Influenza and Parainfluenza Infection in Hematopoietic Stem Cell and Solid Organ Transplant Recipients

Chapter

Abstract

Respiratory viral infections are a cause of morbidity and mortality after stem cell and solid organ transplantation. Most of our knowledge of these viral infections in the transplant population comes from hospitalized patients, which may underrate the incidence and overestimate the severity of disease caused by these respiratory viruses. Besides rhinovirus, influenza and parainfluenza are among the most common viruses affecting transplant recipients. Because clinical presentation of these infections may not be distinctive and the etiology could be broad, the knowledge of the epidemiology of these respiratory viruses coupled with high clinical suspicion and early diagnosis is critical for managing these immunocompromised patients. In this book chapter, we underscore the early recognition of these viral infections, the rapid isolation to prevent hospital spread, the prompt empiric therapy specifically for influenza, the awareness of the risk factors for progression to the lower respiratory tract, and the appreciation of the potential long term impact on pulmonary function in this vulnerable transplant population. In addition to an extensive review of the current literature and update on management, we also discuss specific issues around these respiratory viral infections in patients after transplantation including drug resistance, nosocomial outbreaks, prolonged viral shedding, and future directions in prevention and management.

Keywords

Influenza infection Parainfluenza infection Immunocompromised patients Hematopoietic stem cell transplant Solid organ transplant Respiratory viral infections 

References

  1. 1.
    Bednarska K, Hallmann-Szelinska E, Kondratiuk K, Brydak LB. Evaluation of the activity of influenza and influenza-like viruses in the epidemic season 2013/2014. Adv Exp Med Biol. 2015;857:1–7.PubMedCrossRefGoogle Scholar
  2. 2.
    Appiah GD, Blanton L, D'Mello T, Kniss K, Smith S, Mustaquim D, et al. Influenza activity—United States, 2014–15 season and composition of the 2015–16 influenza vaccine. MMWR Morb Mortal Wkly Rep. 2015;64:583–90.PubMedGoogle Scholar
  3. 3.
    Molinari NA, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM, Weintraub E, et al. The annual impact of seasonal influenza in the us: measuring disease burden and costs. Vaccine. 2007;25:5086–96.PubMedCrossRefGoogle Scholar
  4. 4.
    McCarthy M. Early signs show that 2014–15 flu season may be severe, CDC warns. BMJ. 2014;349:g7530.PubMedCrossRefGoogle Scholar
  5. 5.
    Schiffer JT, Kirby K, Sandmaier B, Storb R, Corey L, Boeckh M. Timing and severity of community acquired respiratory virus infections after myeloablative versus non-myeloablative hematopoietic stem cell transplantation. Haematologica. 2009;94:1101–8.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Weigt SS, Gregson AL, Deng JC, Lynch 3rd JP, Belperio JA. Respiratory viral infections in hematopoietic stem cell and solid organ transplant recipients. Semin Respir Crit Care Med. 2011;32:471–93.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Ison MG. Respiratory viral infections in transplant recipients. Antivir Ther. 2007;12:627–38.PubMedGoogle Scholar
  8. 8.
    Nichols WG, Guthrie KA, Corey L, Boeckh M. Influenza infections after hematopoietic stem cell transplantation: risk factors, mortality, and the effect of antiviral therapy. Clin Infect Dis. 2004;39:1300–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Lopez-Medrano F, Aguado JM, Lizasoain M, Folgueira D, Juan RS, Diaz-Pedroche C, et al. Clinical implications of respiratory virus infections in solid organ transplant recipients: a prospective study. Transplantation. 2007;84:851–6.PubMedCrossRefGoogle Scholar
  10. 10.
    Manuel O, Estabrook M. Practice ASTIDCo RNA respiratory viruses in solid organ transplantation. Am J Transplant. 2013;13 Suppl 4:212–9.PubMedCrossRefGoogle Scholar
  11. 11.
    Chemaly RF, Ghosh S, Bodey GP, Rohatgi N, Safdar A, Keating MJ, et al. Respiratory viral infections in adults with hematologic malignancies and human stem cell transplantation recipients: a retrospective study at a major cancer center. Medicine (Baltimore). 2006;85:278–87.CrossRefGoogle Scholar
  12. 12.
    Peck AJ, Englund JA, Kuypers J, Guthrie KA, Corey L, Morrow R, et al. Respiratory virus infection among hematopoietic cell transplant recipients: evidence for asymptomatic parainfluenza virus infection. Blood. 2007;110:1681–8.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Ljungman P, Ward KN, Crooks BN, Parker A, Martino R, Shaw PJ, et al. Respiratory virus infections after stem cell transplantation: a prospective study from the infectious diseases working party of the European group for blood and marrow transplantation. Bone Marrow Transplant. 2001;28:479–84.PubMedCrossRefGoogle Scholar
  14. 14.
    Cordero E, de la Torre-Cisneros J, Moreno A, Perez-Romero P, Riera M. The impact of influenza A(H1N1)pdm09 infection on immunosuppressed patients. Enferm Infecc Microbiol Clin. 2012;30 Suppl 4:38–42.PubMedCrossRefGoogle Scholar
  15. 15.
    Cordero E, Perez-Romero P, Moreno A, Len O, Montejo M, Vidal E, et al. Pandemic influenza A(H1N1) virus infection in solid organ transplant recipients: impact of viral and non-viral co-infection. Clin Microbiol Infect. 2012;18:67–73.PubMedCrossRefGoogle Scholar
  16. 16.
    Vilchez RA, McCurry K, Dauber J, Lacono A, Griffith B, Fung J, et al. Influenza virus infection in adult solid organ transplant recipients. Am J Transplant. 2002;2:287–91.PubMedCrossRefGoogle Scholar
  17. 17.
    Kumar D, Michaels MG, Morris MI, Green M, Avery RK, Liu C, et al. Outcomes from pandemic influenza A H1N1 infection in recipients of solid-organ transplants: a multicentre cohort study. Lancet Infect Dis. 2010;10:521–6.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Ljungman P, de la Camara R, Perez-Bercoff L, Abecasis M, Nieto Campuzano JB, Cannata-Ortiz MJ, et al. Outcome of pandemic H1N1 infections in hematopoietic stem cell transplant recipients. Haematologica. 2011;96:1231–5.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Mohty B, Thomas Y, Vukicevic M, Nagy M, Levrat E, Bernimoulin M, et al. Clinical features and outcome of 2009-influenza A(H1N1) after allogeneic hematopoietic SCT. Bone Marrow Transplant. 2012;47:236–42.PubMedCrossRefGoogle Scholar
  20. 20.
    Khanna N, Steffen I, Studt JD, Schreiber A, Lehmann T, Weisser M, et al. Outcome of influenza infections in outpatients after allogeneic hematopoietic stem cell transplantation. Transpl Infect Dis. 2009;11:100–5.PubMedCrossRefGoogle Scholar
  21. 21.
    Chemaly RF, Hanmod SS, Rathod DB, Ghantoji SS, Jiang Y, Doshi A, et al. The characteristics and outcomes of parainfluenza virus infections in 200 patients with leukemia or recipients of hematopoietic stem cell transplantation. Blood. 2012;119:2738–45. quiz 969.PubMedCrossRefGoogle Scholar
  22. 22.
    Ustun C, Slaby J, Shanley RM, Vydra J, Smith AR, Wagner JE, et al. Human parainfluenza virus infection after hematopoietic stem cell transplantation: risk factors, management, mortality, and changes over time. Biol Blood Marrow Transplant. 2012;18:1580–8.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Nichols WG, Corey L, Gooley T, Davis C, Boeckh M. Parainfluenza virus infections after hematopoietic stem cell transplantation: risk factors, response to antiviral therapy, and effect on transplant outcome. Blood. 2001;98:573–8.PubMedCrossRefGoogle Scholar
  24. 24.
    Henrickson KJ. Parainfluenza viruses. Clin Microbiol Rev. 2003;16:242–64.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Lopez-Medrano F, Cordero E, Gavalda J, Cruzado JM, Marcos MA, Perez-Romero P, et al. Executive summary. Management of influenza infection in solid-organ transplant recipients: consensus statement of the group for the study of infection in transplant recipients (GESITRA) of the Spanish society of infectious diseases and clinical microbiology (SEIMC) and the Spanish network for research in infectious diseases (REIPI). Enferm Infecc Microbiol Clin. 2013;31:528–34.PubMedCrossRefGoogle Scholar
  26. 26.
    Chakrabarti S, Avivi I, Mackinnon S, Ward K, Kottaridis PD, Osman H, et al. Respiratory virus infections in transplant recipients after reduced-intensity conditioning with campath-1h: high incidence but low mortality. Br J Haematol. 2002;119:1125–32.PubMedCrossRefGoogle Scholar
  27. 27.
    Martino R, Porras RP, Rabella N, Williams JV, Ramila E, Margall N, et al. Prospective study of the incidence, clinical features, and outcome of symptomatic upper and lower respiratory tract infections by respiratory viruses in adult recipients of hematopoietic stem cell transplants for hematologic malignancies. Biol Blood Marrow Transplant. 2005;11:781–96.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Srinivasan A, Wang C, Yang J, Shenep JL, Leung WH, Hayden RT. Symptomatic parainfluenza virus infections in children undergoing hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2011;17:1520–7.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Choi SM, Boudreault AA, Xie H, Englund JA, Corey L, Boeckh M. Differences in clinical outcomes after 2009 influenza A/H1N1 and seasonal influenza among hematopoietic cell transplant recipients. Blood. 2011;117:5050–6.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Seo S, Xie H, Campbell AP, Kuypers JM, Leisenring WM, Englund JA, et al. Parainfluenza virus lower respiratory tract disease after hematopoietic cell transplant: viral detection in the lung predicts outcome. Clin Infect Dis. 2014;58:1357–68.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Espinosa-Aguilar L, Green JS, Forrest GN, Ball ED, Maziarz RT, Strasfeld L, et al. Novel H1N1 influenza in hematopoietic stem cell transplantation recipients: two centers’ experiences. Biol Blood Marrow Transplant. 2011;17:566–73.PubMedCrossRefGoogle Scholar
  32. 32.
    DeFabritus AM, Riggio RR, David DS, Senterfit LB, Cheigh JS, Stenzel KH. Parainfluenza type 3 in a transplant unit. JAMA. 1979;241:384–6.PubMedCrossRefGoogle Scholar
  33. 33.
    Smud A, Nagel CB, Madsen E, Rial Mdel C, Barcan LA, Gomez AA, et al. Pandemic influenza A/H1N1 virus infection in solid organ transplant recipients: a multicenter study. Transplantation. 2010;90:1458–62.PubMedCrossRefGoogle Scholar
  34. 34.
    Wendt CH, Weisdorf DJ, Jordan MC, Balfour Jr HH, Hertz MI. Parainfluenza virus respiratory infection after bone marrow transplantation. N Engl J Med. 1992;326:921–6.PubMedCrossRefGoogle Scholar
  35. 35.
    Apalsch AM, Green M, Ledesma-Medina J, Nour B, Wald ER. Parainfluenza and influenza virus infections in pediatric organ transplant recipients. Clin Infect Dis. 1995;20:394–9.PubMedCrossRefGoogle Scholar
  36. 36.
    Ljungman P. Respiratory virus infections in stem cell transplant patients: the European experience. Biol Blood Marrow Transplant. 2001;7(Suppl):5S–7S.PubMedCrossRefGoogle Scholar
  37. 37.
    Boudreault AA, Xie H, Leisenring W, Englund J, Corey L, Boeckh M. Impact of corticosteroid treatment and antiviral therapy on clinical outcomes in hematopoietic cell transplant patients infected with influenza virus. Biol Blood Marrow Transplant. 2011;17:979–86.PubMedCrossRefGoogle Scholar
  38. 38.
    Kim SH, Hong SB, Yun SC, Choi WI, Ahn JJ, Lee YJ, et al. Corticosteroid treatment in critically ill patients with pandemic influenza A/H1N1 2009 infection: analytic strategy using propensity scores. Am J Respir Crit Care Med. 2009;2011(183):1207–14.Google Scholar
  39. 39.
    Renaud C, Campbell AP. Changing epidemiology of respiratory viral infections in hematopoietic cell transplant recipients and solid organ transplant recipients. Curr Opin Infect Dis. 2011;24:333–43.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Vilchez RA, Fung J, Kusne S. The pathogenesis and management of influenza virus infection in organ transplant recipients. Transpl Infect Dis. 2002;4:177–82.PubMedCrossRefGoogle Scholar
  41. 41.
    Camargo LF, de Sandes-Freitas TV, Silva CD, Bittante CD, Ono G, Correa L, et al. Morbimortality of pandemic influenza A H1N1 infection in kidney transplant recipients requiring hospitalization: a comparative analysis with nonimmunocompromised patients. Transplantation. 2012;93:69–72.PubMedCrossRefGoogle Scholar
  42. 42.
    Pillet S, Lardeux M, Dina J, Grattard F, Verhoeven P, Le Goff J, et al. Comparative evaluation of six commercialized multiplex PCR kits for the diagnosis of respiratory infections. PLoS One. 2013;8:e72174.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Campbell AP, Kuypers J, Englund JA, Guthrie KA, Corey L, Boeckh M. Self-collection of foam nasal swabs for respiratory virus detection by PCR among immunocompetent subjects and hematopoietic cell transplant recipients. J Clin Microbiol. 2013;51:324–7.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Bowden RA, Ljungman P, Snydman DR, editors. Transplant infections diseases. 3rd ed. Philadelphia, PA; Lippincott Williams and Wilkins: 2010.Google Scholar
  45. 45.
    Kuypers J, Campbell AP, Cent A, Corey L, Boeckh M. Comparison of conventional and molecular detection of respiratory viruses in hematopoietic cell transplant recipients. Transpl Infect Dis. 2009;11:298–303.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Ebell MH. Diagnosing and treating patients with suspected influenza. Am Fam Physician. 2005;72:1789–92.PubMedGoogle Scholar
  47. 47.
    Waner JL, Todd SJ, Shalaby H, Murphy P, Wall LV. Comparison of Directigen FLU-A with viral isolation and direct immunofluorescence for the rapid detection and identification of influenza A virus. J Clin Microbiol. 1991;29:479–82.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Landry ML, Cohen S, Ferguson D. Real-time PCR compared to Binax now and cytospin-immunofluorescence for detection of influenza in hospitalized patients. J Clin Virol. 2008;43:148–51.PubMedCrossRefGoogle Scholar
  49. 49.
    Zimmerman RK, Rinaldo CR, Nowalk MP, Balasubramani GK, Thompson MG, Bullotta A, et al. Detection of influenza virus infection using two PCR methods. Adv Virol. 2014;2014:274679.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Wang R, Taubenberger JK. Methods for molecular surveillance of influenza. Expert Rev Anti Infect Ther. 2010;8:517–27.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Chartrand C, Leeflang MM, Minion J, Brewer T, Pai M. Accuracy of rapid influenza diagnostic tests: a meta-analysis. Ann Intern Med. 2012;156:500–11.PubMedCrossRefGoogle Scholar
  52. 52.
    Louie JK, Yang S, Yen C, Acosta M, Schechter R, Uyeki TM. Use of intravenous peramivir for treatment of severe influenza A(H1N1)pdm09. PLoS One. 2012;7:e40261.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    FDA grants first CLIA waiver for nucleic acid-based flu diagnostic test. http://www.fda.gov/newsevents/newsroom/pressannouncements/ucm429127.htm. Accessed 9 June 2015.
  54. 54.
    Templeton KE, Scheltinga SA, Beersma MF, Kroes AC, Claas EC. Rapid and sensitive method using multiplex real-time pcr for diagnosis of infections by influenza A and influenza B viruses, respiratory syncytial virus, and parainfluenza viruses 1, 2, 3, and 4. J Clin Microbiol. 2004;42:1564–9.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Dunn JJ, Woolstenhulme RD, Langer J, Carroll KC. Sensitivity of respiratory virus culture when screening with r-mix fresh cells. J Clin Microbiol. 2004;42:79–82.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Petric M, Comanor L, Petti CA. Role of the laboratory in diagnosis of influenza during seasonal epidemics and potential pandemics. J Infect Dis. 2006;194 Suppl 2:S98–110.PubMedCrossRefGoogle Scholar
  57. 57.
    Steed LL, Salmon VC, Overall Jr JC. Identification of influenza A virus by shell vial culture and two commercially available antigen detection methods. Clin Diagn Virol. 1994;2:261–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Zitterkopf NL, Leekha S, Espy MJ, Wood CM, Sampathkumar P, Smith TF. Relevance of influenza A virus detection by PCR, shell vial assay, and tube cell culture to rapid reporting procedures. J Clin Microbiol. 2006;44:3366–7.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Hajjar LA, Mauad T, Galas FR, Kumar A, da Silva LF, Dolhnikoff M, et al. Severe novel influenza A(H1N1) infection in cancer patients. Ann Oncol. 2010;21:2333–41.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Chemaly RF, Vigil KJ, Saad M, Vilar-Compte D, Cornejo-Juarez P, Perez-Jimenez C, et al. A multicenter study of pandemic influenza A(H1N1) infection in patients with solid tumors in 3 countries: early therapy improves outcomes. Cancer. 2012;118:4627–33.PubMedCrossRefGoogle Scholar
  61. 61.
    Chemaly RF, Shah DP, Boeckh MJ. Management of respiratory viral infections in hematopoietic cell transplant recipients and patients with hematologic malignancies. Clin Infect Dis. 2014;59 Suppl 5:S344–51.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Ison MG, Fraiz J, Heller B, Jauregui L, Mills G, O'Riordan W, et al. Intravenous peramivir for treatment of influenza in hospitalized patients. Antivir Ther. 2014;19:349–61.PubMedCrossRefGoogle Scholar
  63. 63.
    FDA approves RAPIVAB to treat flu infection. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm427755.htmcited. 9 June 2015.
  64. 64.
    Ison MG. Antivirals and resistance: influenza virus. Curr Opin Virol. 2011;1:563–73.PubMedCrossRefGoogle Scholar
  65. 65.
    Conditions of use, conditions for distribution and patients targeted and conditions for safety monitoring addressed to member states for iv zanamivir available for compassionate use. 2011. http://www.ema.europa.eu/docs/en_GB/document_library/Other/2010/02/WC500074124.pdfcited. 28 August 2015.
  66. 66.
    Casper C, Englund J, Boeckh M. How I treat influenza in patients with hematologic malignancies. Blood. 2010;115:1331–42.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Watcharananan SP, Suwatanapongched T, Wacharawanichkul P, Chantratitaya W, Mavichak V, Mossad SB. Influenza A/H1N1 2009 pneumonia in kidney transplant recipients: characteristics and outcomes following high-dose oseltamivir exposure. Transpl Infect Dis. 2009;2010(12):127–31.Google Scholar
  68. 68.
    Dong G, Peng C, Luo J, Wang C, Han L, Wu B, et al. Adamantane-resistant influenza A viruses in the world (1902–2013): frequency and distribution of M2 gene mutations. PLoS One. 2015;10, e0119115.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Quispe-Laime AM, Bracco JD, Barberio PA, Campagne CG, Rolfo VE, Umberger R, et al. H1N1 influenza A virus-associated acute lung injury: response to combination oseltamivir and prolonged corticosteroid treatment. Intensive Care Med. 2010;36:33–41.PubMedCrossRefGoogle Scholar
  70. 70.
    Shah DP, El Taoum KK, Shah JN, Vigil KJ, Adachi JA, Granwehr BP, et al. Characteristics and outcomes of pandemic 2009/H1N1 versus seasonal influenza in children with cancer. Pediatr Infect Dis J. 2012;31:373–8.PubMedCrossRefGoogle Scholar
  71. 71.
    Abed Y, Goyette N, Boivin G. Generation and characterization of recombinant influenza A(H1N1) viruses harboring amantadine resistance mutations. Antimicrob Agents Chemother. 2005;49:556–9.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Baranovich T, Bahl J, Marathe BM, Culhane M, Stigger-Rosser E, Darnell D, et al. Influenza A viruses of swine circulating in the United States during 2009–2014 are susceptible to neuraminidase inhibitors but show lineage-dependent resistance to adamantanes. Antiviral Res. 2015;117:10–9.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Thorlund K, Awad T, Boivin G, Thabane L. Systematic review of influenza resistance to the neuraminidase inhibitors. BMC Infect Dis. 2011;11:134.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Nitsch-Osuch A, Brydak LB. Influenza viruses resistant to neuraminidase inhibitors. Acta Biochim Pol. 2014;61:505–8.PubMedGoogle Scholar
  75. 75.
    Lackenby A, Hungnes O, Dudman SG, Meijer A, Paget WJ, Hay AJ, et al. Emergence of resistance to oseltamivir among influenza A(H1N1) viruses in Europe. Euro Surveill. 2008;13.Google Scholar
  76. 76.
    Baz M, Abed Y, Simon P, Hamelin ME, Boivin G. Effect of the neuraminidase mutation H274Y conferring resistance to oseltamivir on the replicative capacity and virulence of old and recent human influenza A(H1N1) viruses. J Infect Dis. 2010;201:740–5.PubMedCrossRefGoogle Scholar
  77. 77.
    Takashita E, Meijer A, Lackenby A, Gubareva L, Rebelo-de-Andrade H, Besselaar T, et al. Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013–2014. Antiviral Res. 2015;117:27–38.PubMedCrossRefGoogle Scholar
  78. 78.
    Renaud C, Boudreault AA, Kuypers J, Lofy KH, Corey L, Boeckh MJ, et al. H275y mutant pandemic (H1N1) 2009 virus in immunocompromised patients. Emerg Infect Dis. 2011;17:653–60. quiz 765.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Valinotto LE, Diez RA, Barrero PR, Farias JA, Lopez EL, Mistchenko AS. Emergence of intratreatment resistance to oseltamivir in pandemic influenza A H1N1 2009 virus. Antivir Ther. 2010;15:923–7.PubMedCrossRefGoogle Scholar
  80. 80.
    Gooskens J, Jonges M, Claas EC, Meijer A, Kroes AC. Prolonged influenza virus infection during lymphocytopenia and frequent detection of drug-resistant viruses. J Infect Dis. 2009;199:1435–41.PubMedCrossRefGoogle Scholar
  81. 81.
    Weinstock DM, Gubareva LV, Zuccotti G. Prolonged shedding of multidrug-resistant influenza A virus in an immunocompromised patient. N Engl J Med. 2003;348:867–8.PubMedCrossRefGoogle Scholar
  82. 82.
    Renaud C, Pergam SA, Polyak C, Jain R, Kuypers J, Englund JA, et al. Early emergence of an H275Y mutation in a hematopoietic cell transplant recipient treated with intravenous peramivir. Transpl Infect Dis. 2010;12:513–7.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Shetty AK, Ross GA, Pranikoff T, Gubareva LV, Sechrist C, Guirand DM, et al. Oseltamivir-resistant 2009 H1N1 influenza pneumonia during therapy in a renal transplant recipient. Pediatr Transplant. 2012;16:E153–7.PubMedCrossRefGoogle Scholar
  84. 84.
    Takashita E, Fujisaki S, Kishida N, Xu H, Imai M, Tashiro M, et al. Characterization of neuraminidase inhibitor-resistant influenza A(H1N1)pdm09 viruses isolated in four seasons during pandemic and post-pandemic periods in Japan. Influenza Other Respir Viruses. 2013;7:1390–9.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Johny AA, Clark A, Price N, Carrington D, Oakhill A, Marks DI. The use of zanamivir to treat influenza A and B infection after allogeneic stem cell transplantation. Bone Marrow Transplant. 2002;29:113–5.PubMedCrossRefGoogle Scholar
  86. 86.
    Harter G, Zimmermann O, Maier L, Schubert A, Mertens T, Kern P, et al. Intravenous zanamivir for patients with pneumonitis due to pandemic (H1N1) 2009 influenza virus. Clin Infect Dis. 2010;50:1249–51.PubMedCrossRefGoogle Scholar
  87. 87.
    Tamura D, DeBiasi RL, Okomo-Adhiambo M, Mishin VP, Campbell AP, Loechelt B, et al. Emergence of Multidrug-Resistant Influenza A(H1N1)pdm09 Virus Variants in an Immunocompromised Child Treated With Oseltamivir and Zanamivir J Infect Dis. 2015; 212(8):1209–13.Google Scholar
  88. 88.
    Nguyen HT, Fry AM, Loveless PA, Klimov AI, Gubareva LV. Recovery of a multidrug-resistant strain of pandemic influenza A 2009 (H1N1) virus carrying a dual H275Y/I223R mutation from a child after prolonged treatment with oseltamivir. Clin Infect Dis. 2010;51:983–4.PubMedCrossRefGoogle Scholar
  89. 89.
    Laplante J, St George K. Antiviral resistance in influenza viruses: laboratory testing. Clin Lab Med. 2014;34:387–408.PubMedCrossRefGoogle Scholar
  90. 90.
    Chan-Tack KM, Murray JS, Birnkrant DB. Use of ribavirin to treat influenza. N Engl J Med. 2009;361:1713–4.PubMedCrossRefGoogle Scholar
  91. 91.
    Nguyen JT, Hoopes JD, Le MH, Smee DF, Patick AK, Faix DJ, et al. Triple combination of amantadine, ribavirin, and oseltamivir is highly active and synergistic against drug resistant influenza virus strains in vitro. PLoS One. 2010;5, e9332.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    An open label study to examine the effects of das181 administered by dry powder inhaler (dpi) or nebulized formulation in immunocompromised subjects with parainfluenza (piv) infection. https://clinicaltrials.gov/ct2/show/NCT01924793cited. 8 June 2015.
  93. 93.
    Moss RB, Hansen C, Sanders RL, Hawley S, Li T, Steigbigel RT. A phase ii study of das181, a novel host directed antiviral for the treatment of influenza infection. J Infect Dis. 2012;206:1844–51.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Smee DF, Tarbet EB, Furuta Y, Morrey JD, Barnard DL. Synergistic combinations of favipiravir and oseltamivir against wild-type pandemic and oseltamivir-resistant influenza A virus infections in mice. Future Virol. 2013;8:1085–94.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Tarbet EB, Vollmer AH, Hurst BL, Barnard DL, Furuta Y, Smee DF. In vitro activity of favipiravir and neuraminidase inhibitor combinations against oseltamivir-sensitive and oseltamivir-resistant pandemic influenza A(H1N1) virus. Arch Virol. 2014;159:1279–91.PubMedCrossRefGoogle Scholar
  96. 96.
    Rossignol JF, La Frazia S, Chiappa L, Ciucci A, Santoro MG. Thiazolides, a new class of anti-influenza molecules targeting viral hemagglutinin at the post-translational level. J Biol Chem. 2009;284:29798–808.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Haffizulla J, Hartman A, Hoppers M, Resnick H, Samudrala S, Ginocchio C, et al. Effect of nitazoxanide in adults and adolescents with acute uncomplicated influenza: a double-blind, randomised, placebo-controlled, phase 2b/3 trial. Lancet Infect Dis. 2014;14:609–18.PubMedCrossRefGoogle Scholar
  98. 98.
    Limberis MP, Adam VS, Wong G, Gren J, Kobasa D, Ross TM, et al. Intranasal antibody gene transfer in mice and ferrets elicits broad protection against pandemic influenza. Sci Transl Med. 2013;5:187ra72.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Wong JP, Saravolac EG, Sabuda D, Levy HB, Kende M. Prophylactic and therapeutic efficacies of poly(IC.LC) against respiratory influenza A virus infection in mice. Antimicrob Agents Chemother. 1995;39:2574–6.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Jefferson T, Del Mar C, Dooley L, Ferroni E, Al-Ansary LA, Bawazeer GA, et al. Physical interventions to interrupt or reduce the spread of respiratory viruses: systematic review. BMJ. 2009;339:b3675.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Siegel JD, Rhinehart E, Jackson M, Chiarello L, Health Care Infection Control Practices Advisory C 2007 guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control 2007:35:S65–164Google Scholar
  102. 102.
    Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, et al. Prevention and control of seasonal influenza with vaccines: recommendations of the advisory committee on immunization practices (ACIP), 2009. MMWR Recomm Rep. 2009;58:1–52.PubMedGoogle Scholar
  103. 103.
    Chen LF, Dailey NJ, Rao AK, Fleischauer AT, Greenwald I, Deyde VM, et al. Cluster of oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infections on a hospital ward among immunocompromised patients—North Carolina, 2009. J Infect Dis. 2011;203:838–46.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Moore C, Galiano M, Lackenby A, Abdelrahman T, Barnes R, Evans MR, et al. Evidence of person-to-person transmission of oseltamivir-resistant pandemic influenza A(H1N1) 2009 virus in a hematology unit. J Infect Dis. 2011;203:18–24.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Tomblyn M, Chiller T, Einsele H, Gress R, Sepkowitz K, Storek J, et al. Guidelines for preventing infectious complications among hematopoietic cell transplant recipients: a global perspective. Preface Bone Marrow Transplant. 2009;44:453–5.PubMedCrossRefGoogle Scholar
  106. 106.
    Grohskopf LA, Olsen SJ, Sokolow LZ, Bresee JS, Cox NJ, Broder KR, et al. Prevention and control of seasonal influenza with vaccines: recommendations of the advisory committee on immunization practices (ACIP)—United States, 2014–15 influenza season. MMWR Morb Mortal Wkly Rep. 2014;63:691–7.PubMedGoogle Scholar
  107. 107.
    Engelhard D, Nagler A, Hardan I, Morag A, Aker M, Baciu H, et al. Antibody response to a two-dose regimen of influenza vaccine in allogeneic T cell-depleted and autologous BMT recipients. Bone Marrow Transplant. 1993;11:1–5.PubMedGoogle Scholar
  108. 108.
    Issa NC, Marty FM, Gagne LS, Koo S, Verrill KA, Alyea EP, et al. Seroprotective titers against 2009 H1N1 influenza A virus after vaccination in allogeneic hematopoietic stem cell transplantation recipients. Biol Blood Marrow Transplant. 2011;17:434–8.PubMedCrossRefGoogle Scholar
  109. 109.
    Beck CR, McKenzie BC, Hashim AB, Harris RC, University of Nottingham I, the ImmunoCompromised Study G, et al. Influenza vaccination for immunocompromised patients: systematic review and meta-analysis by etiology. J Infect Dis. 2012:206:1250-9.Google Scholar
  110. 110.
    Schuurmans MM, Tini GM, Dalar L, Fretz G, Benden C, Boehler A. Pandemic 2009 H1N1 influenza virus vaccination in lung transplant recipients: coverage, safety and clinical effectiveness in the Zurich cohort. J Heart Lung Transplant. 2011;30:685–90.PubMedCrossRefGoogle Scholar
  111. 111.
    Machado CM, Cardoso MR, da Rocha IF, Boas LS, Dulley FL, Pannuti CS. The benefit of influenza vaccination after bone marrow transplantation. Bone Marrow Transplant. 2005;36:897–900.PubMedCrossRefGoogle Scholar
  112. 112.
    Ljungman P. Vaccination of immunocompromised patients. Clin Microbiol Infect. 2012;18 Suppl 5:93–9.PubMedCrossRefGoogle Scholar
  113. 113.
    Rubin LG, Levin MJ, Ljungman P, Davies EG, Avery R, Tomblyn M, et al. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis. 2014;58:309–18.PubMedCrossRefGoogle Scholar
  114. 114.
    Ariza-Heredia EJ, Gulbis AM, Stolar KR, Kebriaei P, Shah DP, McConn KK, et al. Vaccination guidelines after hematopoietic stem cell transplantation: practitioners’ knowledge, attitudes, and gap between guidelines and clinical practice. Transpl Infect Dis. 2014;16:878–86.PubMedCrossRefGoogle Scholar
  115. 115.
    Chon WJ, Kadambi PV, Harland RC, Thistlethwaite JR, West BL, Udani S, et al. Changing attitudes toward influenza vaccination in U.S. Kidney transplant programs over the past decade. Clin J Am Soc Nephrol. 2010;5:1637–41.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Azzi J, Ella A-H, Shah D, Nesher L, Ghantoji S, Michailidis L, Marsh L, Chemaly R. The impact of influenza vaccination in patients with cancer on subsequent disease during the 2013–2014 influenza season. In Infectious Diseases Society of America meeting ID week 2014; 10 Oct 2014; Philadelphia, PA.Google Scholar
  117. 117.
    Thomas RE, Jefferson TO, Demicheli V, Rivetti D. Influenza vaccination for health-care workers who work with elderly people in institutions: a systematic review. Lancet Infect Dis. 2006;6:273–9.PubMedCrossRefGoogle Scholar
  118. 118.
    Erard V, Chien JW, Kim HW, Nichols WG, Flowers ME, Martin PJ, et al. Airflow decline after myeloablative allogeneic hematopoietic cell transplantation: the role of community respiratory viruses. J Infect Dis. 2006;193:1619–25.PubMedCrossRefGoogle Scholar
  119. 119.
    Kumar D, Erdman D, Keshavjee S, Peret T, Tellier R, Hadjiliadis D, et al. Clinical impact of community-acquired respiratory viruses on bronchiolitis obliterans after lung transplant. Am J Transplant. 2005;5:2031–6.PubMedCrossRefGoogle Scholar
  120. 120.
    Fry AM, Curns AT, Harbour K, Hutwagner L, Holman RC, Anderson LJ. Seasonal trends of human parainfluenza viral infections: United States, 1990–2004. Clin Infect Dis. 2006;43:1016–22.PubMedCrossRefGoogle Scholar
  121. 121.
    Rihkanen H, Ronkko E, Nieminen T, Komsi KL, Raty R, Saxen H, et al. Respiratory viruses in laryngeal croup of young children. J Pediatr. 2008;152:661–5.PubMedCrossRefGoogle Scholar
  122. 122.
    Vilchez R, McCurry K, Dauber J, Iacono A, Keenan R, Griffith B, et al. Influenza and parainfluenza respiratory viral infection requiring admission in adult lung transplant recipients. Transplantation. 2002;73:1075–8.PubMedCrossRefGoogle Scholar
  123. 123.
    Lewis VA, Champlin R, Englund J, Couch R, Goodrich JM, Rolston K, et al. Respiratory disease due to parainfluenza virus in adult bone marrow transplant recipients. Clin Infect Dis. 1996;23:1033–7.PubMedCrossRefGoogle Scholar
  124. 124.
    Wendt CH, Hertz MI. Respiratory syncytial virus and parainfluenza virus infections in the immunocompromised host. Semin Respir Infect. 1995;10:224–31.PubMedGoogle Scholar
  125. 125.
    Vilchez RA, McCurry K, Dauber J, Iacono A, Keenan R, Zeevi A, et al. The epidemiology of parainfluenza virus infection in lung transplant recipients. Clin Infect Dis. 2001;33:2004–8.PubMedCrossRefGoogle Scholar
  126. 126.
    Vilchez RA, Dauber J, McCurry K, Iacono A, Kusne S. Parainfluenza virus infection in adult lung transplant recipients: an emergent clinical syndrome with implications on allograft function. Am J Transplant. 2003;3:116–20.PubMedCrossRefGoogle Scholar
  127. 127.
    Sable CA, Hayden FG. Orthomyxoviral and paramyxoviral infections in transplant patients. Infect Dis Clin North Am. 1995;9:987–1003.PubMedGoogle Scholar
  128. 128.
    Vu DL, Bridevaux PO, Aubert JD, Soccal PM, Kaiser L. Respiratory viruses in lung transplant recipients: a critical review and pooled analysis of clinical studies. Am J Transplant. 2011;11:1071–8.PubMedCrossRefGoogle Scholar
  129. 129.
    Fan J, Henrickson KJ. Rapid diagnosis of human parainfluenza virus type 1 infection by quantitative reverse transcription-PCR-enzyme hybridization assay. J Clin Microbiol. 1996;34:1914–7.PubMedPubMedCentralGoogle Scholar
  130. 130.
    Ferguson PE, Sorrell TC, Bradstock K, Carr P, Gilroy NM. Parainfluenza virus type 3 pneumonia in bone marrow transplant recipients: multiple small nodules in high- resolution lung computed tomography scans provide a radiological clue to diagnosis. Clin Infect Dis. 2009;48:905–9.PubMedCrossRefGoogle Scholar
  131. 131.
    Lange T, Franke G, Niederwieser D. Parotitis associated with a parainfluenza virus type 3 infection during aplasia after unrelated allogeneic stem cell transplantation. Leuk Lymphoma. 2006;47:1714–5.PubMedCrossRefGoogle Scholar
  132. 132.
    Vigil KJ, Mulanovich VE, Chemaly RF, Tarrand J, Raad II, Adachi JA. Severe parainfluenza virus type 2 supraglottitis in an immunocompetent adult host: An unusual cause of a paramyxoviridae viral infection. J Intern Med. 2009;265:397–400.PubMedCrossRefGoogle Scholar
  133. 133.
    Safdar A, Rodriguez GH, Mihu CN, Mora-Ramos L, Mulanovich V, Chemaly RF, et al. Infections in non-myeloablative hematopoietic stem cell transplantation patients with lymphoid malignancies: spectrum of infections, predictors of outcome and proposed guidelines for fungal infection prevention. Bone Marrow Transplant. 2010;45:339–47.PubMedCrossRefGoogle Scholar
  134. 134.
    Billings JL, Hertz MI, Savik K, Wendt CH. Respiratory viruses and chronic rejection in lung transplant recipients. J Heart Lung Transplant. 2002;21:559–66.PubMedCrossRefGoogle Scholar
  135. 135.
    Renaud C, Englund JA. Antiviral therapy of respiratory viruses in haematopoietic stem cell transplant recipients. Antivir Ther. 2012;17:175–91.PubMedCrossRefGoogle Scholar
  136. 136.
    Park SY, Baek S, Lee SO, Choi SH, Kim YS, Woo JH, et al. Efficacy of oral ribavirin in hematologic disease patients with paramyxovirus infection: analytic strategy using propensity scores. Antimicrob Agents Chemother. 2013;57:983–9.PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Fuehner T, Dierich M, Duesberg C, DeWall C, Welte T, Haverich A, et al. Single-centre experience with oral ribavirin in lung transplant recipients with paramyxovirus infections. Antivir Ther. 2011;16:733–40.PubMedCrossRefGoogle Scholar
  138. 138.
    Sparrelid E, Ljungman P, Ekelof-Andstrom E, Aschan J, Ringden O, Winiarski J, et al. Ribavirin therapy in bone marrow transplant recipients with viral respiratory tract infections. Bone Marrow Transplant. 1997;19:905–8.PubMedCrossRefGoogle Scholar
  139. 139.
    Chalkias S, Mackenzie MR, Gay C, Dooley C, Marty FM, Moss RB, et al. Das181 treatment of hematopoietic stem cell transplant patients with parainfluenza virus lung disease requiring mechanical ventilation. Transpl Infect Dis. 2014;16:141–4.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Ansun BioPharma I. An open label study to examine the effects of das181 administered by dry powder inhaler (dpi) or nebulized formulation in immunocompromised subjects with parainfluenza (piv) infection. Available from clinicaltrials.Gov. Web site: https://clinicaltrials.gov/ct2/show/NCT01924793cited. 8 June 2015.
  141. 141.
    Alymova IV, Watanabe M, Boyd KL, Chand P, Babu YS, Portner A. Efficacy of the novel parainfluenza virus haemagglutinin-neuraminidase inhibitor BCX 2798 in mice—further evaluation. Antivir Ther. 2009;14:891–8.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Liu V, Dhillon GS, Weill D. A multi-drug regimen for respiratory syncytial virus and parainfluenza virus infections in adult lung and heart-lung transplant recipients. Transpl Infect Dis. 2010;12:38–44.PubMedCrossRefGoogle Scholar
  143. 143.
    Ottolini MG, Porter DD, Blanco JC, Prince GA. A cotton rat model of human parainfluenza 3 laryngotracheitis: virus growth, pathology, and therapy. J Infect Dis. 2002;186:1713–7.PubMedCrossRefGoogle Scholar
  144. 144.
    Prince GA, Porter DD. Treatment of parainfluenza virus type 3 bronchiolitis and pneumonia in a cotton rat model using topical antibody and glucocorticosteroid. J Infect Dis. 1996;173:598–608.PubMedCrossRefGoogle Scholar
  145. 145.
    van der Veen J, Poort Y, Birchfield DJ. Effect of relative humidity on experimental transmission of Sendai virus in mice. 1. Proc Soc Exp Biol Med. 1972;140:1437–40.PubMedCrossRefGoogle Scholar
  146. 146.
    Brady MT, Evans J, Cuartas J. Survival and disinfection of parainfluenza viruses on environmental surfaces. Am J Infect Control. 1990;18:18–23.PubMedCrossRefGoogle Scholar
  147. 147.
    Zambon M, Bull T, Sadler CJ, Goldman JM, Ward KN. Molecular epidemiology of two consecutive outbreaks of parainfluenza 3 in a bone marrow transplant unit. J Clin Microbiol. 1998;36:2289–93.PubMedPubMedCentralGoogle Scholar
  148. 148.
    Nichols WG, Erdman DD, Han A, Zukerman C, Corey L, Boeckh M. Prolonged outbreak of human parainfluenza virus 3 infection in a stem cell transplant outpatient department: Insights from molecular epidemiologic analysis. Biol Blood Marrow Transplant. 2004;10:58–64.PubMedCrossRefGoogle Scholar
  149. 149.
    Maziarz RT, Sridharan P, Slater S, Meyers G, Post M, Erdman DD, et al. Control of an outbreak of human parainfluenza virus 3 in hematopoietic stem cell transplant recipients. Biol Blood Marrow Transplant. 2010;16:192–8.PubMedCrossRefGoogle Scholar
  150. 150.
    Adderson E, Branum K, Sealy RE, Jones BG, Surman SL, Penkert R, et al. Safety and immunogenicity of an intranasal Sendai virus-based human parainfluenza virus type 1 vaccine in 3- to 6-year-old children. Clin Vaccine Immunol. 2015;22:298–303.PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Karron RA, Wright PF, Newman FK, Makhene M, Thompson J, Samorodin R, et al. A live human parainfluenza type 3 virus vaccine is attenuated and immunogenic in healthy infants and children. J Infect Dis. 1995;172:1445–50.PubMedCrossRefGoogle Scholar
  152. 152.
    Chaparro C, Scavuzzo M, Winton T, Keshavjee S, Kesten S. Status of lung transplant recipients surviving beyond five years. J Heart Lung Transplant. 1997;16:511–6.PubMedGoogle Scholar
  153. 153.
    Tazelaar HD. Perivascular inflammation in pulmonary infections: implications for the diagnosis of lung rejection. J Heart Lung Transplant. 1991;10:437–41.PubMedGoogle Scholar
  154. 154.
    Yoshihara S, Yanik G, Cooke KR, Mineishi S. Bronchiolitis obliterans syndrome (bos), bronchiolitis obliterans organizing pneumonia (boop), and other late-onset noninfectious pulmonary complications following allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2007;13:749–59.PubMedCrossRefGoogle Scholar
  155. 155.
    Filipovich AH, Weisdorf D, Pavletic S, Socie G, Wingard JR, Lee SJ, et al. National institutes of health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant. 2005;11:945–56.PubMedCrossRefGoogle Scholar
  156. 156.
    Shah DP, Alousi AA, Bashoura L, Shah PK, Mahajan S, Mulanovich VE, Ariza-Heredia EJ, Chemaly RF. Bronchiolitis obliterans following respiratory viral infections in allogeneic hematopoietic stem cell transplant recipients. In Interscience conference on antimicrobial agens and chemotherapy (ICAAC); San Francisco, CA, USA.Google Scholar
  157. 157.
    Le Page AK, Kainer G, Glanville AR, Tu E, Bhonagiri D, Rawlinson WD. Influenza B virus transmission in recipients of kidney and lung transplants from an infected donor. Transplantation. 2010;90:99–102.PubMedCrossRefGoogle Scholar
  158. 158.
    Meylan PR, Aubert JD, Kaiser L. Influenza transmission to recipient through lung transplantation. Transpl Infect Dis. 2007;9:55–7.PubMedCrossRefGoogle Scholar
  159. 159.
    Cockbain AJ, Jacob M, Ecuyer C, Hostert L, Ahmad N. Transplantation of solid organs procured from influenza A H1N1 infected donors. Transpl Int. 2011;24:e107–10.PubMedCrossRefGoogle Scholar
  160. 160.
    Campbell AP, Guthrie KA, Englund JA, Farney RM, Minerich EL, Kuypers J, et al. Clinical outcomes associated with respiratory virus detection before allogeneic hematopoietic stem cell transplant. Clin Infect Dis. 2015;61:192–202.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Infectious Diseases, Infection Control, & Employee Healthhe University of Texas MD Anderson Cancer CenterHoustonUSA

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