Human Polyomavirus and Papillomavirus Infection and Disease Posttransplant

Chapter

Abstract

Human papillomavirus (HPV) and human polyomavirus (HPyV) infections are widespread in the general population, but cause very little acute illness. However, certain HPV species are the key etiology of condylomata acuminata, cervical cancer, and also anorectal and head-and-neck cancer, and potentially preventable by current vaccines in immunocompetent individuals. In immunocompromised patients, particularly after solid organ transplantation or hematopoietic stem transplantation, HPV and HPyV show an aggravated clinical course. Here, aspects of pathogenesis, diagnosis, and clinical management are discussed for HPyV-associated nephropathy, hemorrhagic cystitis, and progressive multifocal leukoencephalopathy, as well as HPV-associated proliferative disorders of skin and mucosa including cancer.

Keywords

Polyoma Papilloma Nephropathy Nephritis Cancer Cervix Virus Transplantation 

References

  1. 1.
    Hirsch HH. Virus infections post transplant: risk and immunity. Transpl Infect Dis. 2005;7(3–4):97–8.PubMedCrossRefGoogle Scholar
  2. 2.
    Emery VC, Sabin CA, Cope AV, Gor D, Hassan-Walker AF, Griffiths PD. Application of viral-load kinetics to identify patients who develop cytomegalovirus disease after transplantation. Lancet. 2000;355(9220):2032–6.PubMedCrossRefGoogle Scholar
  3. 3.
    Funk GF, Gosert R, Hirsch HH. Viral dynamics in transplant patients: implication for disease. Lancet Infect Dis. 2007;7(6):460–72.PubMedCrossRefGoogle Scholar
  4. 4.
    Connolly K, Manders P, Earls P, Epstein RJ. Papillomavirus-associated squamous skin cancers following transplant immunosuppression: one Notch closer to control. Cancer Treat Rev. 2014;40(2):205–14.PubMedCrossRefGoogle Scholar
  5. 5.
    Timpone Jr JG, Girlanda R, Rudolph L, Fishbein TM. Infections in intestinal and multivisceral transplant recipients. Infect Dis Clin North Am. 2013;27(2):359–77.PubMedCrossRefGoogle Scholar
  6. 6.
    Helantera I, Egli A, Koskinen P, Lautenschlager I, Hirsch HH. Viral impact on long-term kidney graft function. Infect Dis Clin North Am. 2010;24(2):339–71.PubMedCrossRefGoogle Scholar
  7. 7.
    Buettner M, Xu H, Bohme R, Seliger B, Jacobi J, Wiesener M, et al. Predominance of Th2 cells and plasma cells in polyoma virus nephropathy: a role for humoral immunity? Hum Pathol. 2012;43(9):1453–62.PubMedCrossRefGoogle Scholar
  8. 8.
    Büchen-Osmond C. International Committee on Taxonomy of Viruses Database (ICTVdB). 2008. http://www.ncbi.nlm.nih.gov/ICTVdb/:nn.
  9. 9.
    Polyomaviridae Study Group of the International Committee on Taxonomy of Viruses, Calvignac-Spencer S, Feltkamp MCW, Daugherty MD, Moens U, Ramqvist T, Johne R, Ehlers B. A taxonomy update for the family Polyomaviridae. Arch Virol. 2016; (epub ahead of print; doi:10. 1007/ s00705-016-2794-y).Google Scholar
  10. 10.
    Viruses ICoTo. Virus Taxonomy: 2014 Release. 2014. Available from: http://www.ictvonline.org/virustaxonomy.asp. Accessed 29 Aug 2015.
  11. 11.
    Cole CN. Polyomavirinae: the viruses and their replication. In: Bernard N, Fields DMK, Howley PM, editors. Fundamental virology. 3rd ed. New York: Lippincott-Raven Publishers; 1996. p. 917–45.Google Scholar
  12. 12.
    Rinaldo CH, Hirsch HH. The human polyomaviruses: from orphans and mutants to patchwork family. APMIS. 2013;121:681–4.PubMedCrossRefGoogle Scholar
  13. 13.
    Hirsch HH, Babel N, Comoli P, Friman V, Ginevri F, Jardine A, et al. European perspective on human polyomavirus infection, replication and disease in solid organ transplantation. Clin Microbiol Infect. 2014;20 Suppl 7:74–88.PubMedCrossRefGoogle Scholar
  14. 14.
    Bofill-Mas S, Formiga-Cruz M, Clemente-Casares P, Calafell F, Girones R. Potential transmission of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA. J Virol. 2001;75(21):10290–9.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Egli A, Dumoulin A, Köhli S, Hirsch HH. Polyomavirus BK after kidney transplantation—role of molecular and immunological markers. Trends Transplant. 2009;3:85–102.Google Scholar
  16. 16.
    Cinque P, Dumoulin A, Hirsch HH. Diagnosis of polyomavirus infection, replication and disease. In: Jerome K, editor. Laboratory diagnosis of viral infections. USA: Informa Healthcare; 2009. p. 401–24.Google Scholar
  17. 17.
    Shah KV, Daniel RW, Warszawski RM. High prevalence of antibodies to BK virus, an SV40-related papovavirus, in residents of Maryland. J Infect Dis. 1973;128(6):784–7.PubMedCrossRefGoogle Scholar
  18. 18.
    Knowles WA, Pipkin P, Andrews N, Vyse A, Minor P, Brown DW, et al. Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40. J Med Virol. 2003;71(1):115–23.PubMedCrossRefGoogle Scholar
  19. 19.
    Egli A, Infanti L, Dumoulin A, Buser A, Samaridis J, Stebler C, et al. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis. 2009;199:837–46.PubMedCrossRefGoogle Scholar
  20. 20.
    Kean JM, Rao S, Wang M, Garcea RL. Seroepidemiology of human polyomaviruses. PLoS Pathog. 2009;5(3), e1000363.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Schmidt T, Adam C, Hirsch HH, Janssen MW, Wolf M, Dirks J, et al. BK polyomavirus-specific cellular immune responses are age-dependent and strongly correlate with phases of virus replication. Am J Transplant. 2014;14(6):1334–45.PubMedCrossRefGoogle Scholar
  22. 22.
    Bodaghi S, Comoli P, Boesch R, Azzi A, Gosert R, Leuenberger D, Ginevri F, Hirsch HH. Antibody responses to recombinant polyomavirus BK large T and VP1 proteins in pediatric kidney transplant patients. J Clin Microbiol. 2009;47(8):2577–85.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Cheng XS, Bohl DL, Storch GA, Ryschkewitsch C, Gaudreault-Keener M, Major EO, et al. Inhibitory interactions between BK and JC virus among kidney transplant recipients. J Am Soc Nephrol. 2011;22(5):825–31.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Hirsch HH, Kardas P, Kranz D, Leboeuf C. The human JC polyomavirus (JCPyV): virological background and clinical implications. APMIS. 2013;121:685–727.PubMedCrossRefGoogle Scholar
  25. 25.
    Knowles WA, Pillay D, Johnson MA, Hand JF, Brown DW. Prevalence of long-term BK and JC excretion in HIV-infected adults and lack of correlation with serological markers. J Med Virol. 1999;59(4):474–9.PubMedCrossRefGoogle Scholar
  26. 26.
    Khanna N, Wolbers M, Mueller NJ, Garzoni C, Du Pasquier RA, Fux CA, et al. JC virus-specific immune responses in human immunodeficiency virus type 1 patients with progressive multifocal leukoencephalopathy. J Virol. 2009;83(9):4404–11.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Nicol JT, Leblond V, Arnold F, Guerra G, Mazzoni E, Tognon M, et al. Seroprevalence of human Malawi polyomavirus. J Clin Microbiol. 2014;52(1):321–3.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Nicol JT, Robinot R, Carpentier A, Carandina G, Mazzoni E, Tognon M, et al. Age-specific seroprevalences of Merkel cell polyomavirus, human polyomaviruses 6, 7, and 9, and trichodysplasia spinulosa-associated polyomavirus. Clin Vaccine Immunol. 2013;20(3):363–8.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Rinaldo CH, Tylden GD, Sharma BN. The human polyomavirus BK (BKPyV): virological background and clinical implications. APMIS. 2013;121:728–45.PubMedCrossRefGoogle Scholar
  30. 30.
    Bialasiewicz S, Whiley DM, Lambert SB, Wang D, Nissen MD, Sloots TP. A newly reported human polyomavirus, KI virus, is present in the respiratory tract of Australian children. J Clin Virol. 2007;40(1):15–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Babakir-Mina M, Ciccozzi M, Perno CF, Ciotti M. The human polyomaviruses KI and WU: virological background and clinical implications. APMIS. 2013;121:746–54.PubMedCrossRefGoogle Scholar
  32. 32.
    Gaynor AM, Nissen MD, Whiley DM, Mackay IM, Lambert SB, Wu G, et al. Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLoS Pathog. 2007;3(5), e64.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Dalianis T, Ramqvist T, Andreasson K, Kean JM, Garcea RL. KI, WU and Merkel cell polyomaviruses: a new era for human polyomavirus research. Semin Cancer Biol. 2009;19(4):270–5.PubMedCrossRefGoogle Scholar
  34. 34.
    Sharp CP, Norja P, Anthony I, Bell JE, Simmonds P. Reactivation and mutation of newly discovered WU, KI, and Merkel cell carcinoma polyomaviruses in immunosuppressed individuals. J Infect Dis. 2009;199(3):398–404.PubMedCrossRefGoogle Scholar
  35. 35.
    Allander T, Andreasson K, Gupta S, Bjerkner A, Bogdanovic G, Persson MA, et al. Identification of a third human polyomavirus. J Virol. 2007;81(8):4130–6.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Foulongne V, Sauvage V, Hebert C, Dereure O, Cheval J, Gouilh MA, et al. Human skin microbiota: high diversity of DNA viruses identified on the human skin by high throughput sequencing. PLoS One. 2012;7(6), e38499.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Ehlers B, Wieland U. The novel human polyomaviruses HPyV6, 7, 9 and beyond. APMIS. 2013;121:783–95.PubMedCrossRefGoogle Scholar
  38. 38.
    Kazem S, van der Meijden E, Feltkamp MC. The trichodysplasia spinulosa-associated polyomavirus; virological background and clinical implications. APMIS. 2013;121:770–82.PubMedCrossRefGoogle Scholar
  39. 39.
    Hirsch HH, Knowles W, Dickenmann M, Passweg J, Klimkait T, Mihatsch MJ, et al. Prospective study of polyomavirus type BK replication and nephropathy in renal-transplant recipients. N Engl J Med. 2002;347(7):488–96.PubMedCrossRefGoogle Scholar
  40. 40.
    Arthur RR, Shah KV, Baust SJ, Santos GW, Saral R. Association of BK viruria with hemorrhagic cystitis in recipients of bone marrow transplants. N Engl J Med. 1986;315(4):230–4.PubMedCrossRefGoogle Scholar
  41. 41.
    Randhawa P, Uhrmacher J, Pasculle W, Vats A, Shapiro R, Eghtsead B, et al. A comparative study of BK and JC virus infections in organ transplant recipients. J Med Virol. 2005;77(2):238–43.PubMedCrossRefGoogle Scholar
  42. 42.
    Hirsch HH, Friman S, Wiecek A, Rostaing L, Pescovitz M. Prospective study of polyomavirus BK viruria and viremia in de novo renal transplantation (Abstract #77). Am J Transplant. 2007;7 Suppl 5:150.Google Scholar
  43. 43.
    Funk GA, Gosert R, Comoli P, Ginevri F, Hirsch HH. Polyomavirus BK replication dynamics in vivo and in silico to predict cytopathology and viral clearance in kidney transplants. Am J Transplant. 2008;8:2368–77.PubMedCrossRefGoogle Scholar
  44. 44.
    Azzi A, Fanci R, Bosi A, Ciappi S, Zakrzewska K, de Santis R, et al. Monitoring of polyomavirus BK viruria in bone marrow transplantation patients by DNA hybridization assay and by polymerase chain reaction: an approach to assess the relationship between BK viruria and hemorrhagic cystitis. Bone Marrow Transplant. 1994;14(2):235–40.PubMedGoogle Scholar
  45. 45.
    Azzi A, Cesaro S, Laszlo D, Zakrzewska K, Ciappi S, De Santis R, et al. Human polyomavirus BK (BKV) load and haemorrhagic cystitis in bone marrow transplantation patients. J Clin Virol. 1999;14(2):79–86.PubMedCrossRefGoogle Scholar
  46. 46.
    Leung AY, Suen CK, Lie AK, Liang RH, Yuen KY, Kwong YL. Quantification of polyoma BK viruria in hemorrhagic cystitis complicating bone marrow transplantation. Blood. 2001;98(6):1971–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Hirsch HH, Vincenti F, Friman S, Tuncer M, Citterio F, Wiecek A, et al. Polyomavirus BK replication in de novo kidney transplant patients receiving tacrolimus or cyclosporine: a prospective, randomized, multicenter study. Am J Transplant. 2013;13(1):136–45.PubMedCrossRefGoogle Scholar
  48. 48.
    Drachenberg CB, Hirsch HH, Papadimitriou JC, Gosert R, Wali RK, Munivenkatappa R, et al. Polyomavirus BK versus JC replication and nephropathy in renal transplant recipients: a prospective evaluation. Transplantation. 2007;84(3):323–30.PubMedCrossRefGoogle Scholar
  49. 49.
    Viscidi RP, Khanna N, Tan CS, Li X, Jacobson L, Clifford DB, et al. JC virus antibody and viremia as predictors of progressive multifocal leukoencephalopathy in human immunodeficiency virus-1-infected individuals. Clin Infect Dis. 2011;53(7):711–5.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Lautenschlager I, Jahnukainen T, Kardas P, Lohi J, Auvinen E, Mannonen L, et al. A case of primary JC polyomavirus infection-associated nephropathy. Am J Transplant. 2014;14(12):2887–92.PubMedCrossRefGoogle Scholar
  51. 51.
    Abedi Kiasari B, Vallely PJ, Corless CE, Al-Hammadi M, Klapper PE. Age-related pattern of KI and WU polyomavirus infection. J Clin Virol. 2008;43(1):123–5.PubMedCrossRefGoogle Scholar
  52. 52.
    Bialasiewicz S, Whiley DM, Lambert SB, Jacob K, Bletchly C, Wang D, et al. Presence of the newly discovered human polyomaviruses KI and WU in Australian patients with acute respiratory tract infection. J Clin Virol. 2008;41(2):63–8.PubMedCrossRefGoogle Scholar
  53. 53.
    Venter M, Visser A, Lassauniere R. Human polyomaviruses, WU and KI in HIV exposed children with acute lower respiratory tract infections in hospitals in South Africa. J Clin Virol. 2009;44(3):230–4.PubMedCrossRefGoogle Scholar
  54. 54.
    Koskenvuo M, Dumoulin A, Lautenschlager I, Auvinen E, Mannonen L, Anttila VJ, et al. BK polyomavirus-associated hemorrhagic cystitis among pediatric allogeneic bone marrow transplant recipients: treatment response and evidence for nosocomial transmission. J Clin Virol. 2013;56(1):77–81.PubMedCrossRefGoogle Scholar
  55. 55.
    Zaia J, Baden L, Boeckh MJ, Chakrabarti S, Einsele H, Ljungman P, et al. Viral disease prevention after hematopoietic cell transplantation. Bone Marrow Transplant. 2009;44(8):471–82.PubMedCrossRefGoogle Scholar
  56. 56.
    Kazory A, Ducloux D, Chalopin JM, Angonin R, Fontaniere B, Moret H. The first case of JC virus allograft nephropathy. Transplantation. 2003;76(11):1653–5.PubMedCrossRefGoogle Scholar
  57. 57.
    Wen MC, Wang CL, Wang M, Cheng CH, Wu MJ, Chen CH, et al. Association of JC virus with tubulointerstitial nephritis in a renal allograft recipient. J Med Virol. 2004;72(4):675–8.PubMedCrossRefGoogle Scholar
  58. 58.
    Hix JK, Braun WE, Isada CM. Delirium in a renal transplant recipient associated with BK virus in the cerebrospinal fluid. Transplantation. 2004;78(9):1407–8.PubMedCrossRefGoogle Scholar
  59. 59.
    Hirsch HH, Brennan DC, Drachenberg CB, Ginevri F, Gordon J, Limaye AP, et al. Polyomavirus-associated nephropathy in renal transplantation: interdisciplinary analyses and recommendations. Transplantation. 2005;79(10):1277–86.PubMedCrossRefGoogle Scholar
  60. 60.
    Hirsch HH, Randhawa P. BK polyomavirus in solid organ transplantation. Am J Transplant. 2013;13 Suppl 4:179–88.PubMedCrossRefGoogle Scholar
  61. 61.
    Nickeleit V, Hirsch HH, Binet IF, Gudat F, Prince O, Dalquen P, et al. Polyomavirus infection of renal allograft recipients: from latent infection to manifest disease. J Am Soc Nephrol. 1999;10(5):1080–9.PubMedGoogle Scholar
  62. 62.
    Purighalla R, Shapiro R, McCauley J, Randhawa P. BK virus infection in a kidney allograft diagnosed by needle biopsy. Am J Kidney Dis. 1995;26(4):671–3.PubMedCrossRefGoogle Scholar
  63. 63.
    Drachenberg CB, Papadimitriou JC, Hirsch HH, Wali R, Crowder C, Nogueira J, et al. Histological patterns of polyomavirus nephropathy: correlation with graft outcome and viral load. Am J Transplant. 2004;4(12):2082–92.PubMedCrossRefGoogle Scholar
  64. 64.
    Leuenberger D, Andresen PA, Gosert R, Binggeli S, Strom EH, Bodaghi S, et al. Human polyomavirus type 1 (BK virus) agnoprotein is abundantly expressed but immunologically ignored. Clin Vaccine Immunol. 2007;14(8):959–68.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Dharnidharka VR, Cherikh WS, Abbott KC. An OPTN analysis of national registry data on treatment of BK virus allograft nephropathy in the United States. Transplantation. 2009;87(7):1019–26.PubMedCrossRefGoogle Scholar
  66. 66.
    Schold JD, Rehman S, Kayler LK, Magliocca J, Srinivas TR, Meier-Kriesche HU. Treatment for BK virus: incidence, risk factors and outcomes for kidney transplant recipients in the United States. Transpl Int. 2009;22(6):626–34.PubMedCrossRefGoogle Scholar
  67. 67.
    Elfadawy N, Flechner SM, Schold JD, Srinivas TR, Poggio E, Fatica R, et al. Transient versus persistent BK viremia and long-term outcomes after kidney and kidney-pancreas transplantation. Clin J Am Soc Nephrol. 2014;9(3):553–61.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Renner FC, Dietrich H, Bulut N, Celik D, Freitag E, Gaertner N, et al. The risk of polyomavirus-associated graft nephropathy is increased by a combined suppression of CD8 and CD4 cell-dependent immune effects. Transplant Proc. 2013;45(4):1608–10.PubMedCrossRefGoogle Scholar
  69. 69.
    Comoli P, Hirsch HH, Ginevri F. Cellular immune responses to BK virus. Curr Opin Organ Transplant. 2008;13(6):569–74.PubMedCrossRefGoogle Scholar
  70. 70.
    Wadei HM, Rule AD, Lewin M, Mahale AS, Khamash HA, Schwab TR, et al. Kidney transplant function and histological clearance of virus following diagnosis of polyomavirus-associated nephropathy (PVAN). Am J Transplant. 2006;6(5 Pt 1):1025–32.PubMedCrossRefGoogle Scholar
  71. 71.
    Drachenberg CB, Papadimitriou JC, Wali R, Nogueira J, Mendley S, Hirsch HH, et al. Improved outcome of polyoma virus allograft nephropathy with early biopsy. Transplant Proc. 2004;36(3):758–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Schaub S, Hirsch HH, Dickenmann M, Steiger J, Mihatsch MJ, Hopfer H, et al. Reducing immunosuppression preserves allograft function in presumptive and definitive polyomavirus-associated nephropathy. Am J Transplant. 2010;10(12):2615–23.PubMedCrossRefGoogle Scholar
  73. 73.
    Sood P, Senanayake S, Sujeet K, Medipalli R, Zhu YR, Johnson CP, et al. Management and outcome of BK viremia in renal transplant recipients: a prospective single-center study. Transplantation. 2012;94(8):814–21.PubMedCrossRefGoogle Scholar
  74. 74.
    Huang G, Wang CX, Zhang L, Fei JG, Deng SX, Qiu J, et al. Monitoring of polyomavirus BK replication and impact of preemptive immunosuppression reduction in renal-transplant recipients in China: a 5-year single-center analysis. Diagn Microbiol Infect Dis. 2015;81(1):21–6.PubMedCrossRefGoogle Scholar
  75. 75.
    Brennan DC, Agha I, Bohl DL, Schnitzler MA, Hardinger KL, Lockwood M, et al. Incidence of BK with tacrolimus versus cyclosporine and impact of preemptive immunosuppression reduction. Am J Transplant. 2005;5(3):582–94.PubMedCrossRefGoogle Scholar
  76. 76.
    Ginevri F, Azzi A, Hirsch HH, Basso S, Fontana I, Cioni M, et al. Prospective monitoring of polyomavirus BK replication and impact of pre-emptive intervention in pediatric kidney recipients. Am J Transplant. 2007;7(12):2727–35.PubMedCrossRefGoogle Scholar
  77. 77.
    Hardinger KL, Koch MJ, Bohl DJ, Storch GA, Brennan DC. BK-virus and the impact of pre-emptive immunosuppression reduction: 5-year results. Am J Transplant. 2010;2010:5.Google Scholar
  78. 78.
    Kiberd BA. Screening to prevent polyoma virus nephropathy: a medical decision analysis. Am J Transplant. 2005;5(10):2410–6.PubMedCrossRefGoogle Scholar
  79. 79.
    Rinaldo CH, Hirsch HH. Antivirals for the treatment of polyomavirus BK replication. Expert Rev Anti Infect Ther. 2007;5(1):105–15.PubMedCrossRefGoogle Scholar
  80. 80.
    Egli A, Kohli S, Dickenmann M, Hirsch HH. Inhibition of polyomavirus BK-specific T-Cell responses by immunosuppressive drugs. Transplantation. 2009;88(10):1161–8.PubMedCrossRefGoogle Scholar
  81. 81.
    Binggeli S, Egli A, Schaub S, Binet I, Mayr M, Steiger J, et al. Polyomavirus BK-specific cellular immune response to VP1 and large T-antigen in kidney transplant recipients. Am J Transplant. 2007;7(5):1131–9.PubMedCrossRefGoogle Scholar
  82. 82.
    Schachtner T, Muller K, Stein M, Diezemann C, Sefrin A, Babel N, et al. BK virus-specific immunity kinetics: a predictor of recovery from polyomavirus BK-associated nephropathy. Am J Transplant. 2011;11(11):2443–52.PubMedCrossRefGoogle Scholar
  83. 83.
    Bernhoff E, Gutteberg TJ, Sandvik K, Hirsch HH, Rinaldo CH. Cidofovir inhibits polyomavirus BK replication in human renal tubular cells downstream of viral early gene expression. Am J Transplant. 2008;8:1413–22.PubMedCrossRefGoogle Scholar
  84. 84.
    Kuypers DR, Vandooren AK, Lerut E, Evenepoel P, Claes K, Snoeck R, et al. Adjuvant low-dose cidofovir therapy for BK polyomavirus interstitial nephritis in renal transplant recipients. Am J Transplant. 2005;5(8):1997–2004.PubMedCrossRefGoogle Scholar
  85. 85.
    Halim MA, Al-Otaibi T, Gheith O, Zkaria Z, Mosaad A, Said T, et al. Active management versus minimization of immunosuppressives of BK virus-associated nephropathy after a kidney transplant. Exp Clin Transplant. 2014;12(6):528–33.PubMedGoogle Scholar
  86. 86.
    Elfadawy N, Flechner SM, Liu X, Schold J, Tian D, Srinivas TR, et al. The impact of surveillance and rapid reduction in immunosuppression to control BK virus-related graft injury in kidney transplantation. Transpl Int. 2013;26(8):822–32.PubMedCrossRefGoogle Scholar
  87. 87.
    Knoll GA, Humar A, Fergusson D, Johnston O, House AA, Kim SJ, et al. Levofloxacin for BK virus prophylaxis following kidney transplantation: a randomized clinical trial. JAMA. 2014;312(20):2106–14.PubMedCrossRefGoogle Scholar
  88. 88.
    Josephson MA, Gillen D, Javaid B, Kadambi P, Meehan S, Foster P, et al. Treatment of renal allograft polyoma BK virus infection with leflunomide. Transplantation. 2006;81(5):704–10.PubMedCrossRefGoogle Scholar
  89. 89.
    Faguer S, Hirsch HH, Kamar N, Guilbeau-Frugier C, Ribes D, Guitard J, et al. Leflunomide treatment for polyomavirus BK-associated nephropathy after kidney transplantation. Transpl Int. 2007;20(11):962–9.PubMedCrossRefGoogle Scholar
  90. 90.
    Ramos E, Drachenberg CB, Wali R, Hirsch HH. The decade of polyomavirus BK-associated nephropathy: state of affairs. Transplantation. 2009;87(5):621–30.PubMedCrossRefGoogle Scholar
  91. 91.
    Tedesco Silva Jr H, Cibrik D, Johnston T, Lackova E, Mange K, Panis C, et al. Everolimus plus reduced-exposure CsA versus mycophenolic acid plus standard-exposure CsA in renal-transplant recipients. Am J Transplant. 2010;10(6):1401–13.PubMedCrossRefGoogle Scholar
  92. 92.
    Wali RK, Drachenberg C, Hirsch HH, Papadimitriou J, Nahar A, Mohanlal V, et al. BK virus-associated nephropathy in renal allograft recipients: rescue therapy by sirolimus-based immunosuppression. Transplantation. 2004;78(7):1069–73.PubMedCrossRefGoogle Scholar
  93. 93.
    Hirsch HH, Yakhontova K, Lu M, Manzetti J. BK Polyomavirus replication in renal tubular epithelial cells is inhibited by sirolimus, but activated by tacrolimus through a pathway involving FKBP-12. Am J Transplant. 2016 Mar;16(3):821–32. doi: 10.1111/ajt.13541. PMID:26639422.
  94. 94.
    Liacini A, Seamone ME, Muruve DA, Tibbles LA. Anti-BK virus mechanisms of sirolimus and leflunomide alone and in combination: toward a new therapy for BK virus infection. Transplantation. 2010;90(12):1450–7.PubMedCrossRefGoogle Scholar
  95. 95.
    Hirsch HH, Ramos E. Retransplantation after polyomavirus-associated nephropathy: just do it? Am J Transplant. 2006;6(1):7–9.PubMedCrossRefGoogle Scholar
  96. 96.
    Dharnidharka VR, Cherikh WS, Neff R, Cheng Y, Abbott KC. Retransplantation after BK virus nephropathy in prior kidney transplant: an OPTN database analysis. Am J Transplant. 2010;10(5):1312–5.PubMedCrossRefGoogle Scholar
  97. 97.
    Verghese PS, Finn LS, Englund JA, Sanders JE, Hingorani SR. BK nephropathy in pediatric hematopoietic stem cell transplant recipients. Pediatr Transplant. 2009;13(7):913–8.PubMedCrossRefGoogle Scholar
  98. 98.
    Barber CE, Hewlett TJ, Geldenhuys L, Kiberd BA, Acott PD, Hatchette TF. BK virus nephropathy in a heart transplant recipient: case report and review of the literature. Transpl Infect Dis. 2006;8(2):113–21.PubMedCrossRefGoogle Scholar
  99. 99.
    Egli A, Helmersen DS, Taub K, Hirsch HH, Johnson A. Renal failure five years after lung transplantation due to polyomavirus BK-associated nephropathy. Am J Transplant. 2010;10(10):2324–30.PubMedCrossRefGoogle Scholar
  100. 100.
    Haririan A, Ramos ER, Drachenberg CB, Weir MR, Klassen DK. Polyomavirus nephropathy in native kidneys of a solitary pancreas transplant recipient. Transplantation. 2002;73(8):1350–3.PubMedCrossRefGoogle Scholar
  101. 101.
    Limaye AP, Smith KD, Cook L, Groom DA, Hunt NC, Jerome KR, et al. Polyomavirus nephropathy in native kidneys of non-renal transplant recipients. Am J Transplant. 2005;5(3):614–20.PubMedGoogle Scholar
  102. 102.
    Razonable RR, Brown RA, Humar A, Covington E, Alecock E, Paya CV. A longitudinal molecular surveillance study of human polyomavirus viremia in heart, kidney, liver, and pancreas transplant patients. J Infect Dis. 2005;192(8):1349–54.PubMedCrossRefGoogle Scholar
  103. 103.
    Munoz P, Fogeda M, Bouza E, Verde E, Palomo J, Banares R. Prevalence of BK virus replication among recipients of solid organ transplants. Clin Infect Dis. 2005;41(12):1720–5.PubMedCrossRefGoogle Scholar
  104. 104.
    Rolla D, Giacomazzi GG, Gentile R, Ravetti JL, Cannella G, Varnier OE. Kidney graft loss associated with JC polyomavirus nephropathy. J Nephrol. 2009;22(2):295–8.PubMedGoogle Scholar
  105. 105.
    Svahn BM, Alvin O, Ringden O, Gardulf A, Remberger M. Costs of allogeneic hematopoietic stem cell transplantation. Transplantation. 2006;82(2):147–53.PubMedCrossRefGoogle Scholar
  106. 106.
    Cesaro S, Facchin C, Tridello G, Messina C, Calore E, Biasolo MA, et al. A prospective study of BK-virus-associated haemorrhagic cystitis in paediatric patients undergoing allogeneic haematopoietic stem cell transplantation. Bone Marrow Transplant. 2008;41(4):363–70.PubMedCrossRefGoogle Scholar
  107. 107.
    Hassan Z, Remberger M, Svenberg P, Elbander M, Omazic B, Mattsson J, et al. Hemorrhagic cystitis: a retrospective single-center survey. Clin Transplant. 2007;21(5):659–67.PubMedCrossRefGoogle Scholar
  108. 108.
    Vogeli TA, Peinemann F, Burdach S, Ackermann R. Urological treatment and clinical course of BK polyomavirus-associated hemorrhagic cystitis in children after bone marrow transplantation. Eur Urol. 1999;36(3):252–7.PubMedCrossRefGoogle Scholar
  109. 109.
    Gorczynska E, Turkiewicz D, Rybka K, Toporski J, Kalwak K, Dyla A, et al. Incidence, clinical outcome, and management of virus-induced hemorrhagic cystitis in children and adolescents after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2005;11(10):797–804.PubMedCrossRefGoogle Scholar
  110. 110.
    Giraud G, Priftakis P, Bogdanovic G, Remberger M, Dubrulle M, Hau A, et al. BK-viruria and haemorrhagic cystitis are more frequent in allogeneic haematopoietic stem cell transplant patients receiving full conditioning and unrelated-HLA-mismatched grafts. Bone Marrow Transplant. 2008;41(8):737–42.PubMedCrossRefGoogle Scholar
  111. 111.
    Seber A, Shu XO, Defor T, Sencer S, Ramsay N. Risk factors for severe hemorrhagic cystitis following BMT. Bone Marrow Transplant. 1999;23(1):35–40.PubMedCrossRefGoogle Scholar
  112. 112.
    Bedi A, Miller CB, Hanson JL, Goodman S, Ambinder RF, Charache P, et al. Association of BK virus with failure of prophylaxis against hemorrhagic cystitis following bone marrow transplantation. J Clin Oncol. 1995;13(5):1103–9.PubMedCrossRefGoogle Scholar
  113. 113.
    Kroger N, Zabelina T, Kruger W, Renges H, Stute N, Kabisch H, et al. Comparison of total body irradiation vs busulfan in combination with cyclophosphamide as conditioning for unrelated stem cell transplantation in CML patients. Bone Marrow Transplant. 2001;27(4):349–54.PubMedCrossRefGoogle Scholar
  114. 114.
    Arthur RR, Shah KV, Charache P, Saral R. BK and JC virus infections in recipients of bone marrow transplants. J Infect Dis. 1988;158(3):563–9.PubMedCrossRefGoogle Scholar
  115. 115.
    Koskenvuo M, Lautenschlager I, Kardas P, Auvinen E, Mannonen L, Huttunen P, et al. Diffuse gastrointestinal bleeding and BK polyomavirus replication in a pediatric allogeneic haematopoietic stem cell transplant patient. J Clin Virol. 2015;62:72–4.PubMedCrossRefGoogle Scholar
  116. 116.
    Schulze M, Beck R, Igney A, Vogel M, Maksimovic O, Claussen CD, et al. Computed tomography findings of human polyomavirus BK (BKV)-associated cystitis in allogeneic hematopoietic stem cell transplant recipients. Acta Radiol. 2008;49(10):1187–94.PubMedCrossRefGoogle Scholar
  117. 117.
    Priftakis P, Bogdanovic G, Kokhaei P, Mellstedt H, Dalianis T. BK virus (BKV) quantification in urine samples of bone marrow transplanted patients is helpful for diagnosis of hemorrhagic cystitis, although wide individual variations exist. J Clin Virol. 2003;26(1):71–7.PubMedCrossRefGoogle Scholar
  118. 118.
    Giraud G, Bogdanovic G, Priftakis P, Remberger M, Svahn BM, Barkholt L, et al. The incidence of hemorrhagic cystitis and BK-viruria in allogeneic hematopoietic stem cell recipients according to intensity of the conditioning regimen. Haematologica. 2006;91(3):401–4.PubMedGoogle Scholar
  119. 119.
    Tanaka K, Hori T, Hatakeyama N, Yamamoto M, Takayama R, Yoto Y, et al. Quantification of BK polyoma viruria in Japanese children and adults with hemorrhagic cystitis complicating stem cell transplantation. J Med Virol. 2008;80(12):2108–12.PubMedCrossRefGoogle Scholar
  120. 120.
    Erard V, Kim HW, Corey L, Limaye A, Huang ML, Myerson D, et al. BK DNA viral load in plasma: evidence for an association with hemorrhagic cystitis in allogeneic hematopoietic cell transplant recipients. Blood. 2005;106(3):1130–2.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Erard V, Storer B, Corey L, Nollkamper J, Huang ML, Limaye A, et al. BK virus infection in hematopoietic stem cell transplant recipients: frequency, risk factors, and association with postengraftment hemorrhagic cystitis. Clin Infect Dis. 2004;39(12):1861–5.PubMedCrossRefGoogle Scholar
  122. 122.
    Wong AS, Chan KH, Cheng VC, Yuen KY, Kwong YL, Leung AY. Relationship of pretransplantation polyoma BK virus serologic findings and BK viral reactivation after hematopoietic stem cell transplantation. Clin Infect Dis. 2007;44(6):830–7.PubMedCrossRefGoogle Scholar
  123. 123.
    Bogdanovic G, Priftakis P, Taemmeraes B, Gustafsson A, Flaegstad T, Winiarski J, et al. Primary BK virus (BKV) infection due to possible BKV transmission during bone marrow transplantation is not the major cause of hemorrhagic cystitis in transplanted children. Pediatr Transplant. 1998;2(4):288–93.PubMedGoogle Scholar
  124. 124.
    Korkmaz A, Topal T, Oter S. Pathophysiological aspects of cyclophosphamide and ifosfamide induced hemorrhagic cystitis; implication of reactive oxygen and nitrogen species as well as PARP activation. Cell Biol Toxicol. 2007;23(5):303–12.PubMedCrossRefGoogle Scholar
  125. 125.
    Lima MV, Ferreira FV, Macedo FY, de Castro Brito GA, Ribeiro RA. Histological changes in bladders of patients submitted to ifosfamide chemotherapy even with mesna prophylaxis. Cancer Chemother Pharmacol. 2007;59(5):643–50.PubMedCrossRefGoogle Scholar
  126. 126.
    Binet I, Nickeleit V, Hirsch HH. Polyomavirus infections in transplant recipients. Curr Opin Organ Transplant. 2000;5:210–6.CrossRefGoogle Scholar
  127. 127.
    Hirsch HH, Steiger J. Polyomavirus BK. Lancet Infect Dis. 2003;3(10):611–23.PubMedCrossRefGoogle Scholar
  128. 128.
    Hirsch HH, Kaufmann G, Sendi P, Battegay M. Immune reconstitution in HIV-infected patients. Clin Infect Dis. 2004;38(8):1159–66.PubMedCrossRefGoogle Scholar
  129. 129.
    Hirsch HH. BK virus: opportunity makes a pathogen. Clin Infect Dis. 2005;41(3):354–60.PubMedCrossRefGoogle Scholar
  130. 130.
    Leung AY, Yuen KY, Kwong YL. Polyoma BK virus and haemorrhagic cystitis in haematopoietic stem cell transplantation: a changing paradigm. Bone Marrow Transplant. 2005;36(11):929–37.PubMedCrossRefGoogle Scholar
  131. 131.
    Cheuk DK, Lee TL, Chiang AK, Ha SY, Lau YL, Chan GC. Risk factors and treatment of hemorrhagic cystitis in children who underwent hematopoietic stem cell transplantation. Transpl Int. 2007;20(1):73–81.PubMedCrossRefGoogle Scholar
  132. 132.
    Dropulic LK, Jones RJ. Polyomavirus BK infection in blood and marrow transplant recipients. Bone Marrow Transplant. 2008;41(1):11–8.PubMedCrossRefGoogle Scholar
  133. 133.
    Savona MR, Newton D, Frame D, Levine JE, Mineishi S, Kaul DR. Low-dose cidofovir treatment of BK virus-associated hemorrhagic cystitis in recipients of hematopoietic stem cell transplant. Bone Marrow Transplant. 2007;39(12):783–7.PubMedCrossRefGoogle Scholar
  134. 134.
    Cesaro S, Hirsch HH, Faraci M, Owoc-Lempach J, Beltrame A, Tendas A, et al. Cidofovir for BK virus-associated hemorrhagic cystitis: a retrospective study. Clin Infect Dis. 2009;49(2):233–40.PubMedCrossRefGoogle Scholar
  135. 135.
    Faraci M, Cuzzubbo D, Lanino E, Di Marco E, Cirillo C, Dallorso S, et al. Low dosage cidofovir without probenecid as treatment for BK virus hamorrhagic cystitis after hemopoietic stem cell transplant. Pediatr Infect Dis J. 2009;28(1):55–7.PubMedCrossRefGoogle Scholar
  136. 136.
    Leung AY, Chan MT, Yuen KY, Cheng VC, Chan KH, Wong CL, et al. Ciprofloxacin decreased polyoma BK virus load in patients who underwent allogeneic hematopoietic stem cell transplantation. Clin Infect Dis. 2005;40(4):528–37.PubMedCrossRefGoogle Scholar
  137. 137.
    Cesaro S, Dalianis T, Rinaldo CH, Koskenvuo M, Einsele H, Hirsch HH. ECIL 6—guidelines for the prevention, diagnosis, and treatment of BK polyomavirus disease in stem cell transplant patients. 2016. Accessed 15 Sept 2015. Available from: https://www.ebmt.org/Contents/Resources/Library/ECIL/Pages/ECIL.aspx (last accessed May 5, 2016)
  138. 138.
    Feder Jr HM, Solomon B, Gavin LD. Polyoma virus hemorrhagic cystitis in an otherwise normal child. Pediatr Infect Dis J. 2008;27(10):948–9.PubMedCrossRefGoogle Scholar
  139. 139.
    Cheerva AC, Raj A, Bertolone SJ, Bertolone K, Silverman CL. BK virus-associated hemorrhagic cystitis in pediatric cancer patients receiving high-dose cyclophosphamide. J Pediatr Hematol Oncol. 2007;29(9):617–21.PubMedCrossRefGoogle Scholar
  140. 140.
    Elidemir O, Chang IF, Schecter MG, Mallory GB. BK virus-associated hemorrhagic cystitis in a pediatric lung transplant recipient. Pediatr Transplant. 2007;11(7):807–10.PubMedCrossRefGoogle Scholar
  141. 141.
    Gluck TA, Knowles WA, Johnson MA, Brook MG, Pillay D. BK virus-associated haemorrhagic cystitis in an HIV-infected man. Aids. 1994;8(3):391–2.PubMedCrossRefGoogle Scholar
  142. 142.
    Barouch DH, Faquin WC, Chen Y, Koralnik IJ, Robbins GK, Davis BT. BK virus-associated hemorrhagic cystitis in a Human Immunodeficiency Virus-infected patient. Clin Infect Dis. 2002;35(3):326–9.PubMedCrossRefGoogle Scholar
  143. 143.
    Christmann M, Heitkamp S, Lambrecht E, Doerries K, Schubert R, Zielen S. Haemorrhagic cystitis and polyomavirus JC infection in ataxia telangiectasia. J Pediatr Urol. 2009;5(4):324–6.PubMedCrossRefGoogle Scholar
  144. 144.
    Astrom KE, Mancall EL, Richardson Jr EP. Progressive multifocal leuko-encephalopathy; a hitherto unrecognized complication of chronic lymphatic leukaemia and Hodgkin's disease. Brain. 1958;81(1):93–111.PubMedCrossRefGoogle Scholar
  145. 145.
    Tan CS, Koralnik IJ. Progressive multifocal leukoencephalopathy and other disorders caused by JC virus: clinical features and pathogenesis. Lancet Neurol. 2010;9(4):425–37.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Ferenczy MW, Marshall LJ, Nelson CD, Atwood WJ, Nath A, Khalili K, et al. Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clin Microbiol Rev. 2012;25(3):471–506.PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Zurhein G, Chou SM. Particles resembling papova viruses in human cerebral demyelinating disease. Science. 1965;148:1477–9.PubMedCrossRefGoogle Scholar
  148. 148.
    Berger JR, Major EO. Progressive multifocal leukoencephalopathy. Semin Neurol. 1999;19(2):193–200.PubMedCrossRefGoogle Scholar
  149. 149.
    Khanna N, Elzi L, Mueller NJ, Garzoni C, Cavassini M, Fux CA, Vernazza P, Bernasconi E, Battegay M, Hirsch HH, for the Swiss HIV Cohort Study. Incidence and outcome of progressive multifocal leukoencephalopathy in 20 years of the Swiss HIV Cohort Study. Clin Infect Dis. 2009;48:1459–66.Google Scholar
  150. 150.
    Shitrit D, Lev N, Bar-Gil-Shitrit A, Kramer MR. Progressive multifocal leukoencephalopathy in transplant recipients. Transpl Int. 2005;17(11):658–65.PubMedCrossRefGoogle Scholar
  151. 151.
    Kharfan-Dabaja MA, Ayala E, Greene J, Rojiani A, Murtagh FR, Anasetti C. Two cases of progressive multifocal leukoencephalopathy after allogeneic hematopoietic cell transplantation and a review of the literature. Bone Marrow Transplant. 2007;39(2):101–7.PubMedCrossRefGoogle Scholar
  152. 152.
    Crowder CD, Gyure KA, Drachenberg CB, Werner J, Morales RE, Hirsch HH, et al. Successful outcome of progressive multifocal leukoencephalopathy in a renal transplant patient. Am J Transplant. 2005;5(5):1151–8.PubMedCrossRefGoogle Scholar
  153. 153.
    Lima MA, Hanto DW, Curry MP, Wong MT, Dang X, Koralnik IJ. Atypical radiological presentation of progressive multifocal leukoencephalopathy following liver transplantation. J Neurovirol. 2005;11(1):46–50.PubMedCrossRefGoogle Scholar
  154. 154.
    Phillips T, Jacobs R, Ellis EN. Polyoma nephropathy and progressive multifocal leukoencephalopathy in a renal transplant recipient. J Child Neurol. 2004;19(4):301–4.PubMedCrossRefGoogle Scholar
  155. 155.
    McCalmont V, Bennett K. Progressive multifocal leukoencephalopathy: a case study. Prog Transplant. 2007;17(2):157–60.PubMedCrossRefGoogle Scholar
  156. 156.
    Ng C, Slavin MA, Seymour JF. Progressive multifocal leukoencephalopathy complicating Waldenstrom’s macroglobulinaemia. Leuk Lymphoma. 2003;44(10):1819–21.PubMedCrossRefGoogle Scholar
  157. 157.
    Osorio S, de la Camara R, Golbano N, Marti E, Fedele CG, Nieto S, et al. Progressive multifocal leukoencephalopathy after stem cell transplantation, unsuccessfully treated with cidofovir. Bone Marrow Transplant. 2002;30(12):963–6.PubMedCrossRefGoogle Scholar
  158. 158.
    Ouwens JP, Haaxma-Reiche H, Verschuuren EA, Timens W, Steenhuis LH, de Boer WJ, et al. Visual symptoms after lung transplantation: a case of progressive multifocal leukoencephalopathy. Transpl Infect Dis. 2000;2(1):29–32.PubMedCrossRefGoogle Scholar
  159. 159.
    Coppo P, Laporte JP, Aoudjhane M, Lebon P, Isnard F, Lesage S, et al. Progressive multifocal leucoencephalopathy with peripheral demyelinating neuropathy after autologous bone marrow transplantation for acute myeloblastic leukemia (FAB5). Bone Marrow Transplant. 1999;23(4):401–3.PubMedCrossRefGoogle Scholar
  160. 160.
    Berner B, Krieter DH, Rumpf KW, Grunewald RW, Beuche W, Weber T, et al. Progressive multifocal leukoencephalopathy in a renal transplant patient diagnosed by JCV-specific DNA amplification and an intrathecal humoral immune response to recombinant virus protein 1. Nephrol Dial Transplant. 1999;14(2):462–5.PubMedCrossRefGoogle Scholar
  161. 161.
    Przepiorka D, Jaeckle KA, Birdwell RR, Fuller GN, Kumar AJ, Huh YO, et al. Successful treatment of progressive multifocal leukoencephalopathy with low-dose interleukin-2. Bone Marrow Transplant. 1997;20(11):983–7.PubMedCrossRefGoogle Scholar
  162. 162.
    Berger JR, Aksamit AJ, Clifford DB, Davis L, Koralnik IJ, Sejvar JJ, et al. PML diagnostic criteria: consensus statement from the AAN Neuroinfectious Disease Section. Neurology. 2013;80(15):1430–8.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Van Assche G, Van Ranst M, Sciot R, Dubois B, Vermeire S, Noman M, et al. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn’s disease. N Engl J Med. 2005;353(4):362–8.PubMedCrossRefGoogle Scholar
  164. 164.
    Hirsch HH, Meylan PR, Zimmerli W, Iten A, Battegay M, Erb P. HIV-1-infected patients with focal neurologic signs: diagnostic role of PCR for Toxoplasma gondii, Epstein-Barr virus, and JC virus. Clin Microbiol Infect. 1998;4(10):577–84.PubMedCrossRefGoogle Scholar
  165. 165.
    Jelcic I, Jelcic I, Faigle W, Sospedra M, Martin R. Immunology of progressive multifocal leukoencephalopathy. J Neurovirol. 2015;21:614.PubMedCrossRefGoogle Scholar
  166. 166.
    Berger JR. Progressive multifocal leukoencephalopathy. Handb Clin Neurol. 2014;123:357–76.PubMedCrossRefGoogle Scholar
  167. 167.
    Carson KR, Evens AM, Richey EA, Habermann TM, Focosi D, Seymour JF, et al. Progressive multifocal leukoencephalopathy after rituximab therapy in HIV-negative patients: a report of 57 cases from the Research on Adverse Drug Events and Reports project. Blood. 2009;113(20):4834–40.PubMedPubMedCentralCrossRefGoogle Scholar
  168. 168.
    Major EO, Frohman E, Douek D. JC viremia in natalizumab-treated patients with multiple sclerosis. N Engl J Med. 2013;368(23):2240–1.PubMedPubMedCentralCrossRefGoogle Scholar
  169. 169.
    Hall CD, Dafni U, Simpson D, Clifford D, Wetherill PE, Cohen B, et al. Failure of cytarabine in progressive multifocal leukoencephalopathy associated with human immunodeficiency virus infection. AIDS Clinical Trials Group 243 Team. N Engl J Med. 1998;338(19):1345–51.PubMedCrossRefGoogle Scholar
  170. 170.
    De Luca A, Ammassari A, Pezzotti P, Cinque P, Gasnault J, Berenguer J, et al. Cidofovir in addition to antiretroviral treatment is not effective for AIDS-associated progressive multifocal leukoencephalopathy: a multicohort analysis. Aids. 2008;22(14):1759–67.PubMedCrossRefGoogle Scholar
  171. 171.
    Clifford DB, Nath A, Cinque P, Brew BJ, Zivadinov R, Gorelik L, et al. A study of mefloquine treatment for progressive multifocal leukoencephalopathy: results and exploration of predictors of PML outcomes. J Neurovirol. 2013;19(4):351–8.PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    Dugan AS, Eash S, Atwood WJ. Update on BK virus entry and intracellular trafficking. Transpl Infect Dis. 2006;8(2):62–7.PubMedCrossRefGoogle Scholar
  173. 173.
    Alstadhaug K, Croughs T, Henriksen S, Leboeuf C, Sereti I, Hirsch H, et al. Treatment of progressive multifocal leukoencephalopathy with Interleukin 7. JAMA Neurology; 2014 June 30, 2014.Google Scholar
  174. 174.
    Sospedra M, Schippling S, Yousef S, Jelcic I, Bofill-Mas S, Planas R, et al. Treating progressive multifocal leukoencephalopathy with interleukin 7 and vaccination with JC virus capsid protein VP1. Clin Infect Dis. 2014;59(11):1588–92.PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Mourez T, Bergeron A, Ribaud P, Scieux C, de Latour RP, Tazi A, et al. Polyomaviruses KI and WU in immunocompromised patients with respiratory disease. Emerg Infect Dis. 2009;15(1):107–9.PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    Kuypers J, Campbell AP, Guthrie KA, Wright NL, Englund JA, Corey L, et al. WU and KI polyomaviruses in respiratory samples from allogeneic hematopoietic cell transplant recipients. Emerg Infect Dis. 2012;18(10):1580–8.PubMedPubMedCentralCrossRefGoogle Scholar
  177. 177.
    Babakir-Mina M, Ciccozzi M, Alteri C, Polchi P, Picardi A, Greco F, et al. Excretion of the novel polyomaviruses KI and WU in the stool of patients with hematological disorders. J Med Virol. 2009;81(9):1668–73.PubMedCrossRefGoogle Scholar
  178. 178.
    Siebrasse EA, Nguyen NL, Smith C, Simmonds P, Wang D. Immunohistochemical detection of KI polyomavirus in lung and spleen. Virology. 2014;468–470:178–84.PubMedCrossRefGoogle Scholar
  179. 179.
    Siebrasse EA, Pastrana DV, Nguyen NL, Wang A, Roth MJ, Holland SM, et al. WU polyomavirus in respiratory epithelial cells from lung transplant patient with Job syndrome. Emerg Infect Dis. 2015;21(1):103–6.PubMedPubMedCentralCrossRefGoogle Scholar
  180. 180.
    Hodgson NC. Merkel cell carcinoma: changing incidence trends. J Surg Oncol. 2005;89(1):1–4.PubMedCrossRefGoogle Scholar
  181. 181.
    Koljonen V, Kukko H, Tukiainen E, Bohling T, Sankila R, Pukkala E, et al. Incidence of Merkel cell carcinoma in renal transplant recipients. Nephrol Dial Transplant. 2009;8:8.Google Scholar
  182. 182.
    Coursaget P, Mahtab S, Nicol JTJ, Gardair C, Touzé A. Human Merkel cell polyomavirus: virological background and clinical implications. APMIS. 2013;121:755–69.PubMedCrossRefGoogle Scholar
  183. 183.
    Bhatia S, Afanasiev O, Nghiem P. Immunobiology of Merkel cell carcinoma: implications for immunotherapy of a polyomavirus-associated cancer. Curr Oncol Rep. 2011;13(6):488–97.PubMedPubMedCentralCrossRefGoogle Scholar
  184. 184.
    Wendzicki JA, Moore PS, Chang Y. Large T and small T antigens of Merkel cell polyomavirus. Curr Opin Virol. 2015;11:38–43.PubMedPubMedCentralCrossRefGoogle Scholar
  185. 185.
    Ridd K, Yu S, Bastian BC. The presence of polyomavirus in non-melanoma skin cancer in organ transplant recipients is rare. J Invest Dermatol. 2009;129(1):250–2.PubMedCrossRefGoogle Scholar
  186. 186.
    Becker JC, Houben R, Ugurel S, Trefzer U, Pfohler C, Schrama D. MC polyomavirus is frequently present in Merkel cell carcinoma of European patients. J Invest Dermatol. 2009;129(1):248–50.PubMedCrossRefGoogle Scholar
  187. 187.
    Bluemn EG, Paulson KG, Higgins EE, Sun Y, Nghiem P, Nelson PS. Merkel cell polyomavirus is not detected in prostate cancers, surrounding stroma, or benign prostate controls. J Clin Virol. 2009;5:5.Google Scholar
  188. 188.
    Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science. 2008;319(5866):1096–100.PubMedPubMedCentralCrossRefGoogle Scholar
  189. 189.
    Peretti A, Borgogna C, Rossi D, De Paoli L, Bawadekar M, Zavattaro E, et al. Analysis of human beta-papillomavirus and Merkel cell polyomavirus infection in skin lesions and eyebrow hair bulbs from a cohort of patients with chronic lymphocytic leukaemia. Br J Dermatol. 2014;171(6):1525–8.PubMedCrossRefGoogle Scholar
  190. 190.
    Rajpoot DK, Gomez A, Tsang W, Shanberg A. Ureteric and urethral stenosis: a complication of BK virus infection in a pediatric renal transplant patient. Pediatr Transplant. 2007;11(4):433–5.PubMedCrossRefGoogle Scholar
  191. 191.
    Coleman DV, Mackenzie EF, Gardner SD, Poulding JM, Amer B, Russell WJ. Human polyomavirus (BK) infection and ureteric stenosis in renal allograft recipients. J Clin Pathol. 1978;31(4):338–47.PubMedPubMedCentralCrossRefGoogle Scholar
  192. 192.
    Sandler ES, Aquino VM, Goss-Shohet E, Hinrichs S, Krisher K. BK papova virus pneumonia following hematopoietic stem cell transplantation. Bone Marrow Transplant. 1997;20(2):163–5.PubMedCrossRefGoogle Scholar
  193. 193.
    Jorgensen GE, Hammarin AL, Bratt G, Grandien M, Flaegstad T, Johnsen JI. Identification of a unique BK virus variant in the CNS of a patient with AIDS. J Med Virol. 2003;70(1):14–9.PubMedCrossRefGoogle Scholar
  194. 194.
    Behzad-Behbahani A, Klapper PE, Vallely PJ, Cleator GM, Bonington A. BKV-DNA and JCV-DNA in CSF of patients with suspected meningitis or encephalitis. Infection. 2003;31(6):374–8.PubMedGoogle Scholar
  195. 195.
    Schuetz C, Hoenig M, Gatz S, Speth F, Benninghoff U, Schulz A, et al. Hematopoietic stem cell transplantation from matched unrelated donors in chronic granulomatous disease. Immunol Res. 2009;44(1–3):35–41.PubMedCrossRefGoogle Scholar
  196. 196.
    Hedquist BG, Bratt G, Hammarin AL, Grandien M, Nennesmo I, Sundelin B, et al. Identification of BK virus in a patient with acquired immune deficiency syndrome and bilateral atypical retinitis. Ophthalmology. 1999;106(1):129–32.PubMedCrossRefGoogle Scholar
  197. 197.
    Bratt G, Hammarin AL, Grandien M, Hedquist BG, Nennesmo I, Sundelin B, et al. BK virus as the cause of meningoencephalitis, retinitis and nephritis in a patient with AIDS. Aids. 1999;13(9):1071–5.PubMedCrossRefGoogle Scholar
  198. 198.
    Friedman DP, Flanders AE. MR imaging of BK virus encephalitis. AJNR Am J Neuroradiol. 2006;27(5):1016–8.PubMedGoogle Scholar
  199. 199.
    Barzon L, Squarzon L, Pacenti M, Scotton PG, Palu G. Detection of WU polyomavirus in cerebrospinal fluid specimen from a patient with AIDS and suspected progressive multifocal leukoencephalopathy. J Infect Dis. 2009;200(2):314–5.PubMedCrossRefGoogle Scholar
  200. 200.
    Dalianis T, Hirsch HH. Human polyomaviruses in disease and cancer. Virology. 2013;437(2):63–72.PubMedCrossRefGoogle Scholar
  201. 201.
    Dalianis T, Hirsch HH. Chapter 16: BK polyomavirus and transformation. In: Robertson ES, Medicine PSo, University of Pennsylvania, PA, USA, erle@upenn.edu, editors. Cancer associated viruses. New York: Springer; 2012. p. 419–32.Google Scholar
  202. 202.
    Emerson LL, Carney HM, Layfield LJ, Sherbotie JR. Collecting duct carcinoma arising in association with BK nephropathy post-transplantation in a pediatric patient. A case report with immunohistochemical and in situ hybridization study. Pediatr Transplant. 2008;12(5):600–5.PubMedCrossRefGoogle Scholar
  203. 203.
    Geetha D, Tong BC, Racusen L, Markowitz JS, Westra WH. Bladder carcinoma in a transplant recipient: evidence to implicate the BK human polyomavirus as a causal transforming agent. Transplantation. 2002;73(12):1933–6.PubMedCrossRefGoogle Scholar
  204. 204.
    Wang HH, Liu KL, Chu SH, Tian YC, Lai PC, Chiang YJ. BK virus infection in association with posttransplant urothelial carcinoma. Transplant Proc. 2009;41(1):165–6.PubMedCrossRefGoogle Scholar
  205. 205.
    Narayanan M, Szymanski J, Slavcheva E, Rao A, Kelly A, Jones K, et al. BK virus associated renal cell carcinoma: case presentation with optimized PCR and other diagnostic tests. Am J Transplant. 2007;7(6):1666–71.PubMedCrossRefGoogle Scholar
  206. 206.
    Selgrad M, De Giorgio R, Fini L, Cogliandro RF, Williams S, Stanghellini V, et al. JC virus infects the enteric glia of patients with chronic idiopathic intestinal pseudo-obstruction. Gut. 2009;58(1):25–32.PubMedCrossRefGoogle Scholar
  207. 207.
    Mishra N, Pereira M, Rhodes RH, An P, Pipas JM, Jain K, et al. Identification of a novel polyomavirus in a pancreatic transplant recipient with retinal blindness and vasculitic myopathy. J Infect Dis. 2014;210(10):1595–9.PubMedPubMedCentralCrossRefGoogle Scholar
  208. 208.
    Ho J, Jedrych JJ, Feng H, Natalie AA, Grandinetti L, Mirvish E, et al. Human polyomavirus 7-associated pruritic rash and viremia in transplant recipients. J Infect Dis. 2014;17:1–6.Google Scholar
  209. 209.
    Saha A, Kaul R, Murakami M, Robertson ES. Tumor viruses and cancer biology: modulating signaling pathways for therapeutic intervention. Cancer Biol Ther. 2010;10(10):961–78.PubMedCrossRefGoogle Scholar
  210. 210.
    Nindl I, Rosl F. Molecular concepts of virus infections causing skin cancer in organ transplant recipients. Am J Transplant. 2008;8(11):2199–204.PubMedCrossRefGoogle Scholar
  211. 211.
    Markowitz LE, Sternberg M, Dunne EF, McQuillan G, Unger ER. Seroprevalence of human papillomavirus types 6, 11, 16, and 18 in the United States: National Health and Nutrition Examination Survey 2003–2004. J Infect Dis. 2009;31:31.Google Scholar
  212. 212.
    Antonsson A, Pawlita M, Feltkamp MC, Bouwes Bavinck JN, Euvrard S, Harwood CA, et al. Longitudinal study of seroprevalence and serostability of the human polyomaviruses JCV and BKV in organ transplant recipients. J Med Virol. 2013;85(2):327–35.PubMedCrossRefGoogle Scholar
  213. 213.
    Antonsson A, Green AC, Mallitt KA, O'Rourke PK, Pawlita M, Waterboer T, et al. Prevalence and stability of antibodies to the BK and JC polyomaviruses: a long-term longitudinal study of Australians. J Gen Virol. 2010;91(Pt 7):1849–53.PubMedCrossRefGoogle Scholar
  214. 214.
    Dunne EF, Nielson CM, Stone KM, Markowitz LE, Giuliano AR. Prevalence of HPV infection among men: a systematic review of the literature. J Infect Dis. 2006;194(8):1044–57.PubMedCrossRefGoogle Scholar
  215. 215.
    Partridge JM, Hughes JP, Feng Q, Winer RL, Weaver BA, Xi LF, et al. Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students. J Infect Dis. 2007;196(8):1128–36.PubMedCrossRefGoogle Scholar
  216. 216.
    Chin-Hong PV, Kwak EJ. Human papillomavirus in solid organ transplantation. Am J Transplant. 2013;13 Suppl 4:189–200.PubMedCrossRefGoogle Scholar
  217. 217.
    Wheless L, Jacks S, Mooneyham Potter KA, Leach BC, Cook J. Skin cancer in organ transplant recipients: more than the immune system. J Am Acad Dermatol. 2014;71(2):359–65.PubMedPubMedCentralCrossRefGoogle Scholar
  218. 218.
    Genders RE, Mazlom H, Michel A, Plasmeijer EI, Quint KD, Pawlita M, et al. The presence of betapapillomavirus antibodies around transplantation predicts the development of keratinocyte carcinoma in organ transplant recipients: a cohort study. J Invest Dermatol. 2015;135(5):1275–82.PubMedCrossRefGoogle Scholar
  219. 219.
    Skov Dalgaard L, Fassel U, Ostergaard LJ, Jespersen B, Schmeltz Sogaard O, Jensen-Fangel S. Risk of human papillomavirus-related cancers among kidney transplant recipients and patients receiving chronic dialysis—an observational cohort study. BMC Nephrol. 2013;14:137.PubMedPubMedCentralCrossRefGoogle Scholar
  220. 220.
    Dreno B, Mansat E, Legoux B, Litoux P. Skin cancers in transplant patients. Nephrol Dial Transplant. 1998;13(6):1374–9.PubMedCrossRefGoogle Scholar
  221. 221.
    Dubina M, Goldenberg G. Viral-associated nonmelanoma skin cancers: a review. Am J Dermatopathol. 2009;31(6):561–73.PubMedCrossRefGoogle Scholar
  222. 222.
    Kahn JA. HPV vaccination for the prevention of cervical intraepithelial neoplasia. N Engl J Med. 2009;361(3):271–8.PubMedCrossRefGoogle Scholar
  223. 223.
    Ho WL, Murphy GM. Update on the pathogenesis of post-transplant skin cancer in renal transplant recipients. Br J Dermatol. 2008;158(2):217–24.PubMedCrossRefGoogle Scholar
  224. 224.
    Borgogna C, Lanfredini S, Peretti A, De Andrea M, Zavattaro E, Colombo E, et al. Improved detection reveals active beta-papillomavirus infection in skin lesions from kidney transplant recipients. Mod Pathol. 2014;27(8):1101–15.PubMedCrossRefGoogle Scholar
  225. 225.
    Bonatti H, Brandacher G, Margreiter R, Schneeberger S. Infectious complications in three double hand recipients: experience from a single center. Transplant Proc. 2009;41(2):517–20.PubMedCrossRefGoogle Scholar
  226. 226.
    Maruyama F, Miyazaki H, Matsui T, Okamoto M, Matsunaga K, Ezaki K, et al. Rapid progression of flat warts in a patient with malignant lymphoma after PBSCT. Bone Marrow Transplant. 1996;18(5):1009–11.PubMedGoogle Scholar
  227. 227.
    Ganguly N, Waller S, Stasik CJ, Skikne BS, Ganguly S. Giant anal condylomatosis after allogeneic bone marrow transplantation: a rare complication of human papilloma virus infection. Transpl Infect Dis. 2008;10(1):56–8.PubMedCrossRefGoogle Scholar
  228. 228.
    Bordea C, Wojnarowska F, Millard PR, Doll H, Welsh K, Morris PJ. Skin cancers in renal-transplant recipients occur more frequently than previously recognized in a temperate climate. Transplantation. 2004;77(4):574–9.PubMedCrossRefGoogle Scholar
  229. 229.
    Vajdic CM, McDonald SP, McCredie MR, van Leeuwen MT, Stewart JH, Law M, et al. Cancer incidence before and after kidney transplantation. JAMA. 2006;296(23):2823–31.PubMedCrossRefGoogle Scholar
  230. 230.
    Madeleine MM, Finch JL, Lynch CF, Goodman MT, Engels EA. HPV-related cancers after solid organ transplantation in the United States. Am J Transplant. 2013;13(12):3202–9.PubMedPubMedCentralCrossRefGoogle Scholar
  231. 231.
    Wang Y, Brinch L, Jebsen P, Tanbo T, Kirschner R. A clinical study of cervical dysplasia in long-term survivors of allogeneic stem cell transplantation. Biol Blood Marrow Transplant. 2012;18(5):747–53.PubMedCrossRefGoogle Scholar
  232. 232.
    Shanis D, Merideth M, Pulanic TK, Savani BN, Battiwalla M, Stratton P. Female long-term survivors after allogeneic hematopoietic stem cell transplantation: evaluation and management. Semin Hematol. 2012;49(1):83–93.PubMedPubMedCentralCrossRefGoogle Scholar
  233. 233.
    Hilgendorf I, Freund M, Jilg W, Einsele H, Gea-Banacloche J, Greinix H, et al. Vaccination of allogeneic haematopoietic stem cell transplant recipients: report from the international consensus conference on clinical practice in chronic GVHD. Vaccine. 2011;29(16):2825–33.PubMedCrossRefGoogle Scholar
  234. 234.
    Kumar D, Unger ER, Panicker G, Medvedev P, Wilson L, Humar A. Immunogenicity of quadrivalent human papillomavirus vaccine in organ transplant recipients. Am J Transplant. 2013;13(9):2411–7.PubMedPubMedCentralCrossRefGoogle Scholar
  235. 235.
    Wong G, Howard K, Webster A, Chapman JR, Craig JC. The health and economic impact of cervical cancer screening and human papillomavirus vaccination in kidney transplant recipients. Transplantation. 2009;87(7):1078–91.PubMedCrossRefGoogle Scholar
  236. 236.
    Sasadeusz J, Kelly H, Szer J, Schwarer AP, Mitchell H, Grigg A. Abnormal cervical cytology in bone marrow transplant recipients. Bone Marrow Transplant. 2001;28(4):393–7.PubMedCrossRefGoogle Scholar
  237. 237.
    Savani BN, Stratton P, Shenoy A, Kozanas E, Goodman S, Barrett AJ. Increased risk of cervical dysplasia in long-term survivors of allogeneic stem cell transplantation—implications for screening and HPV vaccination. Biol Blood Marrow Transplant. 2008;14(9):1072–5.PubMedPubMedCentralCrossRefGoogle Scholar
  238. 238.
    Kruse AL, Gratz KW. Oral carcinoma after hematopoietic stem cell transplantation—a new classification based on a literature review over 30 years. Head Neck Oncol. 2009;1(1):29.PubMedPubMedCentralCrossRefGoogle Scholar
  239. 239.
    Demarosi F, Lodi G, Carrassi A, Moneghini L, Sarina B, Sardella A. Clinical and histopathological features of the oral mucosa in allogeneic haematopoietic stem cell transplantation patients. Exp Oncol. 2007;29(4):304–8.PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Biomedicine (Transplantation & Clinical Virology) or Clinic for Infectious Diseases & Hospital EpidemiologyUniversity Hospital BaselBaselSwitzerland

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