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Abstract

Influenza B viruses have become increasingly more prominent during influenza seasons. Influenza B infection is typically considered a mild disease and receives less attention than influenza A, but has been causing 20 to 50 % of the total influenza incidence in several regions around the world. Although there is increasing evidence of mid to lower respiratory tract diseases such as bronchitis and pneumonia in influenza B patients, little is known about the pathogenesis of recent influenza B viruses. Here we investigated the clinical and pathological profiles of infection with strains representing the two current co-circulating B lineages (B/Yamagata and B/Victoria) in the ferret model. Specifically, we studied two B/Victoria (B/Brisbane/60/2008 and B/Bolivia/1526/2010) and two B/Yamagata (B/Florida/04/2006 and B/Wisconsin/01/2010) strain infections in ferrets and observed strain-specific but not lineage-specific pathogenicity. We found B/Brisbane/60/2008 caused the most severe clinical illness and B/Brisbane/60/2008 and the B/Yamagata strains instigated pathology in the middle to lower respiratory tract. Importantly, B/Brisbane/60/2008 established efficient lower respiratory tract infection with high viral burden. Our phylogenetic analyses demonstrate profound reassortment among recent influenza B viruses, which indicates the genetic make-up of B/Brisbane/60/2008 differs from the other strains. This may explain the pathogenicity difference post-infection in ferrets.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2014-10-01
2022-05-27
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References

  1. Banner D., Kelvin A. A. 2012; The current state of H5N1 vaccines and the use of the ferret model for influenza therapeutic and prophylactic development. J Infect Dev Ctries 6:465–469[PubMed]
    [Google Scholar]
  2. Chan P. K., Chan M. C., Cheung J. L., Lee N., Leung T. F., Yeung A. C., Wong M. C., Ngai K. L., Nelson E. A., Hui D. S. 2013; Influenza B lineage circulation and hospitalization rates in a subtropical city, Hong Kong, 2000-2010. Clin Infect Dis 56:677–684 [View Article][PubMed]
    [Google Scholar]
  3. Chen R., Holmes E. C. 2008; The evolutionary dynamics of human influenza B virus. J Mol Evol 66:655–663 [View Article][PubMed]
    [Google Scholar]
  4. Cheng V. C., To K. K., Tse H., Hung I. F., Yuen K. Y. 2012; Two years after pandemic influenza A/2009/H1N1: what have we learned?. Clin Microbiol Rev 25:223–263 [View Article][PubMed]
    [Google Scholar]
  5. Chi C. Y., Wang S. M., Lin C. C., Wang H. C., Wang J. R., Su I. J., Liu C. C. 2008; Clinical features of children infected with different strains of influenza B in southern Taiwan. Pediatr Infect Dis J 27:640–645 [View Article][PubMed]
    [Google Scholar]
  6. Esposito S., Molteni C. G., Daleno C., Valzano A., Fossali E., Da Dalt L., Cecinati V., Bruzzese E., Giacchino R.other authors 2011; Clinical and socioeconomic impact of different types and subtypes of seasonal influenza viruses in children during influenza seasons 2007/2008 and 2008/2009. BMC Infect Dis 11:271 [View Article][PubMed]
    [Google Scholar]
  7. Gill J. R., Sheng Z. M., Ely S. F., Guinee D. G., Beasley M. B., Suh J., Deshpande C., Mollura D. J., Morens D. M.other authors 2010; Pulmonary pathologic findings of fatal 2009 pandemic influenza A/H1N1 viral infections. Arch Pathol Lab Med 134:235–243[PubMed]
    [Google Scholar]
  8. Guarner J., Falcón-Escobedo R. 2009; Comparison of the pathology caused by H1N1, H5N1, and H3N2 influenza viruses. Arch Med Res 40:655–661 [View Article][PubMed]
    [Google Scholar]
  9. Gutiérrez-Pizarraya A., Pérez-Romero P., Alvarez R., Aydillo T. A., Osorio-Gómez G., Milara-Ibáñez C., Sánchez M., Pachón J., Cordero E. 2012; Unexpected severity of cases of influenza B infection in patients that required hospitalization during the first postpandemic wave. J Infect 65:423–430 [View Article][PubMed]
    [Google Scholar]
  10. Hamelin M. E., Baz M., Abed Y., Couture C., Joubert P., Beaulieu E., Bellerose N., Plante M., Mallett C.other authors 2010; Oseltamivir-resistant pandemic A/H1N1 virus is as virulent as its wild-type counterpart in mice and ferrets. PLoS Pathog 6:e1001015 [View Article][PubMed]
    [Google Scholar]
  11. Harms P. W., Schmidt L. A., Smith L. B., Newton D. W., Pletneva M. A., Walters L. L., Tomlins S. A., Fisher-Hubbard A., Napolitano L. M.other authors 2010; Autopsy findings in eight patients with fatal H1N1 influenza. Am J Clin Pathol 134:27–35 [View Article][PubMed]
    [Google Scholar]
  12. Hause B. M., Ducatez M., Collin E. A., Ran Z., Liu R., Sheng Z., Armien A., Kaplan B., Chakravarty S.other authors 2013; Isolation of a novel swine influenza virus from Oklahoma in 2011 which is distantly related to human influenza C viruses. PLoS Pathog 9:e1003176 [View Article][PubMed]
    [Google Scholar]
  13. Hay A. J., Gregory V., Douglas A. R., Lin Y. P. 2001; The evolution of human influenza viruses. Philos Trans R Soc Lond B Biol Sci 356:1861–1870 [View Article][PubMed]
    [Google Scholar]
  14. Huang S. S., Banner D., Fang Y., Ng D. C., Kanagasabai T., Kelvin D. J., Kelvin A. A. 2011; Comparative analyses of pandemic H1N1 and seasonal H1N1, H3N2, and influenza B infections depict distinct clinical pictures in ferrets. PLoS ONE 6:e27512 [View Article][PubMed]
    [Google Scholar]
  15. Huang S. S., Banner D., Degousee N., Leon A. J., Xu L., Paquette S. G., Kanagasabai T., Fang Y., Rubino S.other authors 2012; Differential pathological and immune responses in newly weaned ferrets are associated with a mild clinical outcome of pandemic 2009 H1N1 infection. J Virol 86:13187–13201 [View Article][PubMed]
    [Google Scholar]
  16. Huang S. S., Lin Z., Banner D., León A. J., Paquette S. G., Rubin B., Rubino S., Guan Y., Kelvin D. J., Kelvin A. A. 2013; Immunity toward H1N1 influenza hemagglutinin of historical and contemporary strains suggests protection and vaccine failure. Sci Rep 3:1698 [View Article][PubMed]
    [Google Scholar]
  17. Jayaraman A., Chandrasekaran A., Viswanathan K., Raman R., Fox J. G., Sasisekharan R. 2012; Decoding the distribution of glycan receptors for human-adapted influenza A viruses in ferret respiratory tract. PLoS ONE 7:e27517 [View Article][PubMed]
    [Google Scholar]
  18. Jonsson C. B., Camp J. V., Wu A., Zheng H., Kraenzle J. L., Biller A. E., Vanover C. D., Chu Y. K., Ng C. K.other authors 2012; Molecular imaging reveals a progressive pulmonary inflammation in lower airways in ferrets infected with 2009 H1N1 pandemic influenza virus. PLoS ONE 7:e40094 [View Article][PubMed]
    [Google Scholar]
  19. Kaji M., Watanabe A., Aizawa H. 2003; Differences in clinical features between influenza A H1N1, A H3N2, and B in adult patients. Respirology 8:231–233 [View Article][PubMed]
    [Google Scholar]
  20. Langmead B., Salzberg S. L. 2012; Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359 [View Article][PubMed]
    [Google Scholar]
  21. León A. J., Banner D., Xu L., Ran L., Peng Z., Yi K., Chen C., Xu F., Huang J.other authors 2013; Sequencing, annotation, and characterization of the influenza ferret infectome. J Virol 87:1957–1966 [View Article][PubMed]
    [Google Scholar]
  22. Li W. C., Shih S. R., Huang Y. C., Chen G. W., Chang S. C., Hsiao M. J., Tsao K. C., Lin T. Y. 2008; Clinical and genetic characterization of severe influenza B-associated diseases during an outbreak in Taiwan. J Clin Virol 42:45–51 [View Article][PubMed]
    [Google Scholar]
  23. Li G., Yilmaz M., Kojicic M., Fernández-Pérez E., Wahab R., Huskins W. C., Afessa B., Truwit J. D., Gajic O. 2009a; Outcome of critically ill patients with influenza virus infection. J Clin Virol 46:275–278 [View Article][PubMed]
    [Google Scholar]
  24. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R.1000 Genome Project Data Processing Subgroup 2009b; The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  25. Lindstrom S. E., Hiromoto Y., Nishimura H., Saito T., Nerome R., Nerome K. 1999; Comparative analysis of evolutionary mechanisms of the hemagglutinin and three internal protein genes of influenza B virus: multiple cocirculating lineages and frequent reassortment of the NP, M, and NS genes. J Virol 73:4413–4426[PubMed]
    [Google Scholar]
  26. Luo C., Morishita T., Satou K., Tateno Y., Nakajima K., Nobusawa E. 1999; Evolutionary pattern of influenza B viruses based on the HA and NS genes during 1940 to 1999: origin of the NS genes after 1997. Arch Virol 144:1881–1891 [View Article][PubMed]
    [Google Scholar]
  27. Maher J. A., DeStefano J. 2004; The ferret: an animal model to study influenza virus. Lab Anim (NY) 33:50–53 [View Article][PubMed]
    [Google Scholar]
  28. Marcelin G., Aldridge J. R., Duan S., Ghoneim H. E., Rehg J., Marjuki H., Boon A. C., McCullers J. A., Webby R. J. 2011; Fatal outcome of pandemic H1N1 2009 influenza virus infection is associated with immunopathology and impaired lung repair, not enhanced viral burden, in pregnant mice. J Virol 85:11208–11219 [View Article][PubMed]
    [Google Scholar]
  29. Mauad T., Hajjar L. A., Callegari G. D., da Silva L. F., Schout D., Galas F. R., Alves V. A., Malheiros D. M., Auler J. O. Jrother authors 2010; Lung pathology in fatal novel human influenza A (H1N1) infection. Am J Respir Crit Care Med 181:72–79 [View Article][PubMed]
    [Google Scholar]
  30. McCullers J. A., Wang G. C., He S., Webster R. G. 1999; Reassortment and insertion-deletion are strategies for the evolution of influenza B viruses in nature. J Virol 73:7343–7348[PubMed]
    [Google Scholar]
  31. McCullers J. A., Saito T., Iverson A. R. 2004; Multiple genotypes of influenza B virus circulated between 1979 and 2003. J Virol 78:12817–12828 [View Article][PubMed]
    [Google Scholar]
  32. Nakajima N., Sato Y., Katano H., Hasegawa H., Kumasaka T., Hata S., Tanaka S., Amano T., Kasai T.other authors 2012; Histopathological and immunohistochemical findings of 20 autopsy cases with 2009 H1N1 virus infection. Mod Pathol 25:1–13 [View Article][PubMed]
    [Google Scholar]
  33. Ohishi K., Ninomiya A., Kida H., Park C. H., Maruyama T., Arai T., Katsumata E., Tobayama T., Boltunov A. N.other authors 2002; Serological evidence of transmission of human influenza A and B viruses to Caspian seals (Phoca caspica). Microbiol Immunol 46:639–644 [View Article][PubMed]
    [Google Scholar]
  34. Osterhaus A. D., Rimmelzwaan G. F., Martina B. E., Bestebroer T. M., Fouchier R. A. 2000; Influenza B virus in seals. Science 288:1051–1053 [View Article][PubMed]
    [Google Scholar]
  35. Paul Glezen W., Schmier J. K., Kuehn C. M., Ryan K. J., Oxford J. 2013; The burden of influenza B: a structured literature review. Am J Public Health 103:e43–e51 [View Article][PubMed]
    [Google Scholar]
  36. Reuman P. D., Keely S., Schiff G. M. 1989; Assessment of signs of influenza illness in the ferret model. J Virol Methods 24:27–34 [View Article][PubMed]
    [Google Scholar]
  37. Sakudo A., Baba K., Ikuta K. 2012; Analysis of Vis-NIR spectra changes to measure the inflammatory response in the nasal mucosal region of influenza A and B virus-infected patients. J Clin Virol 55:334–338 [View Article][PubMed]
    [Google Scholar]
  38. Shieh W. J., Blau D. M., Denison A. M., Deleon-Carnes M., Adem P., Bhatnagar J., Sumner J., Liu L., Patel M.other authors 2010; 2009 Pandemic influenza A (H1N1): pathology and pathogenesis of 100 fatal cases in the United States. Am J Pathol 177:166–175 [View Article][PubMed]
    [Google Scholar]
  39. Suzuki Y., Ito T., Suzuki T., Holland R. E. Jr, Chambers T. M., Kiso M., Ishida H., Kawaoka Y. 2000; Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 74:11825–11831 [View Article][PubMed]
    [Google Scholar]
  40. Tamura K., Nei M. 1993; Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526[PubMed]
    [Google Scholar]
  41. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  42. Taubenberger J. K., Morens D. M. 2008; The pathology of influenza virus infections. Annu Rev Pathol 3:499–522 [View Article][PubMed]
    [Google Scholar]
  43. van Riel D., Munster V. J., de Wit E., Rimmelzwaan G. F., Fouchier R. A. M., Osterhaus A. D. M. E., Kuiken T. 2007; Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 171:1215–1223 [View Article][PubMed]
    [Google Scholar]
  44. Wang F., Zhu R. N., Qian Y., Deng J., Zhao L. Q., Liao B., Che L. 2008; [Surveillance for influenza B virus infections in infants and young children in Beijing, China]. Zhonghua Er Ke Za Zhi 46:94–97 (in Chinese) [PubMed]
    [Google Scholar]
  45. Wang Y. F., Chang C. F., Chi C. Y., Wang H. C., Wang J. R., Su I. J. 2012; Characterization of glycan binding specificities of influenza B viruses with correlation with hemagglutinin genotypes and clinical features. J Med Virol 84:679–685 [View Article][PubMed]
    [Google Scholar]
  46. WHO 2003; Influenza. Weekly Epidemiological Record. 78:5764
    [Google Scholar]
  47. Wu U. I., Wang J. T., Chen Y. C., Chang S. C. 2012; Severity of pandemic H1N1 2009 influenza virus infection may not be directly correlated with initial viral load in upper respiratory tract. Influenza Other Respi Viruses 6:367–373 [View Article][PubMed]
    [Google Scholar]
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