Molecular monitoring of viral infections after hematopoietic stem cell transplantation

International Journal of Hematology

Volumn 91, Issue 4, 2010, Pages 596-601

  Ljungman, Per ^a,b  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Adenovirus; EBV; HHV 6; PCR monitoring; Stem cell transplantation

Indexed keywords

CIDOFOVIR; GANCICLOVIR; RIBAVIRIN; RITUXIMAB;

ADENOVIRUS; ADENOVIRUS INFECTION; ANTIVIRAL THERAPY; BLOOD ANALYSIS; CLINICAL FEATURE; CYTOMEGALOVIRUS INFECTION; DIAGNOSTIC PROCEDURE; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN HERPESVIRUS 6; MONITORING; NONHUMAN; POLYMERASE CHAIN REACTION; REVIEW; VIROLOGY; VIRUS INFECTION; VIRUS LOAD;

DNA, VIRAL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; POLYMERASE CHAIN REACTION; VIRAL LOAD; VIRUS DISEASES;

EID: 77954540393     PISSN: 09255710     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12185-010-0570-4     Document Type: Review

References (61)

1. Styczynski J, Einsele H, Gil L, Ljungman P. Outcome of treatment of Epstein-Barr virus-related post-transplant lymphoproliferative disorDer in hematopoietic stem cell recipients: a comprehensive review of reported cases. Transpl Infect Dis. 2009;11(5):383-392
2. Gartner BC, Schafer H, Marggraff K, Eisele G, Schafer M, Roemer K, et al. Evaluation of use of Epstein-Barr viral load in patients after allogeneic stem cell transplantation to diagnose and monitor posttransplant lymphoproliferative disease. J Clin Microbiol. 2002;40(2):351-358
3. Van Esser JW, Van Der Holt B, Meijer E, Niesters HG, Trenschel R, Thijsen SF, et al. Epstein-Barr virus (EBV) reactivation is a frequent event after allogeneic stem cell transplantation (SCT) and quantitatively predicts EBV-lymphoproliferative disease following T-cell-depleted SCT. Blood. 2001;98(4):972-978
4. Juvonen E, Aalto SM, Tarkkanen J, Volin L, Mattila PS, Knuutila S, et al. High incidence of PTLD after non-T-cell-depleted allogeneic haematopoietic stem cell transplantation as a consequence of intensive immunosuppressive treatment. Bone Marrow Transpl. 2003;32(1):97-102.
5. Kinch A, Oberg G, Arvidson J, Falk KI, Linde A, Pauksens K. Post-transplant lymphoproliferative disease and other Epstein- Barr virus diseases in allogeneic haematopoietic stem cell transplantation after introduction of monitoring of viral load by polymerase chain reaction. Scand J Infect Dis. 2007;39(3):235-244
6. Omar H, Hagglund H, Gustafsson-Jernberg A, LeBlanc K, Mattsson J, Remberger M, et al. Targeted monitoring of patients at high risk of post-transplant lymphoproliferative disease by quantitative Epstein-Barr virus polymerase chain reaction. Transpl Infect Dis. 2009;11(5):393-399
7. Limaye AP, Huang ML, Atienza EE, Ferrenberg JM, Corey L. Detection of Epstein-Barr virus DNA in sera from transplant recipients with lymphoproliferative disorDers. J Clin Microbiol. 1999;37(4):1113-1116
8. Rowe DT, Webber S, Schauer EM, Reyes J, Green M. Epstein- Barr virus load monitoring: its role in the prevention and management of post-transplant lymphoproliferative disease. Transpl Infect Dis. 2001;3(2):79-87.
9. Weinstock DM, Ambrossi GG, Brennan C, Kiehn TE, Jakubowski A. Preemptive diagnosis and treatment of Epstein-Barr virus-associated post transplant lymphoproliferative disorDer after hematopoietic stem cell transplant: an approach in development. Bone Marrow Transpl. 2006;37(6):539-546
10. Sundin M, Le Blanc K, Ringden O, Barkholt L, Omazic B, Lergin C, et al. The role of HLA mismatch, splenectomy and recipient Epstein-Barr virus seronegativity as risk factors in post-transplant lymphoproliferative disorDer following allogeneic hematopoietic stem cell transplantation. Haematologica. 2006;91(8):1059-1067
11. Landgren O, Gilbert ES, Rizzo JD, Socie G, Banks PM, Sobocinski KA, et al. Risk factors for lymphoproliferative disorDers after allogeneic hematopoietic cell transplantation. Blood. 2009;113(20):4992-5001.
12. Brunstein CG, Weisdorf DJ, DeFor T, Barker JN, Tolar J, Van Burik JA, et al. Marked increased risk of Epstein-Barr virusrelated complications with the addition of antithymocyte globulin to a nonmyeloablative conditioning prior to unrelated umbilical cord blood transplantation. Blood. 2006;108(8):2874-2880
13. Styczynski J, Reusser P, Einsele H, de la Camara R, Cordonnier C, Ward KN, et al. Management of HSV, VZV and EBV infections in patients with hematological malignancies and after SCT: guidelines from the second European conference on infections in leukemia. Bone Marrow Transpl. 2009;43(10):757-770
14. Zaia J, Baden L, Boeckh MJ, Chakrabarti S, Einsele H, Ljungman P, et al. Viral disease prevention after hematopoietic cell transplantation. Bone Marrow Transpl. 2009;44(8):471-482
15. Curtis RE, Travis LB, Rowlings PA, Socie G, Kingma DW, Banks PM, et al. Risk of lymphoproliferative disorDers after bone marrow transplantation: a multi-institutional study. Blood. 1999;94(7):2208-2216 (Pubitemid 29467666)
16. Gustafsson A, Levitsky V, Zou JZ, Frisan T, Dalianis T, Ljungman P, et al. Epstein-Barr virus (EBV) load in bone marrow transplant recipients at risk to develop posttransplant lymphoproliferative disease: prophylactic infusion of EBV-specific cytotoxic T cells. Blood. 2000;95(3):807-814
17. Rooney CM, Smith CA, Ng CY, Loftin SK, Sixbey JW, Gan Y, et al. Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood. 1998;92(5):1549-1555
18. Haque T, Wilkie GM, Jones MM, Higgins CD, Urquhart G, Wingate P, et al. Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood. 2007;110(4):1123-1131
19. Wang FZ, Linde A, Hagglund H, Testa M, Locasciulli A, Ljungman P. Human herpesvirus 6 DNA in cerebrospinal fluid specimens from allogeneic bone marrow transplant patients: does it have clinical significance? Clin Infect Dis. 1999;28(3):562-568
20. Zerr DM, Gooley TA, Yeung L, Huang ML, Carpenter P, Wade JC, et al. Human herpesvirus 6 reactivation and encephalitis in allogeneic bone marrow transplant recipients. Clin Infect Dis. 2001;33(6):763-771
21. SeeleyWW,Marty FM,HolmesTM,Upchurch K, Soiffer RJ, Antin JH, et al. Post-transplant acute limbic encephalitis: clinical features and relationship to HHV6. Neurology. 2007;69(2):156-165
22. Chamberlain MC, Chowdhary S. Post-transplant acute limbic encephalitis: clinical features and relationship to HHV6. Neurology. 2008;70(6):491-492 (author reply 2-3).
23. Carrigan DR, Knox KK. Human herpesvirus 6 (HHV-6) isolation from bone marrow: HHV-6-associated bone marrow suppression in bone marrow transplant patients. Blood. 1994;84(10):3307-3310
24. Knox KK, Carrigan DR. In vitro suppression of bone marrow progenitor cell differentiation by human herpesvirus 6 infection. J Infect Dis. 1992;165(5):925-929
25. Isomura H, Yamada M, Yoshida M, Tanaka H, Kitamura T, Oda M, et al. Suppressive effects of human herpesvirus 6 on in vitro colony formation of hematopoietic progenitor cells. J Med Virol. 1997;52(4):406-412
26. Ljungman P, Wang FZ, Clark DA, Emery VC, Remberger M, Ringden O, et al. High levels of human herpesvirus 6 DNA in peripheral blood leucocytes are correlated to platelet engraftment and disease in allogeneic stem cell transplant patients. Br J Haematol. 2000;111(3):774-781
27. Yoshikawa T, Ihira M, Ohashi M, Suga S, Asano Y, Miyazaki H, et al. Correlation between HHV-6 infection and skin rash after allogeneic bone marrow transplantation. Bone Marrow Transpl. 2001;28(1):77-81.
28. Yoshikawa T, Suga S, Asano Y, Nakashima T, Yazaki T, Sobue R, et al. Human herpesvirus-6 infection in bone marrow transplantation. Blood. 1991;78(5):1381-1384
29. Luppi M, Barozzi P, Marasca R, Torelli G. Integration of human herpesvirus-6 (HHV-6) genome in chromosome 17 in two lymphoma patients. Leukemia. 1994;8(Suppl 1):S41-5.
30. Clark DA, Nacheva EP, Leong HN, Brazma D, Li YT, Tsao EH, et al. Transmission of integrated human herpesvirus 6 through stem cell transplantation: implications for laboratory diagnosis. J Infect Dis. 2006;193(7):912-916
31. Ward KN, Leong HN, Nacheva EP, Howard J, Atkinson CE, Davies NW, et al. Human herpesvirus 6 chromosomal integration in immunocompetent patients results in high levels of viral DNA in blood, sera, and hair follicles. J Clin Microbiol. 2006; 44(4):1571-1574
32. Ward KN, Leong HN, Thiruchelvam AD, Atkinson CE, Clark DA. Human herpesvirus 6 DNA levels in cerebrospinal fluid due to primary infection differ from those due to chromosomal viral integration and have implications for diagnosis of encephalitis. J Clin Microbiol. 2007;45(4):1298-1304
33. Mori T, Tanaka-Taya K, Satoh H, Aisa Y, Yamazaki R, Kato J, et al. Transmission of chromosomally integrated human herpesvirsus 6 (HHV-6) variant A from a parent to children leading to misdiagnosis of active HHV-6 infection. Transpl Infect Dis. 2009;11(6):503-506
34. Hubacek P, Virgili A, Ward KN, Pohlreich D, Keslova P, Goldova B, et al. HHV-6 DNA throughout the tissues of two stem cell transplant patients with chromosomally integrated HHV-6 and fatal CMV pneumonitis. Br J Haematol. 2009;145(3):394-398
35. Imbert-Marcille BM, Tang XW, Lepelletier D, Besse B, Moreau P, Billaudel S, et al. Human herpesvirus 6 infection after autologous or allogeneic stem cell transplantation: a single-center prospective longitudinal study of 92 patients. Clin Infect Dis. 2000;31(4):881-886
36. Yoshikawa T, Asano Y, Ihira M, Suzuki K, Ohashi M, Suga S, et al. Human herpesvirus 6 viremia in bone marrow transplant recipients: clinical features and risk factors. J Infect Dis. 2002;185(7):847-853
37. Zerr DM, Corey L, Kim HW, Huang ML, Nguy L, Boeckh M. Clinical outcomes of human herpesvirus 6 reactivation after hematopoietic stem cell transplantation. Clin Infect Dis. 2005;40(7):932-940
38. Sashihara J, Tanaka-Taya K, Tanaka S, Amo K, Miyagawa H, Hosoi G, et al. High incidence of human herpesvirus 6 infection with a high viral load in cord blood stem cell transplant recipients. Blood. 2002;100(6):2005-2011
39. Maeda Y, Teshima T, Yamada M, Harada M. Reactivation of human herpesviruses after allogeneic peripheral blood stem cell transplantation and bone marrow transplantation. Leuk Lymphoma. 2000;39(3-4):229-239
40. Wang FZ, Dahl H, Linde A, Brytting M, Ehrnst A, Ljungman P. Lymphotropic herpes viruses in allogeneic bone marrow transplantation. Blood. 1996;88(9):3615-3620
41. Ljungman P, de la Camara R, Cordonnier C, Einsele H, Engelhard D, Reusser P, et al. Management of CMV, HHV-6, HHV-7 and Kaposi-sarcoma herpesvirus (HHV-8) infections in patients with hematological malignancies and after SCT. Bone Marrow Transpl. 2008;42(4):227-240
42. Shields AF, Hackman RC, Fife KH, Corey L, Meyers JD. Adenovirus infections in patients unDergoing bone-marrow transplantation. N Engl J Med. 1985;312(9):529-533
43. Symeonidis N, Jakubowski A, Pierre-Louis S, Jaffe D, Pamer E, Sepkowitz K, et al. Invasive adenoviral infections in T-celldepleted allogeneic hematopoietic stem cell transplantation: high mortality in the era of cidofovir. Transpl Infect Dis. 2007;9(2):108-113
44. Feuchtinger T, Lang P, Handgretinger R. Adenovirus infection after allogeneic stem cell transplantation. Leuk Lymphoma. 2007;48(2):244-255
45. De Mezerville MH, Tellier R, Richardson S, Hebert D, Doyle J, Allen U. Adenoviral infections in pediatric transplant recipients: a hospital-based study. Pediatr Infect Dis J. 2006;25(9):815-818
46. Van Tol MJ, Kroes AC, Schinkel J, Dinkelaar W, Claas EC, Jol-Van Der Zijde CM, et al. Adenovirus infection in paediatric stem cell transplant recipients: increased risk in young children with a delayed immune recovery. Bone Marrow Transpl. 2005;36(1):39-50.
47. Lion T, Baumgartinger R, Watzinger F, Matthes-Martin S, Suda M, Preuner S, et al. Molecular monitoring of adenovirus in peripheral blood after allogeneic bone marrow transplantation permits early diagnosis of disseminated disease. Blood. 2003;102(3):1114-1120
48. Chakrabarti S, Mautner V, Osman H, Collingham KE, Fegan CD, Klapper PE, et al. Adenovirus infections following allogeneic stem cell transplantation: incidence and outcome in relation to graft manipulation, immunosuppression, and immune recovery. Blood. 2002;100(5):1619-1627
49. La Rosa AM, Champlin RE, Mirza N, Gajewski J, Giralt S, Rolston KV, et al. Adenovirus infections in adult recipients of blood and marrow transplants. Clin Infect Dis. 2001;32(6):871-876 (Pubitemid 32524820)
50. Howard DS, Phillips IG, Reece DE, Munn RK, Henslee-Downey J, Pittard M, et al. Adenovirus infections in hematopoietic stem cell transplant recipients. Clin Infect Dis. 1999;29(6):1494-1501
51. Flomenberg P, Babbitt J, Drobyski WR, Ash RC, Carrigan DR, Sedmak GV, et al. Increasing incidence of adenovirus disease in bone marrow transplant recipients. J Infect Dis. 1994;169(4): 775-781
52. Ljungman P, Ribaud P, Eyrich M, Matthes-Martin S, Einsele H, Bleakley M, et al. Cidofovir for adenovirus infections after allogeneic hematopoietic stem cell transplantation: a survey by the Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation. Bone Marrow Transpl. 2003;31(6):481-486
53. Ebner K, Suda M, Watzinger F, Lion T. Molecular detection and quantitative analysis of the entire spectrum of human adenoviruses by a two-reaction real-time PCR assay. J Clin Microbiol. 2005;43(7):3049-3053
54. Echavarria M, Forman M, Van Tol MJ, Vossen JM, Charache P, Kroes AC. Prediction of severe disseminated adenovirus infection by serum PCR. Lancet. 2001;358(9279):384-385
55. Heim A, Ebnet C, Harste G, Pring-Akerblom P. Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J Med Virol. 2003;70(2):228-239
56. Suparno C, Milligan DW, Moss PA, Mautner V. Adenovirus infections in stem cell transplant recipients: recent developments in unDerstanding of pathogenesis, diagnosis and management. Leuk Lymphoma. 2004;45(5):873-885
57. Erard V, Huang ML, Ferrenberg J, Nguy L, Stevens-Ayers TL, Hackman RC, et al. Quantitative real-time polymerase chain reaction for detection of adenovirus after T cell-replete hematopoietic cell transplantation: viral load as a marker for invasive disease. Clin Infect Dis. 2007;45(8):958-965
58. Gustafson I, Lindblom A, Yun Z, Omar H, Engstrom L, Lewensohn-Fuchs I, et al. Quantification of adenovirus DNA in unrelated donor hematopoietic stem cell transplant recipients. J Clin Virol. 2008;43(1):79-85.
59. Schilham MW, Claas EC, Van Zaane W, Heemskerk B, Vossen JM, Lankester AC, et al. High levels of adenovirus DNA in serum correlate with fatal outcome of adenovirus infection in children after allogeneic stem-cell transplantation. Clin Infect Dis. 2002;35(5):526-532
60. Sivaprakasam P, Carr TF, Coussons M, Khalid T, Bailey AS, Guiver M, et al. Improved outcome from invasive adenovirus infection in pediatric patients after hemopoietic stem cell transplantation using intensive clinical surveillance and early intervention. J Pediatr Hematol Oncol. 2007;29(2):81-85
61. Lion T, Kosulin K, Landlinger C, Rauch M, Preuner S, Jugovic D, et al. Monitoring of adenovirus load in stool by real-time PCR permits early detection of impending invasive infection in patients after allogeneic stem cell transplantation. Leukemia. 2010 (online publication).