The clinical and financial burden of pre-emptive management ofcytomegalovirus disease after allogeneic stem cell transplantation-implications for preventative treatment approaches

Cytotherapy

Volumn 16, Issue 7, 2014, Pages 927-933

  Jain, Natasha A ^a   Lu, Kit ^a   Ito, Sawa ^a   Muranski, Pawel ^a   Hourigan, Christopher S ^a   Haggerty, Janice ^a   Chokshi, Puja D ^a   Ramos, Catalina ^a   Cho, Elena ^a   Cook, Lisa ^a   Childs, Richard ^a   Battiwalla, Minoo ^a   Barrett, A John ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Antiviral cellular therapy; CMV reactivation; Economic cost; Pre emptive therapy

Indexed keywords

FOSCARNET; GANCICLOVIR; VALGANCICLOVIR;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ADOLESCENT; ADULT; AGED; ALLOGENEIC STEM CELL TRANSPLANTATION; APLASTIC ANEMIA; ARTICLE; CHILD; CHRONIC LYMPHATIC LEUKEMIA; CHRONIC MYELOID LEUKEMIA; CHRONIC MYELOMONOCYTIC LEUKEMIA; CONTROLLED STUDY; COST BENEFIT ANALYSIS; CYTOMEGALOVIRUS INFECTION; FEMALE; HEALTH CARE COST; HEMATURIA; HODGKIN DISEASE; HOSPITALIZATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MORTALITY; MULTIPLE MYELOMA; MYELODYSPLASTIC SYNDROME; MYELOPROLIFERATIVE DISORDER; NONHODGKIN LYMPHOMA; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SCHOOL CHILD; T LYMPHOCYTE; UMBILICAL CORD BLOOD; VIRUS REACTIVATION; ALLOTRANSPLANTATION; COST OF ILLNESS; CYTOMEGALOVIRUS; DONOR; ECONOMICS; GENETICS; HEMATOLOGIC NEOPLASMS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; MIDDLE AGED; PATHOGENICITY; PATHOLOGY; RISK FACTOR; VIROLOGY; VIRUS ACTIVATION;

CYTOMEGALOVIRUS;

ADOLESCENT; ADULT; AGED; CHILD; COST OF ILLNESS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FEMALE; HEMATOLOGIC NEOPLASMS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; MALE; MIDDLE AGED; RISK FACTORS; T-LYMPHOCYTES; TISSUE DONORS; TRANSPLANTATION, HOMOLOGOUS; VIRUS ACTIVATION;

EID: 84901985882     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2014.02.010     Document Type: Article

References (51)

1. Nichols W.G., Corey L., Gooley T., Drew W.L., Miner R., Huang M., et al. Rising pp65 antigenemia during preemptive anticytomegalovirus therapy after allogeneic hematopoietic stem cell transplantation: risk factors, correlation with DNA load, and outcomes. Blood 2001, 97:867-874.
2. Nichols W.G., Corey L., Gooley T., Davis C., Boeckh M. High risk of death due to bacterial and fungal infection among cytomegalovirus (CMV)-seronegative recipients of stem cell transplants from seropositive donors: evidence for indirect effects of primary CMV infection. JInfect Dis 2002, 185:273-282.
3. Boeckh M., Nichols W.G. The impact of cytomegalovirus serostatus of donor and recipient before hematopoietic stem cell transplantation in the era of antiviral prophylaxis and preemptive therapy. Blood 2004, 103:2003-2008.
4. Boeckh M., Gooley T.A., Myerson D., Cunningham T., Schoch G., Bowden R.A. Cytomegalovirus pp65 antigenemia-guided early treatment with ganciclovir versus ganciclovir at engraftment after allogeneic marrow transplantation: a randomized double-blind study. Blood 1996, 88:4063-4071.
5. Griffiths P., Whitley R., Snydman D.R., Singh N., Boeckh M. Contemporary management of cytomegalovirus infection in transplant recipients: guidelines from an IHMF workshop, 2007. Herpes 2008, 15:4-12.
6. Bacigalupo A., Bregante S., Tedone E., Isaza A., Van Lint M.T., Moro F., et al. Combined foscarnet-ganciclovir treatment for cytomegalovirus infections after allogeneic hemopoietic stem cell transplantation (Hsct). Bone Marrow Transplant 1996, 18(Suppl. 2):110-114.
7. Bregante S., Bertilson S., Tedone E., Van Lint M.T., Trespi G., Mordini N., et al. Foscarnet prophylaxis of cytomegalovirus infections in patients undergoing allogeneic bone marrow transplantation (BMT): a dose-finding study. Bone Marrow Transplant 2000, 26:23-29.
8. Boeckh M., Bowden R.A., Gooley T., Myerson D., Corey L. Successful modification of a pp65 antigenemia-based early treatment strategy for prevention of cytomegalovirus disease in allogeneic marrow transplant recipients. Blood 1999, 93:1781-1782.
9. Einsele H., Ehninger G., Hebart H., Wittkowski K.M., Schuler U., Jahn G., et al. Polymerase chain reaction monitoring reduces the incidence of cytomegalovirus disease and the duration and side effects of antiviral therapy after bone marrow transplantation. Blood 1995, 86:2815-2820.
10. Ljungman P., Engelhard D., Link H., Biron P., Brandt L., Brunet S., et al. Treatment of interstitial pneumonitis due to cytomegalovirus with ganciclovir and intravenous immune globulin: experience of European Bone Marrow Transplant Group. Clin Infect Dis 1992, 14:831-835.
11. Junghanss C., Storb R., Maris M.B., Carter R.A., Sandmaier B.M., Maloney D.G., et al. Impact of unrelated donor status on the incidence and outcome of cytomegalovirus infections after non-myeloablative allogeneic stem cell transplantation. Br J Haematol 2003, 123:662-670.
12. Ljungman P., Brand R., Einsele H., Frassoni F., Niederwieser D., Cordonnier C. Donor CMV serologic status and outcome of CMV-seropositive recipients after unrelated donor stem cell transplantation: an EBMT megafile analysis. Blood 2003, 102:4255-4260.
13. Craddock C., Szydlo R.M., Dazzi F., Olavarria E., Cwynarski K., Yong A., et al. Cytomegalovirus seropositivity adversely influences outcome after T-depleted unrelated donor transplant in patients with chronic myeloid leukaemia: the case for tailored graft-versus-host disease prophylaxis. Br J Haematol 2001, 112:228-236.
14. Meijer E., Dekker A.W., Rozenberg-Arska M., Weersink A.J., Verdonck L.F. Influence of cytomegalovirus seropositivity on outcome after T cell-depleted bone marrow transplantation: contrasting results between recipients of grafts from related and unrelated donors. Clin Infect Dis 2002, 35:703-712.
15. Salzberger B., Bowden R.A., Hackman R.C., Davis C., Boeckh M. Neutropenia in allogeneic marrow transplant recipients receiving ganciclovir for prevention of cytomegalovirus disease: risk factors and outcome. Blood 1997, 90:2502-2508.
16. Battiwalla M., Wu Y., Bajwa R.P., Radovic M., Almyroudis N.G., Segal B.H., et al. Ganciclovir inhibits lymphocyte proliferation by impairing DNA synthesis. Biol Blood Marrow Transplant 2007, 13:765-770.
17. Nakamura R., Battiwalla M., Solomon S., Follmann D., Chakrabarti S., Cortez K., et al. Persisting posttransplantation cytomegalovirus antigenemia correlates with poor lymphocyte proliferation to cytomegalovirus antigen and predicts for increased late relapse and treatment failure. Biol Blood Marrow Transplant 2004, 10:49-57.
18. Riddell S.R., Watanabe K.S., Goodrich J.M., Li C.R., Agha M.E., Greenberg P.D. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 1992, 257:238-241.
19. Walter E.A., Greenberg P.D., Gilbert M.J., Finch R.J., Watanabe K.S., Thomas E.D., et al. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. NEngl J Med 1995, 333:1038-1044.
20. Micklethwaite K., Hansen A., Foster A., Snape E., Antonenas V., Sartor M., et al. Ex vivo expansion and prophylactic infusion of CMV-pp65 peptide-specific cytotoxic T-lymphocytes following allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2007, 13:707-714.
21. Cobbold M., Khan N., Pourgheysari B., Tauro S., McDonald D., Osman H., et al. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. JExp Med 2005, 202:379-386.
22. Leen A.M., Myers G.D., Sili U., Huls M.H., Weiss H., Leung K.S., et al. Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat Med 2006, 12:1160-1166.
23. Park K.D., Marti L., Kurtzberg J., Szabolcs P. In vitro priming and expansion of cytomegalovirus-specific Th1 and Tc1 T cells from naive cord blood lymphocytes. Blood 2006, 108:1770-1773.
24. Einsele H., Roosnek E., Rufer N., Sinzger C., Riegler S., Loffler J., et al. Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 2002, 99:3916-3922.
25. Green M.L., Leisenring W., Stachel D., Pergam S.A., Sandmaier B.M., Wald A., et al. Efficacy of a viral load-based, risk-adapted, preemptive treatment strategy for prevention ofcytomegalovirus disease after hematopoietic cell transplantation. Biol Blood Marrow Transplant 2012, 18:1687-1699.
26. Matsumura T., Narimatsu H., Kami M., Yuji K., Kusumi E., Hori A., et al. Cytomegalovirus infections following umbilical cord blood transplantation using reduced intensity conditioning regimens for adult patients. Biol Blood Marrow Transplant 2007, 13:577-583.
27. Saglio F., Hanley P.J., Bollard C.M. The time is now: moving toward virus-specific T cells after allogeneic hematopoietic stem cell transplantation as the standard of care. Cytotherapy 2014, 16:149-159.
28. La Rosa C., Longmate J., Lacey S.F., Kaltcheva T., Sharan R., Marsano D., et al. Clinical evaluation of safety and immunogenicity of PADRE-cytomegalovirus (CMV) and tetanus-CMV fusion peptide vaccines with or without PF03512676 adjuvant. JInfect Dis 2012, 205:1294-1304.
29. Ljungman P., Griffiths P., Paya C. Definitions of cytomegalovirus infection and disease in transplant recipients. Clin Infect Dis 2002, 34:1094-1097.
30. Takami A., Mochizuki K., Asakura H., Yamazaki H., Okumura H., Nakao S. High incidence of cytomegalovirus reactivation in adult recipients of an unrelated cord blood transplant. Haematologica 2005, 90:1290-1292.
31. Tomonari A., Takahashi S., Ooi J., Tsukada N., Konuma T., Kato S., et al. Impact of cytomegalovirus serostatus on outcome of unrelated cord blood transplantation for adults: a single-institute experience in Japan. Eur J Haematol 2008, 80:251-257.
32. Vij R., Khoury H., Brown R., Goodnough L.T., Devine S.M., Blum W., et al. Low-dose short-course intravenous ganciclovir as pre-emptive therapy for CMV viremia post allo-PBSC transplantation. Bone Marrow Transplant 2003, 32:703-707.
33. Khera N., Zeliadt S.B., Lee S.J. Economics of hematopoietic cell transplantation. Blood 2012, 120:1545-1551.
34. Majhail N.S., Mothukuri J.M., Brunstein C.G., Weisdorf D.J. Costs of hematopoietic cell transplantation: comparison of umbilical cord blood and matched related donor transplantation and the impact of posttransplant complications. Biol Blood Marrow Transplant 2009, 15:564-573.
35. Gratama J.W., Boeckh M., Nakamura R., Cornelissen J.J., Brooimans R.A., Zaia J.A., et al. Immune monitoring with iTAg MHC Tetramers for prediction of recurrent or persistent cytomegalovirus infection or disease in allogeneic hematopoietic stem cell transplant recipients: a prospective multicenter study. Blood 2010, 116:1655-1662.
36. Einsele H., Hebart H., Kauffmann-Schneider C., Sinzger C., Jahn G., Bader P., et al. Risk factors for treatment failures in patients receiving PCR-based preemptive therapy for CMV infection. Bone Marrow Transplant 2000, 25:757-763.
37. Ito S., Pophali P., Co W., Koklanaris E.K., Superata J., Fahle G.A., et al. CMV reactivation is associated with a lower incidence of relapse after allo-SCT for CML. Bone Marrow Transplant 2013, 48:1313-1316.
38. Elmaagacli A.H., Steckel N.K., Koldehoff M., Hegerfeldt Y., Trenschel R., Ditschkowski M., et al. Early human cytomegalovirus replication after transplantation is associated with a decreased relapse risk: evidence for a putative virus-versus-leukemia effect in acute myeloid leukemia patients. Blood 2011, 118:1402-1412.
39. Green M.L., Leisenring W.M., Xie H., Walter R.B., Mielcarek M., Sandmaier B.M., et al. CMV reactivation after allogeneic HCT and relapse risk: evidence for early protection in acute myeloid leukemia. Blood 2013, 122:1316-1324.
40. Mackinnon S., Thomson K., Verfuerth S., Peggs K., Lowdell M. Adoptive cellular therapy for cytomegalovirus infection following allogeneic stem cell transplantation using virus-specific T cells. Blood Cells Mol Dis 2008, 40:63-67.
41. Peggs K.S., Thomson K., Samuel E., Dyer G., Armoogum J., Chakraverty R., et al. Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stem cell transplantation. Clin Infect Dis 2011, 52:49-57.
42. Heslop H.E., Leen A.M. T-cell therapy for viral infections. Hematology 2013, 2013:342-347.
43. Gerdemann U., Katari U.L., Papadopoulou A., Keirnan J.M., Craddock J.A., Liu H., et al. Safety and clinical efficacy of rapidly-generated trivirus-directed T cells as treatment for adenovirus, EBV, and CMV infections after allogeneic hematopoietic stem cell transplant. Mol Ther 2013, 21:2113-2121.
44. Gerdemann U., Keirnan J.M., Katari U.L., Yanagisawa R., Christin A.S., Huye L.E., et al. Rapidly generated multivirus-specific cytotoxic T lymphocytes for the prophylaxis and treatment of viral infections. Mol Ther 2012, 20:1622-1632.
45. Blyth E., Clancy L., Simms R., Ma C.K., Burgess J., Deo S., et al. Donor-derived CMV-specific T cells reduce the requirement for CMV-directed pharmacotherapy after allogeneic stem cell transplantation. Blood 2013, 121:3745-3758.
46. Meij P., Jedema I., Zandvliet M.L., van der Heiden P.L., van de Meent M., van Egmond H.M., et al. Effective treatment of refractory CMV reactivation after allogeneic stem cell transplantation with in vitro-generated CMV pp65-specific CD8+ T-cell lines. JImmunother 2012, 35:621-628.
47. Leen A.M., Bollard C.M., Mendizabal A.M., Shpall E.J., Szabolcs P., Antin J.H., et al. Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stem cell transplantation. Blood 2013, 121:5113-5123.
48. Kharfan-Dabaja M.A., Boeckh M., Wilck M.B., Langston A.A., Chu A.H., Wloch M.K., et al. Anovel therapeutic cytomegalovirus DNA vaccine in allogeneic haemopoietic stem-cell transplantation: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Infect Dis 2012, 12:290-299.
49. Schleiss M.R. Cytomegalovirus vaccines: at last, a major step forward. Herpes 2009, 15:44-45.
50. Grigoleit G.U., Kapp M., Hebart H., Fick K., Beck R., Jahn G., et al. Dendritic cell vaccination in allogeneic stem cell recipients: induction of human cytomegalovirus (HCMV)-specific cytotoxic T lymphocyte responses even in patients receiving a transplant from an HCMV-seronegative donor. JInfect Dis 2007, 196:699-704.
51. Peggs K.S., Verfuerth S., Pizzey A., Khan N., Guiver M., Moss P.A., et al. Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 2003, 362:1375-1377.