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01-10-2015 | Original Article

Virus infection in HLA-haploidentical hematopoietic stem cell transplantation: incidence in the context of immune recovery in two different transplantation settings

Authors: Johanna Tischer, Nicole Engel, Susanne Fritsch, Dusan Prevalsek, Max Hubmann, Christoph Schulz, Anna-K. Zoellner, Veit Bücklein, Roland Reibke, Friederike Mumm, Christina T. Rieger, Wolfgang Hill, Georg Ledderose, Hans Joachim Stemmler, Thomas Köhnke, Gundula Jäger, Hans Jochem Kolb, Christoph Schmid, Andreas Moosmann, Andreas Hausmann

Published in: Annals of Hematology | Issue 10/2015

Abstract

We retrospectively compared the incidence of virus infections and outcome in the context of immune reconstitution in two different HLA-haploidentical transplantation (haplo-HSCT) settings. The first was a combined T-cell-replete and T-cell-deplete approach using antithymocyte globulin (ATG) prior to transplantation in patients with hematological diseases (cTCR/TCD group, 28 patients; median age 31 years). The second was a T-cell-replete (TCR) approach using high-dose posttransplantation cyclophosphamide (TCR/PTCY group, 27 patients; median age 43 years). The incidence of herpesvirus infection was markedly lower in the TCR/PTCY (22 %) than in the cTCR/TCD group (93 %). Recovery of CD4+ T cells on day +100 was faster in the TCR/PTCY group. CMV reactivation was 30 % in the TCR/PTCY compared to 57 % in the cTCR/TCD group, and control with antiviral treatment was superior after TCR/PTCY transplantation (100 vs 50 % cTCR/TCD). Twenty-five percent of the patients in the cTCR/TCD group but no patient in the TCR/PTCY group developed PTLD. While 1-year OS was not different (TCR/PTCY 59 % vs cTCR/TCD 39 %; p = 0.28), virus infection-related mortality (VIRM) was significantly lower after TCR/PTCY transplantation (1-year VIRM, 0 % TCR/PTCY vs 29 % cTCR/TCD; p = 0.009). On day +100, predictors of better OS were lymphocytes >300/μl, CD3+ T cells >200/μl, and CD4+ T cells >150/μl, whereas the application of steroids >1 mg/kg was correlated with worse outcome. Our results suggest that by presumably preserving antiviral immunity and allowing fast immune recovery of CD4+ T cells, the TCR approach using posttransplantation cyclophosphamide is well suited to handle the important issue of herpesvirus infection after haplo-HSCT.

Anasetti C, Beatty PG, Storb R, Martin PJ, Mori M, Sanders JE, Thomas ED, Hansen JA (1990) Effect of HLA incompatibility on graft-versus-host disease, relapse, and survival after marrow transplantation for patients with leukemia or lymphoma. Hum Immunol 29(2):79–91CrossRefPubMed

Powles RL, Morgenstern GR, Kay HE, McElwain TJ, Clink HM, Dady PJ, Barrett A, Jameson B, Depledge MH, Watson JG, Sloane J, Leigh M, Lumley H, Hedley D, Lawler SD, Filshie J, Robinson B (1983) Mismatched family donors for bone-marrow transplantation as treatment for acute leukaemia. Lancet 1(8325):612–615CrossRefPubMed

Ash RC, Horowitz MM, Gale RP, van Bekkum DW, Casper JT, Gordon-Smith EC, Henslee PJ, Kolb HJ, Lowenberg B, Masaoka T et al (1991) Bone marrow transplantation from related donors other than HLA-identical siblings: effect of T cell depletion. Bone Marrow Transplant 7(6):443–452PubMed

Aversa F, Tabilio A, Velardi A, Cunningham I, Terenzi A, Falzetti F, Ruggeri L, Barbabietola G, Aristei C, Latini P, Reisner Y, Martelli MF (1998) Treatment of high-risk acute leukemia with T-cell-depleted stem cells from related donors with one fully mismatched HLA haplotype. N Engl J Med 339(17):1186–1193. doi:10.1056/NEJM199810223391702 CrossRefPubMed

Aversa F, Terenzi A, Tabilio A, Falzetti F, Carotti A, Ballanti S, Felicini R, Falcinelli F, Velardi A, Ruggeri L, Aloisi T, Saab JP, Santucci A, Perruccio K, Martelli MP, Mecucci C, Reisner Y, Martelli MF (2005) Full haplotype-mismatched hematopoietic stem-cell transplantation: a phase II study in patients with acute leukemia at high risk of relapse. J Clin Oncol 23(15):3447–3454. doi:10.1200/JCO.2005.09.117 CrossRefPubMed

Ciceri F, Labopin M, Aversa F, Rowe JM, Bunjes D, Lewalle P, Nagler A, Di Bartolomeo P, Lacerda JF, Lupo Stanghellini MT, Polge E, Frassoni F, Martelli MF, Rocha V (2008) A survey of fully haploidentical hematopoietic stem cell transplantation in adults with high-risk acute leukemia: a risk factor analysis of outcomes for patients in remission at transplantation. Blood 112(9):3574–3581. doi:10.1182/blood-2008-02-140095 CrossRefPubMed

Lacerda JF, Martins C, Carmo JA, Lourenco F, Juncal C, Rodrigues A, Vilalobos I, Moura MC, Ligeiro D, Martinho A, Lacerda JM (2003) Haploidentical stem cell transplantation with purified CD34 cells after a chemotherapy-alone conditioning regimen. Biol Blood Marrow Transplant 9(10):633–642. doi:10.1016/S1083 CrossRefPubMed

Ogawa H, Ikegame K, Yoshihara S, Kawakami M, Fujioka T, Masuda T, Taniguchi Y, Hasei H, Kaida K, Inoue T, Kim EH, Kawase I (2006) Unmanipulated HLA 2-3 antigen-mismatched (haploidentical) stem cell transplantation using nonmyeloablative conditioning. Biol Blood Marrow Transplant 12(10):1073–1084. doi:10.1016/j.bbmt.2006.06.007 CrossRefPubMed

Rizzieri DA, Koh LP, Long GD, Gasparetto C, Sullivan KM, Horwitz M, Chute J, Smith C, Gong JZ, Lagoo A, Niedzwiecki D, Dowell JM, Waters-Pick B, Liu C, Marshall D, Vredenburgh JJ, Gockerman J, Decastro C, Moore J, Chao NJ (2007) Partially matched, nonmyeloablative allogeneic transplantation: clinical outcomes and immune reconstitution. J Clin Oncol 25(6):690–697. doi:10.1200/JCO.2006.07.0953 CrossRefPubMed

10.

Sykes M, Preffer F, McAfee S, Saidman SL, Weymouth D, Andrews DM, Colby C, Sackstein R, Sachs DH, Spitzer TR (1999) Mixed lymphohaemopoietic chimerism and graft-versus-lymphoma effects after non-myeloablative therapy and HLA-mismatched bone-marrow transplantation. Lancet 353(9166):1755–1759. doi:10.1016/S0140-6736(98)11135-2 CrossRefPubMed

11.

Handgretinger R, Klingebiel T, Lang P, Schumm M, Neu S, Geiselhart A, Bader P, Schlegel PG, Greil J, Stachel D, Herzog RJ, Niethammer D (2001) Megadose transplantation of purified peripheral blood CD34(+) progenitor cells from HLA-mismatched parental donors in children. Bone Marrow Transplant 27(8):777–783. doi:10.1038/sj.bmt.1702996 CrossRefPubMed

12.

Bethge WA, Haegele M, Faul C, Lang P, Schumm M, Bornhauser M, Handgretinger R, Kanz L (2006) Haploidentical allogeneic hematopoietic cell transplantation in adults with reduced-intensity conditioning and CD3/CD19 depletion: fast engraftment and low toxicity. Exp Hematol 34(12):1746–1752. doi:10.1016/j.exphem.2006.08.009 CrossRefPubMed

13.

Boeckh M, Erard V, Zerr D, Englund J (2005) Emerging viral infections after hematopoietic cell transplantation. Pediatr Transplant 9(Suppl 7):48–54. doi:10.1111/j.1399-3046.2005.00442.x CrossRefPubMed

14.

Dykewicz CA (2001) Summary of the guidelines for preventing opportunistic infections among hematopoietic stem cell transplant recipients. Clin Infect Dis 33(2):139–144. doi:10.1086/321805 CrossRefPubMed

15.

Einsele H, Bertz H, Beyer J, Kiehl MG, Runde V, Kolb HJ, Holler E, Beck R, Schwerdfeger R, Schumacher U, Hebart H, Martin H, Kienast J, Ullmann AJ, Maschmeyer G, Kruger W, Niederwieser D, Link H, Schmidt CA, Oettle H, Klingebiel T (2003) Infectious complications after allogeneic stem cell transplantation: epidemiology and interventional therapy strategies—guidelines of the Infectious Diseases Working Party (AGIHO) of the German Society of Hematology and Oncology (DGHO). Ann Hematol 82(Suppl 2):S175–185. doi:10.1007/s00277-003-0772-4 CrossRefPubMed

16.

Ciurea SO, Mulanovich V, Saliba RM, Bayraktar UD, Jiang Y, Bassett R, Wang SA, Konopleva M, Fernandez-Vina M, Montes N, Bosque D, Chen J, Rondon G, Alatrash G, Alousi A, Bashir Q, Korbling M, Qazilbash M, Parmar S, Shpall E, Nieto Y, Hosing C, Kebriaei P, Khouri I, Popat U, de Lima M, Champlin RE (2012) Improved early outcomes using a T cell replete graft compared with T cell depleted haploidentical hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 18(12):1835–1844. doi:10.1016/j.bbmt.2012.07.003 PubMedCentralCrossRefPubMed

17.

Luznik L, O’Donnell PV, Symons HJ, Chen AR, Leffell MS, Zahurak M, Gooley TA, Piantadosi S, Kaup M, Ambinder RF, Huff CA, Matsui W, Bolanos-Meade J, Borrello I, Powell JD, Harrington E, Warnock S, Flowers M, Brodsky RA, Sandmaier BM, Storb RF, Jones RJ, Fuchs EJ (2008) HLA-haploidentical bone marrow transplantation for hematologic malignancies using nonmyeloablative conditioning and high-dose, posttransplantation cyclophosphamide. Biol Blood Marrow Transplant 14(6):641–650. doi:10.1016/j.bbmt.2008.03.005 PubMedCentralCrossRefPubMed

18.

Schuster FR, Meisel R, Fuhrer M, Reuther S, Hauer J, Tischer J, Feuchtinger T, Laws HJ, Kolb HJ, Borkhardt A (2013) Anti-leukaemic activity of a novel haploidentical-transplantation approach employing unmanipulated bone marrow followed by CD6-depleted peripheral blood stem cells in children with refractory/relapsed acute leukaemia. Br J Haematol 162(6):802–807. doi:10.1111/bjh.12455 CrossRefPubMed

19.

Kolb H-J, Bigalke I, Simoes B, Falk C, Tischer J, Hill W, Ledderose G (2004) CD6-depleted mobilized stem cells for modification of HVG and GVH reactions after HLA-haploidentical marrow transplantation. ASH Annu Meet Abstr 104(11):978

20.

Tischer J, Engel N, Fritsch S, Prevalsek D, Hubmann M, Schulz C, Zoellner AK, Bucklein V, Lippl S, Reibke R, Rieger CT, Ledderose G, Stemmler HJ, Hiddemann W, Schmid C, Hausmann A (2014) Second haematopoietic SCT using HLA-haploidentical donors in patients with relapse of acute leukaemia after a first allogeneic transplantation. Bone Marrow Transplant 49(7):895–901. doi:10.1038/bmt.2014.83 CrossRefPubMed

21.

Tischer J, Stemmler HJ, Engel N, Hubmann M, Fritsch S, Prevalsek D, Schulz C, Zoellner AK, Bucklein V, Hill W, Ledderose G, Hausmann A (2013) Feasibility of clofarabine cytoreduction followed by haploidentical hematopoietic stem cell transplantation in patients with relapsed or refractory advanced acute leukemia. Ann Hematol 92(10):1379–1388. doi:10.1007/s00277-013-1862-6 CrossRefPubMed

22.

Ljungman P, Griffiths P, Paya C (2002) Definitions of cytomegalovirus infection and disease in transplant recipients. Clin Infect Dis 34(8):1094–1097. doi:10.1086/339329 CrossRefPubMed

23.

Ganepola S, Gentilini C, Hilbers U, Lange T, Rieger K, Hofmann J, Maier M, Liebert UG, Niederwieser D, Engelmann E, Heilbronn R, Thiel E, Uharek L (2007) Patients at high risk for CMV infection and disease show delayed CD8+ T-cell immune recovery after allogeneic stem cell transplantation. Bone Marrow Transplant 39(5):293–299. doi:10.1038/sj.bmt.1705585 CrossRefPubMed

24.

Bacigalupo A, Ballen K, Rizzo D, Giralt S, Lazarus H, Ho V, Apperley J, Slavin S, Pasquini M, Sandmaier BM, Barrett J, Blaise D, Lowski R, Horowitz M (2009) Defining the intensity of conditioning regimens: working definitions. Biol Blood Marrow Transplant 15(12):1628–1633. doi:10.1016/j.bbmt.2009.07.004 PubMedCentralCrossRefPubMed

25.

Filipovich AH, Weisdorf D, Pavletic S, Socie G, Wingard JR, Lee SJ, Martin P, Chien J, Przepiorka D, Couriel D, Cowen EW, Dinndorf P, Farrell A, Hartzman R, Henslee-Downey J, Jacobsohn D, McDonald G, Mittleman B, Rizzo JD, Robinson M, Schubert M, Schultz K, Shulman H, Turner M, Vogelsang G, Flowers ME (2005) 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 11(12):945–956. doi:10.1016/j.bbmt.2005.09.004 CrossRefPubMed

26.

Przepiorka D, Weisdorf D, Martin P, Klingemann HG, Beatty P, Hows J, Thomas ED (1995) 1994 Consensus conference on acute GVHD grading. Bone Marrow Transplant 15(6):825–828PubMed

27.

Kaplan E, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457–481CrossRef

28.

Moosmann A, Bigalke I, Tischer J, Schirrmann L, Kasten J, Tippmer S, Leeping M, Prevalsek D, Jaeger G, Ledderose G, Mautner J, Hammerschmidt W, Schendel DJ, Kolb HJ (2010) Effective and long-term control of EBV PTLD after transfer of peptide-selected T cells. Blood 115(14):2960–2970. doi:10.1182/blood-2009-08-236356 CrossRefPubMed

29.

Mulanovich VE, Jiang Y, de Lima M, Shpall EJ, Champlin RE, Ciurea SO (2011) Infectious complications in cord blood and T-cell depleted haploidentical stem cell transplantation. Am J Blood Res 1(1):98–105PubMedCentralPubMed

30.

Parody R, Martino R, Rovira M, Vazquez L, Vazquez MJ, de la Camara R, Blazquez C, Fernandez-Aviles F, Carreras E, Salavert M, Jarque I, Martin C, Martinez F, Lopez J, Torres A, Sierra J, Sanz GF (2006) Severe infections after unrelated donor allogeneic hematopoietic stem cell transplantation in adults: comparison of cord blood transplantation with peripheral blood and bone marrow transplantation. Biol Blood Marrow Transplant 12(7):734–748. doi:10.1016/j.bbmt.2006.03.007 CrossRefPubMed

31.

Ruggeri A, Peffault de Latour R, Carmagnat M, Clave E, Douay C, Larghero J, Cayuela JM, Traineau R, Robin M, Madureira A, Ribaud P, Ferry C, Devergie A, Purtill D, Rabian C, Gluckman E, Toubert A, Socie G, Rocha V (2011) Outcomes, infections, and immune reconstitution after double cord blood transplantation in patients with high-risk hematological diseases. Transpl Infect Dis 13(5):456–465. doi:10.1111/j.1399-3062.2011.00632.x CrossRefPubMed

32.

Verdeguer A, de Heredia CD, Gonzalez M, Martinez AM, Fernandez-Navarro JM, Perez-Hurtado JM, Badell I, Gomez P, Gonzalez ME, Munoz A, Diaz MA (2011) Observational prospective study of viral infections in children undergoing allogeneic hematopoietic cell transplantation: a 3-year GETMON experience. Bone Marrow Transplant 46(1):119–124. doi:10.1038/bmt.2010.52 CrossRefPubMed

33.

Chang YJ, Zhao XY, Huo MR, Xu LP, Liu DH, Liu KY, Huang XJ (2012) Immune reconstitution following unmanipulated HLA-mismatched/haploidentical transplantation compared with HLA-identical sibling transplantation. J Clin Immunol 32(2):268–280. doi:10.1007/s10875-011-9630-7 CrossRefPubMed

34.

Dominietto A, Raiola AM, Bruno B, van Lint MT, Frassoni F, Grazia CD, Gualandi F, Bregante S, Varaldo R, Ghiso A, Bacigalupo A (2011) Rapid immune reconstitution following unmanipulated haploidentical BMT with post-transplant high dose cyclophosphamide. ASH Annu Meet Abstr 118((21):3050

35.

Lu DP, Dong L, Wu T, Huang XJ, Zhang MJ, Han W, Chen H, Liu DH, Gao ZY, Chen YH, Xu LP, Zhang YC, Ren HY, Li D, Liu KY (2006) Conditioning including antithymocyte globulin followed by unmanipulated HLA-mismatched/haploidentical blood and marrow transplantation can achieve comparable outcomes with HLA-identical sibling transplantation. Blood 107(8):3065–3073. doi:10.1182/blood-2005-05-2146 CrossRefPubMed

36.

Rieger CT, Rieger H, Kolb HJ, Peterson L, Huppmann S, Fiegl M, Ostermann H (2009) Infectious complications after allogeneic stem cell transplantation: incidence in matched-related and matched-unrelated transplant settings. Transpl Infect Dis 11(3):220–226. doi:10.1111/j.1399-3062.2009.00379.x CrossRefPubMed

37.

Finke J, Bethge WA, Schmoor C, Ottinger HD, Stelljes M, Zander AR, Volin L, Ruutu T, Heim DA, Schwerdtfeger R, Kolbe K, Mayer J, Maertens JA, Linkesch W, Holler E, Koza V, Bornhauser M, Einsele H, Kolb HJ, Bertz H, Egger M, Grishina O, Socie G, Group AT-FT (2009) Standard graft-versus-host disease prophylaxis with or without anti-T-cell globulin in haematopoietic cell transplantation from matched unrelated donors: a randomised, open-label, multicentre phase 3 trial. Lancet Oncol 10(9):855–864CrossRefPubMed

38.

Pidala J, Tomblyn M, Nishihori T, Ayala E, Field T, Fernandez H, Perez L, Locke F, Alsina M, Ochoa JL, Perkins J, Tate C, Shapiro J, Conwell M, Bookout R, Anasetti C (2011) ATG prevents severe acute graft-versus-host disease in mismatched unrelated donor hematopoietic cell transplantation. Biol Blood Marrow Transplant 17(8):1237–1244. doi:10.1016/j.bbmt.2010.12.705 CrossRefPubMed

39.

Muller TF, Grebe SO, Neumann MC, Heymanns J, Radsak K, Sprenger H, Lange H (1997) Persistent long-term changes in lymphocyte subsets induced by polyclonal antibodies. Transplantation 64(10):1432–1437CrossRefPubMed

40.

Shenoy S, Mohanakumar T, Todd G, Westhoff W, Dunnigan K, Adkins DR, Brown RA, DiPersio JF (1999) Immune reconstitution following allogeneic peripheral blood stem cell transplants. Bone Marrow Transplant 23(4):335–346. doi:10.1038/sj.bmt.1701581 CrossRefPubMed

41.

Luznik L, Jalla S, Engstrom LW, Iannone R, Fuchs EJ (2001) Durable engraftment of major histocompatibility complex-incompatible cells after nonmyeloablative conditioning with fludarabine, low-dose total body irradiation, and posttransplantation cyclophosphamide. Blood 98(12):3456–3464CrossRefPubMed

42.

Raiola AM, Dominietto A, Ghiso A, Di Grazia C, Lamparelli T, Gualandi F, Bregante S, Van Lint MT, Geroldi S, Luchetti S, Ballerini F, Miglino M, Varaldo R, Bacigalupo A (2013) Unmanipulated haploidentical bone marrow transplantation and posttransplantation cyclophosphamide for hematologic malignancies after myeloablative conditioning. Biol Blood Marrow Transplant 19(1):117–122. doi:10.1016/j.bbmt.2012.08.014 CrossRefPubMed

43.

Mayumi H, Himeno K, Tokuda N, Nomoto K (1986) Drug-induced tolerance to allografts in mice. VII. Optimal protocol and mechanism of cyclophosphamide-induced tolerance in an H-2 haplotype-identical strain combination. Transplant Proc 18(2):363–369PubMed

44.

Kanakry CG, Ganguly S, Zahurak M, Bolanos-Meade J, Thoburn C, Perkins B, Fuchs EJ, Jones RJ, Hess AD, Luznik L (2013) Aldehyde dehydrogenase expression drives human regulatory T cell resistance to posttransplantation cyclophosphamide. Sci Transl Med 5(211):211ra–157. doi:10.1126/scitranslmed.3006960

45.

Kastan MB, Schlaffer E, Russo JE, Colvin OM, Civin CI, Hilton J (1990) Direct demonstration of elevated aldehyde dehydrogenase in human hematopoietic progenitor cells. Blood 75(10):1947–1950PubMed

46.

Munchel A, Kesserwan C, Symons HJ, Luznik L, Kasamon YL, Jones RJ, Fuchs EJ (2011) Nonmyeloablative, HLA-haploidentical bone marrow transplantation with high dose, post-transplantation cyclophosphamide. Pediatr Rep 3(Suppl 2):e15. doi:10.4081/pr.2011.s2.e15 PubMedCentralPubMed

47.

Kanakry JA, Kasamon YL, Gocke CD, Tsai HL, Davis-Sproul J, Ghosh N, Symons H, Bolanos-Meade J, Gladstone DE, Swinnen LJ, Luznik L, Fuchs EJ, Jones RJ, Ambinder RF (2013) Outcomes of related donor HLA-identical or HLA-haploidentical allogeneic blood or marrow transplantation for peripheral T cell lymphoma. Biol Blood Marrow Transplant 19(4):602–606. doi:10.1016/j.bbmt.2013.01.006 PubMedCentralCrossRefPubMed

48.

Solomon SR, Sizemore CA, Sanacore M, Zhang X, Brown S, Holland HK, Morris LE, Bashey A (2012) Haploidentical transplantation using T cell replete peripheral blood stem cells and myeloablative conditioning in patients with high-risk hematologic malignancies who lack conventional donors is well tolerated and produces excellent relapse-free survival: results of a prospective phase II trial. Biol Blood Marrow Transplant 18(12):1859–1866. doi:10.1016/j.bbmt.2012.06.019 CrossRefPubMed

49.

Brunstein CG, Weisdorf DJ, DeFor T, Barker JN, Tolar J, van Burik JA, Wagner JE (2006) Marked increased risk of Epstein-Barr virus-related complications with the addition of antithymocyte globulin to a nonmyeloablative conditioning prior to unrelated umbilical cord blood transplantation. Blood 108(8):2874–2880. doi:10.1182/blood-2006-03-011791 PubMedCentralCrossRefPubMed

50.

Berger M, Figari O, Bruno B, Raiola A, Dominietto A, Fiorone M, Podesta M, Tedone E, Pozzi S, Fagioli F, Madon E, Bacigalupo A (2008) Lymphocyte subsets recovery following allogeneic bone marrow transplantation (BMT): CD4+ cell count and transplant-related mortality. Bone Marrow Transplant 41(1):55–62. doi:10.1038/sj.bmt.1705870 CrossRefPubMed

51.

Kim DH, Sohn SK, Won DI, Lee NY, Suh JS, Lee KB (2006) Rapid helper T-cell recovery above 200 × 10⁶/l at 3 months correlates to successful transplant outcomes after allogeneic stem cell transplantation. Bone Marrow Transplant 37(12):1119–1128. doi:10.1038/sj.bmt.1705381 CrossRefPubMed

52.

Chang YJ, Zhao XY, Xu LP, Liu DH, Liu KY, Chen YH, Wang Y, Zhang XH, Zhao XS, Han W, Chen H, Wang FR, Lv M, Huang XJ (2013) Early lymphocyte recovery predicts superior overall survival after unmanipulated haploidentical blood and marrow transplant for myelodysplastic syndrome and acute myeloid leukemia evolving from myelodysplastic syndrome. Leuk Lymphoma 54(12):2671–2677. doi:10.3109/10428194.2013.783912 CrossRefPubMed

53.

Ciurea SO, Mulanovich V, Jiang Y, Bassett R, Rondon G, McMannis J, de Lima M, Shpall EJ, Champlin RE (2011) Lymphocyte recovery predicts outcomes in cord blood and T cell-depleted haploidentical stem cell transplantation. Biol Blood Marrow Transplant 17(8):1169–1175. doi:10.1016/j.bbmt.2010.11.020 PubMedCentralCrossRefPubMed

54.

Wolfromm A, Porcher R, Legoff J, Peffault de Latour R, Xhaard A, de Fontbrune FS, Ribaud P, Bergeron A, Socie G, Robin M (2014) Viral respiratory infections diagnosed by multiplex PCR after allogeneic hematopoietic stem cell transplantation: long-term incidence and outcome. Biol Blood Marrow Transplant 20(8):1238–1241. doi:10.1016/j.bbmt.2014.04.004 CrossRefPubMed

Title: Virus infection in HLA-haploidentical hematopoietic stem cell transplantation: incidence in the context of immune recovery in two different transplantation settings
Authors: Johanna Tischer
Nicole Engel
Susanne Fritsch
Dusan Prevalsek
Max Hubmann
Christoph Schulz
Anna-K. Zoellner
Veit Bücklein
Roland Reibke
Friederike Mumm
Christina T. Rieger
Wolfgang Hill
Georg Ledderose
Hans Joachim Stemmler
Thomas Köhnke
Gundula Jäger
Hans Jochem Kolb
Christoph Schmid
Andreas Moosmann
Andreas Hausmann
Publication date: 01-10-2015
Publisher: Springer Berlin Heidelberg
Published in: Annals of Hematology / Issue 10/2015
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI: https://doi.org/10.1007/s00277-015-2423-y

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Virus infection in HLA-haploidentical hematopoietic stem cell transplantation: incidence in the context of immune recovery in two different transplantation settings

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