. Kash J.C., Basler C.F., Garcia-Sastre A., Carter V., Billharz R., Swayne D.E., Przygodzki R.M., Taubenberger J.K., Katze M.G., Tumpey T.M. Global host immune response: Pathogenesis and transcriptional profiling of type A influenza viruses expressing the hemagglutinin and neuraminidase genes from the 1918 pandemic virus. J. Virol. 2004, 78:9499.
94. Kash J.C., Tumpey T.M., Proll S.C., Carter V., Perwitasari O., Thomas M.J., Basler C.F., Palese P., Taubenberger J.K., Garcia-Sastre A., Swayne D.E., Katze M.G. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 2006, 443:578.
95. Katz J.M., Plowden J., Renshaw-Hoelscher M., Lu X., Tumpey T.M., Sambhara S. Immunity to influenza: the challenges of protecting an aging population. Immunol. Res. 2004, 29:113.
96. Kedzierska K., La Gruta N.L., Turner S.J., Doherty P.C. Establishment and recall of CD8+ T-cell memory in a model of localized transient infection. Immunol. Rev. 2006, 211:133.
97. Kim H.M., Kang Y.M., Ku K.B., Park E.H., Yum J., Kim J.C., Jin S.Y., Lee J.S., Kim H.S., Seo S.H. The severe pathogenicity of alveolar macrophage-depleted ferrets infected with 2009 pandemic H1N1 influenza virus. Virology 2013, 444:394.
98. Kimble J.B., Sorrell E., Shao H., Martin P.L., Perez D.R. Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:12084.
99. Kiso M., Shinya K., Shimojima M., Takano R., Takahashi K., Katsura H., Kakugawa S., Le M.T., Yamashita M., Furuta Y., Ozawa M., Kawaoka Y. Characterization of oseltamivir-resistant 2009 H1N1 pandemic influenza A viruses. PLoS Pathog. 2010, 6:e1001079.
100. Klimov A., Balish A., Veguilla V., Sun H., Schiffer J., Lu X., Katz J.M., Hancock K. Influenza virus titration, antigenic characterization, and serological methods for antibody detection. Methods Mol. Biol. 2012, 865:25.
101. Kobasa D., Takada A., Shinya K., Hatta M., Halfmann P., Theriault S., Suzuki H., Nishimura H., Mitamura K., Sugaya N., Usui T., Murata T., Maeda Y., Watanabe S., Suresh M., Suzuki T., Suzuki Y., Feldmann H., Kawaoka Y. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 2004, 431:703.
102. Koster F., Gouveia K., Zhou Y., Lowery K., Russell R., MacInnes H., Pollock Z., Layton R.C., Cromwell J., Toleno D., Pyle J., Zubelewicz M., Harrod K., Sampath R., Hofstadler S., Gao P., Liu Y., Cheng Y.S. Exhaled aerosol transmission of pandemic and seasonal H1N1 influenza viruses in the ferret. PLoS ONE 2012, 7:e33118.
103. Krammer F., Hai R., Yondola M., Tan G.S., Leyva-Grado V., Ryder A.B., Miller M.S., Rose J.K., Palese P., Garcia-Sastre A., Albrecht R.A. Assessment of influenza virus hemagglutinin stalk-based immunity in ferrets. J. Virol. 2014, 88:3432.
104. Kreijtz J.H., Fouchier R.A., Rimmelzwaan G.F. Immune responses to influenza virus infection. Virus Res. 2011, 162:19.
105. Kroeze E.J., Kuiken T., Osterhaus A.D. Animal models. Methods Mol. Biol. 2012, 865:127.
106. Kugel D., Kochs G., Obojes K., Roth J., Kobinger G.P., Kobasa D., Haller O., Staeheli P., von Messling V. Intranasal administration of alpha interferon reduces seasonal influenza A virus morbidity in ferrets. J. Virol. 2009, 83:3843.
107. Kwon Y.K., Lipatov A.S., Swayne D.E. Bronchointerstitial pneumonia in guinea pigs following inoculation with H5N1 high pathogenicity avian influenza virus. Vet. Pathol. 2009, 46:138.
108. Kwon D., Shin K., Kim S., Ha Y., Choi J.H., Yang J.S., Lee J.Y., Chae C., Oh H.B., Kang C. Replication and pathogenesis of the pandemic (H1N1) 2009 influenza virus in mammalian models. J. Microbiol. 2010, 48:657.
109. Lakdawala S.S., Lamirande E.W., Suguitan A.L., Wang W., Santos C.P., Vogel L., Matsuoka Y., Lindsley W.G., Jin H., Subbarao K. Eurasian-origin gene segments contribute to the transmissibility, aerosol release, and morphology of the 2009 pandemic H1N1 influenza virus. PLoS Pathog. 2011, 7:e1002443.
110. Lapinsky S.E. Epidemic viral pneumonia. Curr. Opin. Infect. Dis. 2010, 23:139.
111. Lednicky J.A., Croutch C.R., Lawrence S.J., Hamilton S.B., Daniels D.E., Astroff B. A nonlethal young domesticated ferret (Mustela putorius furo) model for studying pandemic influenza virus A/California/04/2009 (H1N1). Comp. Med. 2010, 60:364.
112. Lindsley W.G., Blachere F.M., Thewlis R.E., Vishnu A., Davis K.A., Cao G., Palmer J.E., Clark K.E., Fisher M.A., Khakoo R., Beezhold D.H. Measurements of airborne influenza virus in aerosol particles from human coughs. PLoS ONE 2010, 5:e15100.
113. Lindsley W.G., Pearce T.A., Hudnall J.B., Davis K.A., Davis S.M., Fisher M.A., Khakoo R., Palmer J.E., Clark K.E., Celik I., Coffey C.C., Blachere F.M., Beezhold D.H. Quantity and size distribution of cough-generated aerosol particles produced by influenza patients during and after illness. J. Occup. Environ. Hyg. 2012, 9:443.
114. Lloyd-Smith J.O., Schreiber S.J., Kopp P.E., Getz W.M. Superspreading and the effect of individual variation on disease emergence. Nature 2005, 438:355.
115. Long J., Bushnell R.V., Tobin J.K., Pan K., Deem M.W., Nara P.L., Tobin G.J. Evolution of H3N2 influenza virus in a guinea pig model. PLoS ONE 2011, 6:e20130.
116. Lowen A.C., Mubareka S., Tumpey T.M., 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.
117. Lowen A.C., Mubareka S., Steel J., Palese P. Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog. 2007, 3:1470.
118. Lowen A.C., Steel J., Mubareka S., Palese P. High temperature (30°C) blocks aerosol but not contact transmission of influenza virus. J. Virol. 2008, 82:5650.
119. Lowen A.C., Steel J., Mubareka S., Carnero E., Garcia-Sastre A., Palese P. Blocking inter-host transmission of influenza virus by vaccination in the guinea pig model. J. Virol. 2009, 83:2803.
120. Lyle L.R., Jutila J.W. D-amino acid oxidase induction in the kidneys of germ-free mice. J. Bacteriol. 1968, 96:606.
121. MacInnes H., Zhou Y., Gouveia K., Cromwell J., Lowery K., Layton R.C., Zubelewicz M., Sampath R., Hofstadler S., Liu Y., Cheng Y.S., Koster F. Transmission of aerosolized seasonal H1N1 influenza A to ferrets. PLoS ONE 2011, 6:e24448.
122. 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.
123. 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. U. S. A. 2006, 103:12121.
124. 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 2009 A(H1N1) influenza viruses in ferrets and mice. Science 2009, 325:484.
125. Maines T.R., Belser J.A., Gustin K.M., van Hoeven N., Zeng H., Svitek N., von Messling V., Katz J.M., Tumpey T.M. Local innate immune responses and influenza virus transmission and virulence in ferrets. J. Infect. Dis. 2011, 205:474.
126. Martel C.J., Aasted B. Characterization of antibodies against ferret immunoglobulins, cytokines and CD markers. Vet. Immunol. Immunopathol. 2009, 132:109.
127. Matsuoka Y., Lamirande E.W., Subbarao K. The ferret model for influenza. Curr. Protoc. Microbiol. 2009, 13:15G.2.1.
128. McGill J., Heusel J.W., Legge K.L. Innate immune control and regulation of influenza virus infections. J. Leukoc. Biol. 2009, 86:803.
129. McMurray D.N. Disease model: pulmonary tuberculosis. Trends Mol. Med. 2001, 7:135.
130. Memoli M.J., Hrabal R.J., Hassantoufighi A., Jagger B.W., Sheng Z.M., Eichelberger M.C., Taubenberger J.K. Rapid selection of a transmissible multidrug-resistant influenza A/H3N2 virus in an immunocompromised host. J. Infect. Dis. 2010, 201:1397.
131. Mertz D., Kim T.H., Johnstone J., Lam P.P., Science M., Kuster S.P., Fadel S.A., Tran D., Fernandez E., Bhatnagar N., Loeb M. Populations at risk for severe or complicated influenza illness: Systematic review and meta-analysis. BMJ 2013, 347:f5061.
132. Meunier I., von Messling V. PB1-F2 modulates early host responses but does not affect the pathogenesis of H1N1 seasonal influenza virus. J. Virol. 2012, 86:4271.
133. 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.
134. Moltedo B., Lopez C.B., Pazos M., Becker M.I., Hermesh T., Moran T.M. Cutting edge: Stealth influenza virus replication precedes the initiation of adaptive immunity. J. Immunol. 2009, 183:3569.
135. Moltedo B., Li W., Yount J.S., Moran T.M. Unique type I interferon responses determine the functional fate of migratory lung dendritic cells during influenza virus infection. PLoS Pathog. 2011, 7:e1002345.
136. Moncla L.H., Ross T.M., Dinis J.M., Weinfurter J.T., Mortimer T.D., Schultz-Darken N., Brunner K., Capuano S.V., Boettcher C., Post J., Johnson M., Bloom C.E., Weiler A.M., Friedrich T.C. A novel nonhuman primate model for influenza transmission. PLoS ONE 2013, 8:e78750.
137. Morgan O.W., Parks S., Shim T., Blevins P.A., Lucas P.M., Sanchez R., Walea N., Loustalot F., Duffy M.R., Shim M.J., Guerra S., Guerra F., Mills G., Verani J., Alsip B., Lindstrom S., Shu B., Emery S., Cohen A.L., Menon M., Fry A.M., Dawood F., Fonseca V.P., Olsen S.J. Household transmission of pandemic (H1N1) 2009, San Antonio, Texas, USA, April-May 2009. Emerg. Infect. Dis. 2010, 16:631.
138. Mount A.M., Belz G.T. Mouse models of viral infection: Influenza infection in the lung. Methods Mol. Biol. 2010, 595:299.
139. Mubareka S., Lowen A.C., Steel J., Coates A.L., Garcia-Sastre A., Palese P. Transmission of influenza virus via aerosols and fomites in the guinea pig model. J. Infect. Dis. 2009, 199:858.
140. Munster V.J., de Wit E., van den Brand J.M., Herfst S., Schrauwen E.J., Bestebroer T.M., van de Vijver D., Boucher C.A., Koopmans M., Rimmelzwaan G.F., Kuiken T., Osterhaus A.D., Fouchier R.A. Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 2009, 325:481.
141. Murata Y., Walsh E.E., Falsey A.R. Pulmonary complications of interpandemic influenza A in hospitalized adults. J. Infect. Dis. 2007, 195:1029.
142. National Research Council of the National Academies Guide for the Care and Use of Laboratory Animals 2011, The National Academies Press, Washington, DC. 8th edition.
143. Nishiura H., Yen H.L., Cowling B.J. Sample size considerations for one-to-one animal transmission studies of the influenza A viruses. PLoS ONE 2013, 8:e55358.
144. Oshansky C.M., Thomas P.G. The human side of influenza. J. Leukoc. Biol. 2012, 92:83.
145. Padilla-Carlin D.J., McMurray D.N., Hickey A.J. The guinea pig as a model of infectious diseases. Comp. Med. 2008, 58:324.
146. Pascua P.N., Song M.S., Lee J.H., Baek Y.H., Kwon H.I., Park S.J., Choi E.H., Lim G.J., Lee O.J., Kim S.W., Kim C.J., Sung M.H., Kim M.H., Yoon S.W., Govorkova E.A., Webby R.J., Webster R.G., Choi Y.K. Virulence and transmissibility of H1N2 influenza virus in ferrets imply the continuing threat of triple-reassortant swine viruses. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:15900.
147. Pearce M.B., Jayaraman A., Pappas C., Belser J.A., Zeng H., Gustin K.M., Maines T.R., Sun X., Raman R., Cox N.J., Sasisekharan R., Katz J.M., Tumpey T.M. Pathogenesis and transmission of swine origin A(H3N2)v influenza viruses in ferrets. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3944.
148. Peiris J.S., Cheung C.Y., Leung C.Y., Nicholls J.M. Innate immune responses to influenza A H5N1: Friend or foe?. Trends Immunol. 2009, 30:574.
149. Petsch B., Schnee M., Vogel A.B., Lange E., Hoffmann B., Voss D., Schlake T., Thess A., Kallen K.J., Stitz L., Kramps T. Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection. Nat. Biotechnol. 2012, 30:1210.
150. Phair J.P., Kauffman C.A., Jennings R., Potter C.W. Influenza virus infection of the guinea pig: Immune response and resistance. Med. Microbiol. Immunol. 1979, 165:241.
151. Pica N., Bouvier N.M. Environmental factors affecting the transmission of respiratory viruses. Curr. Opin. Virol. 2012, 2:90.
152. Pica N., Iyer A., Ramos I., Bouvier N.M., Fernandez-Sesma A., Garcia-Sastre A., Lowen A.C., Palese P., Steel J. The DBA.2 mouse is susceptible to disease following infection with a broad, but limited, range of influenza A and B viruses. J. Virol. 2011, 85:12825.
153. Pica N., Chou Y.Y., Bouvier N.M., Palese P. Transmission of influenza B viruses in the guinea pig. J. Virol. 2012, 86:4279.
154. Plourde J.R., Pyles J.A., Layton R.C., Vaughan S.E., Tipper J.L., Harrod K.S. Neurovirulence of H5N1 infection in ferrets is mediated by multifocal replication in distinct permissive neuronal cell regions. PLoS ONE 2012, 7:e46605.
155. Pushko P., Pearce M.B., Ahmad A., Tretyakova I., Smith G., Belser J.A., Tumpey T.M. Influenza virus-like particle can accommodate multiple subtypes of hemagglutinin and protect from multiple influenza types and subtypes. Vaccine 2011, 29:5911.
156. Reeve P., Almond J.W., Felsenreich V., Pibermann M., Maassab H.F. Studies with a cold-recombinant A/Victoria/3/75 (H3N2) virus. I. Biologic, genetic, and biochemical characterization. J. Infect. Dis. 1980, 142:850.
157. Richard M., Schrauwen E.J., de Graaf M., Bestebroer T.M., Spronken M.I., van Boheemen S., de Meulder D., Lexmond P., Linster M., Herfst S., Smith D.J., van den Brand J.M., Burke D.F., Kuiken T., Rimmelzwaan G.F., Osterhaus A.D., Fouchier R.A. Limited airborne transmission of H7N9 influenza A virus between ferrets. Nature 2013, 501:560.
158. Roberts K.L., Shelton H., Scull M., Pickles R., Barclay W.S. Lack of transmission of a human influenza virus with avian receptor specificity between ferrets is not due to decreased virus shedding but rather a lower infectivity in vivo. J. Gen. Virol. 2011, 92:1822.
159. Rowe T., Leon A.J., Crevar C.J., Carter D.M., Xu L., Ran L., Fang Y., Cameron C.M., Cameron M.J., Banner D., Ng D.C., Ran R., Weirback H.K., Wiley C.A., Kelvin D.J., Ross T.M. Modeling host responses in ferrets during A/California/07/2009 influenza infection. Virology 2010, 401:257.
160. Rutigliano J.A., Doherty P.C., Franks J., Morris M.Y., Reynolds C., Thomas P.G. Screening monoclonal antibodies for cross-reactivity in the ferret model of influenza infection. J. Immunol. Methods 2008, 336:71.
161. Sato M., Hosoya M., Kato K., Suzuki H. Viral shedding in children with influenza virus infections treated with neuraminidase inhibitors. Pediatr. Infect. Dis. J. 2005, 24:931.
162. Scallan C.D., Tingley D.W., Lindbloom J.D., Toomey J.S., Tucker S.N. An adenovirus-based vaccine with a double-stranded RNA adjuvant protects mice and ferrets against H5N1 avian influenza in oral delivery models. Clin. Vaccine Immunol. 2013, 20:85.
163. Schulman J.L. Experimental transmission of influenza virus infection in mice: IV. Relationship of transmissibility of different strains of virus and recovery of airborne virus in the environment of infector mice. J. Exp. Med. 1967, 125:479.
164. Schulman J.L. Experimental transmission of influenza virus infection in mice: III. Differing effects of immunity induced by infection and by inactivated influenza virus vaccine on transmission of infection. J. Exp. Med. 1967, 125:467.
165. Schulman J.L. The use of an animal model to study transmission of influenza virus infection. Am. J. Public Health Nations Health 1968, 58:2092.
166. Schulman J.L., Kilbourne E.D. Airborne transmission of influenza virus infection in mice. Nature 1962, 195:1129.
167. Schulman J.L., Kilbourne E.D. Experimental transmission of influenza virus infection in mice: I. The period of transmissibility. J. Exp. Med. 1963, 118:257.
168. Schulman J.L., Kilbourne E.D. Experimental transmission of influenza virus infection in mice: II. Some factors affecting the incidence of transmitted infection. J. Exp. Med. 1963, 118:267.
169. Seibert C.W., Kaminski M., Philipp J., Rubbenstroth D., Albrecht R.A., Schwalm F., Stertz S., Medina R.A., Kochs G., Garcia-Sastre A., Staeheli P., Palese P. Oseltamivir-resistant variants of the 2009 pandemic H1N1 influenza A virus are not attenuated in the guinea pig and ferret transmission models. J. Virol. 2010, 84:11219.
170. Seibert C.W., Rahmat S., Krause J.C., Eggink D., Albrecht R.A., Goff P.H., Krammer F., Duty J.A., Bouvier N.M., Garcia-Sastre A., Palese P. Recombinant IgA is sufficient to prevent influenza virus transmission in guinea pigs. J. Virol. 2013, 87:7793.
171. Shinya K., Ebina M., Yamada S., Ono M., Kasai N., Kawaoka Y. Avian flu: Influenza virus receptors in the human airway. Nature 2006, 440:435.
172. Shope R.E. Swine influenza: V. Studies on contagion. J. Exp. Med. 1934, 59:201.
173. Shope R.E. The infection of mice with swine influenza virus. J. Exp. Med. 1935, 62:561.
174. Smee D.F., Barnard D.L. Methods for evaluation of antiviral efficacy against influenza virus infections in animal models. Methods Mol. Biol. 2013, 1030:407.
175. Smith W., Stuart-Harris C.H. Influenza infection of man from the ferret. Lancet 1936, 228:121.
176. Smith W., Andrewes C.H., Laidlaw P.P. A virus obtained from influenza patients. Lancet 1933, 222:66.
177. Smith J.H., Nagy T., Barber J., Brooks P., Tompkins S.M., Tripp R.A. Aerosol inoculation with a sub-lethal influenza virus leads to exacerbated morbidity and pulmonary disease pathogenesis. Viral Immunol. 2011, 24:131.
178. Smith J.H., Nagy T., Driskell E., Brooks P., Tompkins S.M., Tripp R.A. Comparative pathology in ferrets infected with H1N1 influenza A viruses isolated from different hosts. J. Virol. 2011, 85:7572.
179. Sorrell E.M., Wan H., Araya Y., Song H., Perez D.R. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7565.
180. Srivastava B., Blazejewska P., Hessmann M., Bruder D., Geffers R., Mauel S., Gruber A.D., Schughart K. Host genetic background strongly influences the response to influenza a virus infections. PLoS ONE 2009, 4:e4857.
181. Steel J. New strategies for the development of H5N1 subtype influenza vaccines: Progress and challenges. BioDrugs 2011, 25:285.
182. Steel J., Lowen A.C., Mubareka S., Palese P. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 2009, 5:e1000252.
183. Steel J., Staeheli P., Mubareka S., Garcia-Sastre A., Palese P., Lowen A.C. Transmission of pandemic H1N1 influenza virus and impact of prior exposure to seasonal strains or interferon treatment. J. Virol. 2010, 84:21.
184. Steel J., Palese P., Lowen A.C. Transmission of a 2009 pandemic influenza virus shows a sensitivity to temperature and humidity similar to that of an H3N2 seasonal strain. J. Virol. 2011, 85:1400.
185. Stein R.A. Super-spreaders in infectious diseases. Int. J. Infect. Dis. 2011, 15:e510.
186. Stelzer-Braid S., Oliver B.G., Blazey A.J., Argent E., Newsome T.P., Rawlinson W.D., Tovey E.R. Exhalation of respiratory viruses by breathing, coughing, and talking. J. Med. Virol. 2009, 81:1674.
187. Stuart-Harris C.H., Francis T. Studies on the nasal histology of epidemic influenza virus infection in the ferret: II. The resistance of regenerating respiratory epithelium to reinfection and to physicochemical injury. J. Exp. Med. 1938, 68:803.
188. Studahl M. Influenza virus and CNS manifestations. J. Clin. Virol. 2003, 28:225.
189. Subbarao K., Luke C. H5N1 viruses and vaccines. PLoS Pathog. 2007, 3:e40.
190. Sun Y., Bi Y., Pu J., Hu Y., Wang J., Gao H., Liu L., Xu Q., Tan Y., Liu M., Guo X., Yang H., Liu J. Guinea pig model for evaluating the potential public health risk of swine and avian influenza viruses. PLoS ONE 2010, 5:e15537.
191. Tang X., Chong K.T. Histopathology and growth kinetics of influenza viruses (H1N1 and H3N2) in the upper and lower airways of guinea pigs. J. Gen. Virol. 2009, 90:386.
192. Taubenberger J.K., Morens D.M. 1918 influenza: The mother of all pandemics. Emerg. Infect. Dis. 2006, 12:15.
193. Tellier R. Aerosol transmission of influenza A virus: A review of new studies. J. R. Soc. Interface 2009, 6(Suppl. 6):S783.
194. The European Parliament and the Council of the European Union Directive 2010/63/EU of the European parliament and of the council on the protection of animals used for scientific purposes. Off. J. Eur. Union 2010, 276.
195. Tisoncik J.R., Korth M.J., Simmons C.P., Farrar J., Martin T.R., Katze M.G. Into the eye of the cytokine storm. Microbiol. Mol. Biol. Rev. 2012, 76:16.
196. Toms G.L., Sweet C., Smith H. Behaviour in ferrets of swine influenza virus isolated from man. Lancet 1977, 1:68.
197. Treanor J.J. Influenza viruses, including avian influenza and swine influenza. Mandell, Douglas, and Bennett's Principles and Practices of Infectious Diseases 2010, vol. 2. Churchill Livingstone Elsevier, Philadelphia.
198. Tripp R.A., Tompkins S.M. Animal models for evaluation of influenza vaccines. Curr. Top. Microbiol. Immunol. 2009, 333:397.
199. Tumpey T.M., Basler C.F., Aguilar P.V., Zeng H., Solorzano A., Swayne D.E., Cox N.J., Katz J.M., Taubenberger J.K., Palese P., Garcia-Sastre A. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 2005, 310:77.
200. Tumpey T.M., Garcia-Sastre A., Taubenberger J.K., Palese P., Swayne D.E., Pantin-Jackwood M.J., Schultz-Cherry S., Solorzano A., Van Rooijen N., Katz J.M., Basler C.F. Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: Functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J. Virol. 2005, 79:14933.
201. Turner R.B. The common cold. Mandell, Douglas, and Bennett's Principles and Practices of Infectious Diseases 2010, vol. 1. Churchill Livingstone Elsevier, Philadelphia.
202. Tuttle R.S., Sosna W.A., Daniels D.E., Hamilton S.B., Lednicky J.A. Design, assembly, and validation of a nose-only inhalation exposure system for studies of aerosolized viable influenza H5N1 virus in ferrets. Virol. J. 2010, 7:135.
203. van de Sandt C.E., Kreijtz J.H., Rimmelzwaan G.F. Evasion of influenza A viruses from innate and adaptive immune responses. Viruses 2012, 4:1438.
204. van den Brand J.M., Stittelaar K.J., van Amerongen G., Reperant L., de Waal L., Osterhaus A.D., Kuiken T. Comparison of temporal and spatial dynamics of seasonal H3N2, pandemic H1N1 and highly pathogenic avian influenza H5N1 virus infections in ferrets. PLoS ONE 2012, 7:e42343.
205. van der Laan J.W., Herberts C., Lambkin-Williams R., Boyers A., Mann A.J., Oxford J. Animal models in influenza vaccine testing. Expert Rev. Vaccines 2008, 7:783.
206. Van Hoeven N., Belser J.A., Szretter K.J., Zeng H., Staeheli P., Swayne D.E., Katz J.M., Tumpey T.M. Pathogenesis of 1918 pandemic and H5N1 influenza virus infections in a guinea pig model: Antiviral potential of exogenous alpha interferon to reduce virus shedding. J. Virol. 2009, 83:2851.
207. van Riel D., Munster V.J., de Wit E., Rimmelzwaan G.F., Fouchier R.A.M., Osterhaus A.D.M.E., Kuiken T. H5N1 virus attachment to lower respiratory tract. Science 2006, 312:399.
208. van Riel D., Munster V.J., de Wit E., Rimmelzwaan G.F., Fouchier R.A.M., Osterhaus A.D.M.E., Kuiken T. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 2007, 171:1215.
209. Walker E., Hernandez A.V., Kattan M.W. Meta-analysis: Its strengths and limitations. Cleve. Clin. J. Med. 2008, 75:431.
210. Wan H., Sorrell E.M., Song H., Hossain M.J., Ramirez-Nieto G., Monne I., Stevens J., Cattoli G., Capua I., Chen L.M., Donis R.O., Busch J., Paulson J.C., Brockwell C., Webby R., Blanco J., Al-Natour M.Q., Perez D.R. Replication and transmission of H9N2 influenza viruses in ferrets: Evaluation of pandemic potential. PLoS ONE 2008, 3:e2923.
211. Watanabe T., Bartrand T.A., Omura T., Haas C.N. Dose-response assessment for influenza A virus based on data sets of infection with its live attenuated reassortants. Risk Anal. 2012, 32:555.
212. 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.
213. Wei C.J., Yassine H.M., McTamney P.M., Gall J.G., Whittle J.R., Boyington J.C., Nabel G.J. Elicitation of broadly neutralizing influenza antibodies in animals with previous influenza exposure. Sci. Transl. Med. 2012, 4:147ra114.
214. Weinstock D.M., Gubareva L.V., Zuccotti G. Prolonged shedding of multidrug-resistant influenza A virus in an immunocompromised patient. N. Engl. J. Med. 2003, 348:867.
215. Wetherbee R.E. Induction of systemic delayed hypersensitivity during experimental viral infection of the respiratory tract with a myxovirus or paramyxovirus. J. Immunol. 1973, 111:157.
216. Widmer K., Zhu Y., Williams J.V., Griffin M.R., Edwards K.M., Talbot H.K. Rates of hospitalizations for respiratory syncytial virus, human metapneumovirus, and influenza virus in older adults. J. Infect. Dis. 2012, 206:56.
217. Woolpert T., Brodine S., Lemus H., Waalen J., Blair P., Faix D. Determination of clinical and demographic predictors of laboratory-confirmed influenza with subtype analysis. BMC Infect. Dis. 2012, 12:129.
218. Wright S. The results of crosses between inbred strains of guinea pigs, differing in number of digits. Genetics 1934, 19:537.
219. Wright S., Chase H.B. On the genetics of the spotted pattern of the guinea pig. Genetics 1936, 21:758.
220. Xie X., Li Y., Sun H., Liu L. Exhaled droplets due to talking and coughing. J. R. Soc. Interface 2009, 6(Suppl. 6):S703.
221. Xu L., Bao L., Deng W., Dong L., Zhu H., Chen T., Lv Q., Li F., Yuan J., Xiang Z., Gao K., Xu Y., Huang L., Li Y., Liu J., Yao Y., Yu P., Li X., Huang W., Zhao X., Lan Y., Guo J., Yong W., Wei Q., Chen H., Zhang L., Qin C. Novel avian-origin human influenza A(H7N9) can be transmitted between ferrets via respiratory droplets. J. Infect. Dis. 2014, 209:551.
222. Yang Y., Sugimoto J.D., Halloran M.E., Basta N.E., Chao D.L., Matrajt L., Potter G., Kenah E., Longini I.M. The transmissibility and control of pandemic influenza A (H1N1) virus. Science 2009, 326:729.
223. Yen H.L., Herlocher L.M., Hoffmann E., Matrosovich M.N., Monto A.S., Webster R.G., Govorkova E.A. Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob. Agents Chemother. 2005, 49:4075.
224. Zaas A.K., Chen M., Varkey J., Veldman T., Hero A.O., Lucas J., Huang Y., Turner R., Gilbert A., Lambkin-Williams R., Oien N.C., Nicholson B., Kingsmore S., Carin L., Woods C.W., Ginsburg G.S. Gene expression signatures diagnose influenza and other symptomatic respiratory viral infections in humans. Cell Host Microbe 2009, 6:207.
225. Zayas G., Chiang M.C., Wong E., MacDonald F., Lange C.F., Senthilselvan A., King M. Cough aerosol in healthy participants: fundamental knowledge to optimize droplet-spread infectious respiratory disease management. BMC Pulm. Med. 2012, 12:11.
226. Zhang Q., Shi J., Deng G., Guo J., Zeng X., He X., Kong H., Gu C., Li X., Liu J., Wang G., Chen Y., Liu L., Liang L., Li Y., Fan J., Wang J., Li W., Guan L., Li Q., Yang H., Chen P., Jiang L., Guan Y., Xin X., Jiang Y., Tian G., Wang X., Qiao C., Li C., Bu Z., Chen H. H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science 2013, 341:410.
227. Zhu H., Wang D., Kelvin D.J., Li L., Zheng Z., Yoon S.W., Wong S.S., Farooqui A., Wang J., Banner D., Chen R., Zheng R., Zhou J., Zhang Y., Hong W., Dong W., Cai Q., Roehrl M.H., Huang S.S., Kelvin A.A., Yao T., Zhou B., Chen X., Leung G.M., Poon L.L., Webster R.G., Webby R.J., Peiris J.S., Guan Y., Shu Y. Infectivity, transmission, and pathology of human-isolated H7N9 influenza virus in ferrets and pigs. Science 2013, 341:183.
228. Zitzow L.A., Rowe T., Morken T., Shieh W.J., Zaki S., Katz J.M. Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J. Virol. 2002, 76:4420.