Pathogenicity and peramivir efficacy in immunocompromised murine models of influenza B virus infection

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Pascua, Philippe Noriel Q ^a   Mostafa, Heba H ^a   Marathe, Bindumadhav M ^a   Vogel, Peter ^a   Russell, Charles J ^a   Webby, Richard J ^a   Govorkova, Elena A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; AUTACOID; CYCLOPENTANE DERIVATIVE; CYTOKINE; GUANIDINE DERIVATIVE; PERAMIVIR;

ANIMAL; BRONCHOALVEOLAR LAVAGE FLUID; DISEASE MODEL; DRUG EFFECT; FEMALE; IMMUNOCOMPROMISED PATIENT; IMMUNOLOGY; INFLUENZA B VIRUS; METABOLISM; MORBIDITY; MORTALITY; MOUSE; NONOBESE DIABETIC MOUSE; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; VIROLOGY; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; BRONCHOALVEOLAR LAVAGE FLUID; CYCLOPENTANES; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GUANIDINES; IMMUNOCOMPROMISED HOST; INFLAMMATION MEDIATORS; INFLUENZA B VIRUS; MICE; MICE, INBRED NOD; MICE, SCID; MORBIDITY; MORTALITY; ORTHOMYXOVIRIDAE INFECTIONS; VIRAL LOAD; VIRUS REPLICATION;

EID: 85026778439     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-07433-z     Document Type: Article

References (70)

1. Englund, J., Feuchtinger, T. & Ljungman, P. Viral infections in immunocompromised patients. Biol Blood Marrow Transplant 17, S2-5 (2011).
2. Ison, M. G. Influenza prevention and treatment in transplant recipients and immunocompromised hosts. Influenza Other Respir Viruses 7(Suppl 3), 60-66 (2013).
3. Kim, Y. J., Boeckh, M. & Englund, J. A. Community respiratory virus infections in immunocompromised patients: hematopoietic stem cell and solid organ transplant recipients, and individuals with human immunodeficiency virus infection. Semin Respir Crit Care Med 28, 222-242 (2007).
4. Kunisaki, K. M. & Janoff, E. N. Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect Dis 9, 493-504 (2009).
5. Memoli, M. J. et al. The natural history of influenza infection in the severely immunocompromised vs nonimmunocompromised hosts. Clin Infect Dis 58, 214-224 (2014).
6. Bowden, R. A. Respiratory virus infections after marrow transplant: the Fred Hutchinson Cancer Research Center experience. Am J Med 102, 27-30, discussion, 42-23 (1997).
7. Carr, S. et al. 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 (2011).
8. Englund, J. A. et al. Common emergence of amantadine-and rimantadine-resistant influenza A viruses in symptomatic immunocompromised adults. Clin Infect Dis 26, 1418-1424 (1998).
9. Gubareva, L. V., Matrosovich, M. N., Brenner, M. K., Bethell, R. C. & Webster, R. G. Evidence for zanamivir resistance in an immunocompromised child infected with influenza B virus. J Infect Dis 178, 1257-1262 (1998).
10. van der Vries, E. et al. Prolonged influenza virus shedding and emergence of antiviral resistance in immunocompromised patients and ferrets. PLoS Pathog 9, e1003343 (2013).
11. Baz, M., Abed, Y., McDonald, J. & Boivin, G. Characterization of multidrug-resistant influenza A/H3N2 viruses shed during 1 year by an immunocompromised child. Clin Infect Dis 43, 1555-1561 (2006).
12. Ison, M. G., Gubareva, L. V., Atmar, R. L., Treanor, J. & Hayden, F. G. Recovery of drug-resistant influenza virus from immunocompromised patients: a case series. J Infect Dis 193, 760-764 (2006).
13. Kossyvakis, A. et al. Antiviral susceptibility profile of influenza A viruses; keep an eye on immunocompromised patients under prolonged treatment. Eur J Clin Microbiol Infect Dis 36, 361-371 (2017).
14. Tramontana, A. R. et al. Oseltamivir resistance in adult oncology and hematology patients infected with pandemic (H1N1) 2009 virus, Australia. Emerg Infect Dis 16, 1068-1075 (2010).
15. Kawai, N. et al. A comparison of the effectiveness of oseltamivir for the treatment of influenza A and influenza B: a Japanese multicenter study of the 2003-2004 and 2004-2005 influenza seasons. Clin Infect Dis 43, 439-444 (2006).
16. Skowronski, D. M. et al. Component-specific effectiveness of trivalent influenza vaccine as monitored through a sentinel surveillance network in Canada, 2006-2007. J Infect Dis 199, 168-179 (2009).
17. Burnham, A. J., Baranovich, T. & Govorkova, E. A. Neuraminidase inhibitors for influenza B virus infection: efficacy and resistance. Antiviral Res 100, 520-534 (2013).
18. Koutsakos, M., Nguyen, T. H., Barclay, W. S. & Kedzierska, K. Knowns and unknowns of influenza B viruses. Future Microbiol 11, 119-135 (2016).
19. Bodewes, R. et al. Recurring influenza B virus infections in seals. Emerg Infect Dis 19, 511-512 (2013).
20. Osterhaus, A. D., Rimmelzwaan, G. F., Martina, B. E., Bestebroer, T. M. & Fouchier, R. A. Influenza B virus in seals. Science 288, 1051-1053 (2000).
21. Namendys-Silva, S. A., Gonzalez-Herrera, M. O., Texcocano-Becerra, J. & Herrera-Gomez, A. Acute respiratory distress syndrome caused by influenza B virus infection in a patient with diffuse large B-cell lymphoma. Case Rep Med 2011, 647528 (2011).
22. Peltola, V., Ziegler, T. & Ruuskanen, O. Influenza A and B virus infections in children. Clin Infect Dis 36, 299-305 (2003).
23. Kawai, N. et al. Factors influencing the effectiveness of oseltamivir and amantadine for the treatment of influenza: a multicenter study from Japan of the 2002-2003 influenza season. Clin Infect Dis 40, 1309-1316 (2005).
24. Sugaya, N. et al. Lower clinical effectiveness of oseltamivir against influenza B contrasted with influenza A infection in children. Clin Infect Dis 44, 197-202 (2007).
25. Kawai, N. et al. Longer virus shedding in influenza B than in influenza A among outpatients treated with oseltamivir. J Infect 55, 267-272 (2007).
26. Barnard, D. L. Animal models for the study of influenza pathogenesis and therapy. Antiviral Res 82, A110-122 (2009).
27. Davis, P. H. & Stanley, S. L. Jr. Breaking the species barrier: use of SCID mouse-human chimeras for the study of human infectious diseases. Cell Microbiol 5, 849-860 (2003).
28. Shultz, L. D., Ishikawa, F. & Greiner, D. L. Humanized mice in translational biomedical research. Nat Rev Immunol 7, 118-130 (2007).
29. Bosma, G. C., Custer, R. P. & Bosma, M. J. A severe combined immunodeficiency mutation in the mouse. Nature 301, 527-530 (1983).
30. Kirchgessner, C. U. et al. DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 267, 1178-1183 (1995).
31. Bosma, M. J. & Carroll, A. M. The SCID mouse mutant: definition, characterization, and potential uses. Annu Rev Immunol 9, 323-350 (1991).
32. Shultz, L. D. & Sidman, C. L. Genetically determined murine models of immunodeficiency. Annu Rev Immunol 5, 367-403 (1987).
33. Shultz, L. D. et al. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol 154, 180-191 (1995).
34. Prochazka, M., Gaskins, H. R., Shultz, L. D. & Leiter, E. H. The nonobese diabetic scid mouse: model for spontaneous thymomagenesis associated with immunodeficiency. Proc Natl Acad Sci USA 89, 3290-3294 (1992).
35. Sidwell, R. W. et al. Inhibition of influenza virus infections in immunosuppressed mice with orally administered peramivir (BCX-1812). Antiviral Res 60, 17-25 (2003).
36. Ison, M. G., Mishin, V. P., Braciale, T. J., Hayden, F. G. & Gubareva, L. V. Comparative activities of oseltamivir and A-322278 in immunocompetent and immunocompromised murine models of influenza virus infection. J Infect Dis 193, 765-772 (2006).
37. Bot, A. et al. Cellular mechanisms involved in protection and recovery from influenza virus infection in immunodeficient mice. J Virol 70, 5668-5672 (1996).
38. World Health Organization. Influenza: WHO recommendations on the composition of influenza virus vaccines. http://www. who. int/influenza/vaccines/virus/recommendations/en/ (2017).
39. de Jong, M. D. et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12, 1203-1207 (2006).
40. Cline, T. D., Karlsson, E. A., Seufzer, B. J. & Schultz-Cherry, S. The hemagglutinin protein of highly pathogenic H5N1 influenza viruses overcomes an early block in the replication cycle to promote productive replication in macrophages. J Virol 87, 1411-1419 (2013).
41. Maines, T. R. et al. Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J Virol 79, 11788-11800 (2005).
42. Duan, S. & Thomas, P. G. Balancing Immune Protection and Immune Pathology by CD8(+) T-Cell Responses to Influenza Infection. Front Immunol 7, 25 (2016).
43. Kobasa, D. et al. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445, 319-323 (2007).
44. Perrone, L. A., Plowden, J. K., Garcia-Sastre, A., Katz, J. M. & Tumpey, T. M. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4, e1000115 (2008).
45. Tumpey, T. M. et al. 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 79, 14933-14944 (2005).
46. Szretter, K. J. et al. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J Virol 81, 2736-2744 (2007).
47. Doherty, P. C., Turner, S. J., Webby, R. G. & Thomas, P. G. Influenza and the challenge for immunology. Nat Immunol 7, 449-455 (2006).
48. Bantia, S., Arnold, C. S., Parker, C. D., Upshaw, R. & Chand, P. Anti-influenza virus activity of peramivir in mice with single intramuscular injection. Antiviral Res 69, 39-45 (2006).
49. World Health Organization. Influenza: Laboratory methodologies for testing the antiviral susceptibility of influenza viruses: Neuraminidase inhibitor (NAI). http://www. who. int/influenza/gisrs
50. Hurt, A. C. et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2014-2015. Antiviral Res 132, 178-185 (2016).
51. Leang, S. K. et al. Peramivir and laninamivir susceptibility of circulating influenza A and B viruses. Influenza Other Respir Viruses 8, 135-139 (2014).
52. Halford, W. P., Maender, J. L. & Gebhardt, B. M. Re-evaluating the role of natural killer cells in innate resistance to herpes simplex virus type 1. Virol J 2, 56, doi:10. 1186/1743-422X-2-56 (2005).
53. Tripathi, S., White, M. R. & Hartshorn, K. L. The amazing innate immune response to influenza A virus infection. Innate Immun 21, 73-98 (2015).
54. Chiu, C. & Openshaw, P. J. Antiviral B cell and T cell immunity in the lungs. Nat Immunol 16, 18-26 (2015).
55. Caini, S. et al. Epidemiological and virological characteristics of influenza B: results of the Global Influenza B Study. Influenza Other Respir Viruses 9(Suppl 1), 3-12 (2015).
56. Kim, J. C. et al. Severe pathogenesis of influenza B virus in pregnant mice. Virology 448, 74-81 (2014).
57. Huang, S. S. et al. Comparative analyses of pandemic H1N1 and seasonal H1N1, H3N2, and influenza B infections depict distinct clinical pictures in ferrets. PLoS One 6, e27512 (2011).
58. Huang, S. S. et al. Pathogenic influenza B virus in the ferret model establishes lower respiratory tract infection. J Gen Virol 95, 2127-2139 (2014).
59. Iwasaki, A. & Pillai, P. S. Innate immunity to influenza virus infection. Nat Rev Immunol 14, 315-328 (2014).
60. Brandes, M., Klauschen, F., Kuchen, S. & Germain, R. N. A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 154, 197-212 (2013).
61. Wester, A. & Shetty, A. K. Peramivir injection in the treatment of acute influenza: a review of the literature. Infect Drug Resist 9, 201-214 (2016).
62. Abed, Y., Simon, P. & Boivin, G. Prophylactic activity of intramuscular peramivir in mice infected with a recombinant influenza A/ WSN/33 (H1N1) virus containing the H274Y neuraminidase mutation. Antimicrob Agents Chemother 54, 2819-2822 (2010).
63. Abed, Y., Pizzorno, A. & Boivin, G. Therapeutic activity of intramuscular peramivir in mice infected with a recombinant influenza A/WSN/33 (H1N1) virus containing the H275Y neuraminidase mutation. Antimicrob Agents Chemother 56, 4375-4380 (2012).
64. Farooqui, A. et al. Assessment of Antiviral Properties of Peramivir against H7N9 Avian Influenza Virus in an Experimental Mouse Model. Antimicrob Agents Chemother 59, 7255-7264 (2015).
65. Yun, N. E. et al. Injectable peramivir mitigates disease and promotes survival in ferrets and mice infected with the highly virulent influenza virus, A/Vietnam/1203/04 (H5N1). Virology 374, 198-209 (2008).
66. Boltz, D. A. et al. Intramuscularly administered neuraminidase inhibitor peramivir is effective against lethal H5N1 influenza virus in mice. Antiviral Res 80, 150-157 (2008).
67. Kitano, M. et al. Efficacy of single intravenous injection of peramivir against influenza B virus infection in ferrets and cynomolgus macaques. Antimicrob Agents Chemother 55, 4961-4970 (2011).
68. Reed, L. & Muench, H. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27, 493-497 (1938).
69. Govorkova, E. A. et al. Antiviral resistance among highly pathogenic influenza A (H5N1) viruses isolated worldwide in 2002-2012 shows need for continued monitoring. Antiviral Res 98, 297-304 (2013).
70. Hoffmann, E. et al. Rescue of influenza B virus from eight plasmids. Proc Natl Acad Sci USA 99, 11411-11416 (2002).