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Allogeneic hematopoietic stem cell transplantation for intermediate-risk acute myeloid leukemia in the first remission: outcomes using haploidentical donors are similar to those using matched siblings


Allogeneic hematopoietic stem cell transplantation (allo-HSCT) is an effective and curative treatment for acute myeloid leukemia (AML). We explored the outcome of haploidentical donor (HID) transplantation for intermediate-risk AML and compared to that of matched sibling donor (MSD) transplants. One hundred twenty-seven consecutive patients with intermediate-risk AML in the first complete remission (CR1) who underwent allo-HSCT between January 1, 2015, and August 1, 2016, were enrolled. Thirty-seven patients received MSD grafts, and 90 received HID grafts. The 2-year leukemia-free survival (LFS) of the HID group was comparable to that of the MSD group: 82.0% ± 4.1% versus 82.7% ± 6.4%, P = 0.457. The 2-year cumulative incidences of relapse and transplantation-related mortality (TRM) were comparable between the HID and MSD groups (relapse, 4.5% ± 0.1%, versus 11.5% ± 0.3%, P = 0.550; TRM, 13.4% ± 0.1% vs. 5.8% ± 0.2%, P = 0.154). The HID recipients had a trend of a lower 2-year cumulative incidence of positive posttransplant flow cytometry (FCM+) and relapse than the MSD recipients (5.6% ± 0.1% vs. 19.9% ± 0.5%, P = 0.092). These results suggest that the outcomes of allo-HSCT with HIDs are comparable to those with MSDs in terms of LFS, TRM, and relapse for intermediate-risk AML in CR1. HIDs could be an alternative to MSDs for intermediate-risk AML.

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  1. 1.

    D’Souza A, Lee S, Zhu X, Pasquini M (2017) Current use and trends in hematopoietic cell transplantation in the United States. Biol Blood Marrow Transplant 23(9):1417–1421

    Article  Google Scholar 

  2. 2.

    Passweg JR, Baldomero H, Bader P et al (2017) Use of haploidentical stem cell transplantation continues to increase: the 2015 European Society for Blood and Marrow Transplant activity survey report. Bone Marrow Transplant 52(6):811–817

    CAS  Article  Google Scholar 

  3. 3.

    Xu L, Chen H, Chen J, Han M, Huang H, Lai Y, Liu D, Liu Q, Liu T, Jiang M, Ren H, Song Y, Sun Z, Wang J, Wu D, Zhou D, Zou P, Liu K, Huang X (2018) The consensus on indications, conditioning regimen, and donor selection of allogeneic hematopoietic cell transplantation for hematological diseases in China-recommendations from the Chinese Society of Hematology. J Hematol Oncol 11(1):33

    Article  Google Scholar 

  4. 4.

    Dohner H, Estey E, Grimwade D et al (2017) Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood. 129(4):424–447

    Article  Google Scholar 

  5. 5. Accessed Feb 1, 2019

  6. 6.

    Burnett AK, Wheatley K, Goldstone AH, Stevens RF, Hann IM, Rees JHK, Harrison G, the Medical Research Council Adult and Paediatric Working Parties (2002) The value of allogeneic bone marrow transplant in patients with acute myeloid leukaemia at differing risk of relapse: results of the UK MRC AML 10 trial. Br J Haematol 118(2):385–400

    Article  Google Scholar 

  7. 7.

    Huang XJ, Zhu HH, Chang YJ, Xu LP, Liu DH, Zhang XH, Jiang B, Jiang Q, Jiang H, Chen YH, Chen H, Han W, Liu KY, Wang Y (2012) The superiority of haploidentical related stem cell transplantation over chemotherapy alone as postremission treatment for patients with intermediate- or high-risk acute myeloid leukemia in first complete remission. Blood. 119(23):5584–5590

    CAS  Article  Google Scholar 

  8. 8.

    Lv M, Wang Y, Chang Y-J, Zhang XH, Xu LP, Jiang Q, Jiang H, Lu J, Chen H, Han W, Wang FR, Wang JZ, Chen Y, Yan CH, Zhang YY, Sun YQ, Mo XD, Zhu HH, Jia JS, Zhao T, Wang J, Liu KY, Huang XJ (2019) Myeloablative haploidentical transplantation is superior to chemotherapy for patients with intermediate-risk acute myelogenous leukemia in first complete remission. Clin Cancer Res 25(6):1737–1748

    CAS  Article  Google Scholar 

  9. 9.

    Cornelissen JJ, van Putten WL, Verdonck LF et al (2007) Results of a HOVON/SAKK donor versus no-donor analysis of myeloablative HLA-identical sibling stem cell transplantation in first remission acute myeloid leukemia in young and middle-aged adults: benefits for whom? Blood. 109(9):3658–3666

    CAS  Article  Google Scholar 

  10. 10.

    Koreth J, Schlenk R, Kopecky KJ, Honda S, Sierra J, Djulbegovic BJ, Wadleigh M, DeAngelo DJ, Stone RM, Sakamaki H, Appelbaum FR, Döhner H, Antin JH, Soiffer RJ, Cutler C (2009) Allogeneic stem cell transplantation for acute myeloid leukemia in first complete remission: systematic review and meta-analysis of prospective clinical trials. Jama. 301(22):2349–2361

    CAS  Article  Google Scholar 

  11. 11.

    Wang Y, Liu QF, Xu LP, Liu KY, Zhang XH, Ma X, Fan ZP, Wu DP, Huang XJ (2015) Haploidentical vs identical-sibling transplant for AML in remission: a multicenter, prospective study. Blood. 125(25):3956–3962

    CAS  Article  Google Scholar 

  12. 12.

    Salvatore D, Labopin M, Ruggeri A et al (2018) Outcomes of hematopoietic stem cell transplantation from unmanipulated haploidentical versus matched sibling donor in patients with acute myeloid leukemia in first complete remission with intermediate or high-risk cytogenetics: a study from the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation. Haematologica. 103(8):1317–1328

    CAS  Article  Google Scholar 

  13. 13.

    Ciurea SO, Zhang M-J, Bacigalupo AA, Bashey A, Appelbaum FR, Aljitawi OS, Armand P, Antin JH, Chen J, Devine SM, Fowler DH, Luznik L, Nakamura R, O’Donnell PV, Perales MA, Pingali SR, Porter DL, Riches MR, Ringdén OTH, Rocha V, Vij R, Weisdorf DJ, Champlin RE, Horowitz MM, Fuchs EJ, Eapen M (2015) Haploidentical transplant with post-transplant cyclophosphamide versus matched unrelated donor transplant for acute myeloid leukemia. Blood. 126(8):1033–1040

    CAS  Article  Google Scholar 

  14. 14.

    McCurdy SR, Kasamon YL, Kanakry CG et al (2017) Comparable composite endpoints after HLA-matched and HLA-haploidentical transplantation with post-transplantation cyclophosphamide. Haematologica. 102(2):391–400

    CAS  Article  Google Scholar 

  15. 15.

    Bashey A, Zhang X, Sizemore CA et al (2011) T-cell replete haploidentical transplantation using post-transplant cyclophosphamide results in equivalent non-relapse mortality and disease-free survival compared to transplantation from HLA-identical sibling and matched unrelated donors: a stratified cox model analysis of two hundred and sixty contemporaneous allogeneic transplants from a single center. Blood. 118(21):833–833

    Article  Google Scholar 

  16. 16.

    Raiola AM, Dominietto A, di Grazia C, Lamparelli T, Gualandi F, Ibatici A, Bregante S, van Lint MT, Varaldo R, Ghiso A, Gobbi M, Carella AM, Signori A, Galaverna F, Bacigalupo A (2014) Unmanipulated haploidentical transplants compared with other alternative donors and matched sibling grafts. Biol Blood Marrow Transplant 20(10):1573–1579

    Article  Google Scholar 

  17. 17.

    Versluis J, Labopin M, Ruggeri A, Socie G, Wu D, Volin L, Blaise D, Milpied N, Craddock C, Yakoub-Agha I, Maertens J, Ljungman P, Huynh A, Michallet M, Deconinck E, Chevallier P, Passweg J, Ciceri F, Mohty M, Cornelissen JJ, Nagler A (2017) Alternative donors for allogeneic hematopoietic stem cell transplantation in poor-risk AML in CR1. Blood Adv 1(7):477–485

    CAS  Article  Google Scholar 

  18. 18.

    Wang Y, Chang YJ, Chen L, Xu LP, Bian ZL, Zhang XH, Yan CH, Liu KY, Huang XJ (2017) Low-dose post-transplant cyclophosphamide can mitigate GVHD and enhance the G-CSF/ATG induced GVHD protective activity and improve haploidentical transplant outcomes. Oncoimmunology. 6(11):e1356152

    Article  Google Scholar 

  19. 19.

    Wang Y, Liu DH, Liu KY, Xu LP, Zhang XH, Han W, Chen H, Chen YH, Wang FR, Wang JZ, Sun YQ, Huang XJ (2013) Long-term follow-up of haploidentical hematopoietic stem cell transplantation without in vitro T cell depletion for the treatment of leukemia: nine years of experience at a single center. Cancer. 119(5):978–985

    Article  Google Scholar 

  20. 20.

    Huang X-J, Liu D-H, Liu K-Y, Xu LP, Chen H, Han W, Chen YH, Wang JZ, Gao ZY, Zhang YC, Jiang Q, Shi HX, Lu DP (2006) Haploidentical hematopoietic stem cell transplantation without in vitro T-cell depletion for the treatment of hematological malignancies. Bone Marrow Transplant 38(4):291–297

    Article  Google Scholar 

  21. 21.

    Huang XJ, Liu DH, Liu KY, Xu LP, Chen H, Han W, Chen YH, Zhang XH, Lu DP (2009) Treatment of acute leukemia with unmanipulated HLA-mismatched/haploidentical blood and bone marrow transplantation. Biol Blood Marrow Transplant 15(2):257–265

    CAS  Article  Google Scholar 

  22. 22.

    Mo XD, Zhang XH, Xu LP, Wang Y, Yan CH, Chen H, Chen YH, Han W, Wang FR, Wang JZ, Liu KY, Huang XJ (2017) Haploidentical hematopoietic stem cell transplantation for myelodysplastic syndrome. Biol Blood Marrow Transplant 23(12):2143–2150

    Article  Google Scholar 

  23. 23.

    Yan CH, Liu DH, Liu KY, Xu LP, Liu YR, Chen H, Han W, Wang Y, Qin YZ, Huang XJ (2012) Risk stratification-directed donor lymphocyte infusion could reduce relapse of standard-risk acute leukemia patients after allogeneic hematopoietic stem cell transplantation. Blood. 119(14):3256–3262

    CAS  Article  Google Scholar 

  24. 24.

    Yan CH, Wang Y, Wang JZ et al (2016) Minimal residual disease- and graft-vs.-host disease-guided multiple consolidation chemotherapy and donor lymphocyte infusion prevent second acute leukemia relapse after allotransplant. J Hematol Oncol 9(1):87

    Article  Google Scholar 

  25. 25.

    Wang Y, Chen H, Chen J, Han M, Hu JD, Jiong Hu, Huang H, Lai Y, Liu D, Liu Q, Liu T, Jiang M, Ren H, Song Y, Sun Z, Wang C, Wang J, Wu D, Xu K, Zhang X, Xu L, Liu K, Huang X (2018) The consensus on the monitoring, treatment, and prevention of leukemia relapse after allogeneic hematopoietic stem cell transplantation in China. Cancer Lett 438:63–75

    CAS  Article  Google Scholar 

  26. 26.

    Holtan SG, DeFor TE, Lazaryan A et al (2015) Composite end point of graft-versus-host disease-free, relapse-free survival after allogeneic hematopoietic cell transplantation. Blood. 125(8):1333–1338

    CAS  Article  Google Scholar 

  27. 27.

    Di Stasi A, Milton DR, Poon LM et al (2014) Similar transplantation outcomes for acute myeloid leukemia and myelodysplastic syndrome patients with haploidentical versus 10/10 human leukocyte antigen-matched unrelated and related donors. Biol Blood Marrow Transplant 20(12):1975–1981

    Article  Google Scholar 

  28. 28.

    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

    CAS  Article  Google Scholar 

  29. 29.

    Yoon JH, Kim HJ, Park SS, Jeon YW, Lee SE, Cho BS, Eom KS, Kim YJ, Lee S, Min CK, Cho SG, Kim DW, Lee JW, Min WS (2017) Long-term clinical outcomes of hematopoietic cell transplantation for intermediate-to-poor-risk acute myeloid leukemia during first remission according to available donor types. Oncotarget. 8(25):41590–41604

    Article  Google Scholar 

  30. 30.

    Ringden O, Labopin M, Ciceri F et al (2016) Is there a stronger graft-versus-leukemia effect using HLA-haploidentical donors compared with HLA-identical siblings? Leukemia. 30(2):447–455

    CAS  Article  Google Scholar 

  31. 31.

    Wang Y, Liu DH, Xu LP, Liu KY, Chen H, Chen YH, Han W, Shi HX, Huang XJ (2011) Superior graft-versus-leukemia effect associated with transplantation of haploidentical compared with HLA-identical sibling donor grafts for high-risk acute leukemia: an historic comparison. Biol Blood Marrow Transplant 17(6):821–830

    Article  Google Scholar 

  32. 32.

    Yu S, Fan Q, Sun J, Fan Z, Zhang Y, Jiang Q, Huang F, Xuan L, Dai M, Zhou H, Liu H, Liu QF (2016) Haploidentical transplantation without in vitro T-cell depletion results in outcomes equivalent to those of contemporaneous matched sibling and unrelated donor transplantation for acute leukemia. Medicine. 95(11):e2973

    CAS  Article  Google Scholar 

  33. 33.

    Mo XD, Zhang XH, Xu LP, Wang Y, Yan CH, Chen H, Chen YH, Han W, Wang FR, Wang JZ, Liu KY, Huang XJ (2017) IFN-alpha is effective for treatment of minimal residual disease in patients with acute leukemia after allogeneic hematopoietic stem cell transplantation: results of a registry study. Biol Blood Marrow Transplant 23(8):1303–1310

    CAS  Article  Google Scholar 

  34. 34.

    Mo XD, Xu LP, Liu DH, Chen YH, Han W, Zhang XH, Chen H, Wang Y, Wang JZ, Liu KY, Huang XJ (2012) Patients receiving HLA-haploidentical/partially matched related Allo-HSCT can achieve desirable health-related QoL that is comparable to that of patients receiving HLA-identical sibling Allo-HSCT. Bone Marrow Transplant 47(9):1201–1205

    Article  Google Scholar 

  35. 35.

    Wang Y, Wang HX, Lai YR, Sun ZM, Wu DP, Jiang M, Liu DH, Xu KL, Liu QF, Liu L, Wang JB, Gao F, Ou-Yang J, Gao SJ, Xu LP, Huang XJ (2016) Haploidentical transplant for myelodysplastic syndrome: registry-based comparison with identical sibling transplant. Leukemia. 30(10):2055–2063

    CAS  Article  Google Scholar 

  36. 36.

    Randolph SS, Gooley TA, Warren EH, Appelbaum FR, Riddell SR (2004) Female donors contribute to a selective graft-versus-leukemia effect in male recipients of HLA-matched, related hematopoietic stem cell transplants. Blood. 103(1):347–352

    CAS  Article  Google Scholar 

  37. 37.

    Chang YJ, Luznik L, Fuchs EJ, Huang XJ (2016) How do we choose the best donor for T-cell-replete, HLA-haploidentical transplantation? J Hematol Oncol 9:35

    Article  Google Scholar 

  38. 38.

    Wang Y, Wu DP, Liu QF, Xu LP, Liu KY, Zhang XH, Xu Y, Huang F, Huang XJ (2018) Donor and recipient age, gender and ABO incompatibility regardless of donor source: validated criteria for donor selection for haematopoietic transplants. Leukemia. 32(2):492–498

    CAS  Article  Google Scholar 

  39. 39.

    Jagasia M, Arora M, Flowers ME et al (2012) Risk factors for acute GVHD and survival after hematopoietic cell transplantation. Blood. 119(1):296–307

    CAS  Article  Google Scholar 

  40. 40.

    Chen Y, Wang Y, Xu LP, Liu KY, Chen H, Chen YH, Zhang XH, Wang FR, Han W, Wang JZ, Yan CH, Zhang YY, Sun YQ, Huang XJ (2015) Haploidentical stem cell transplantation in patients aged 50 yr and older with leukemia: similar outcomes compared to younger adults. Clin Transpl 29(6):523–530

    Article  Google Scholar 

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We thank the principal investigators and the skilled teams at each of the participating sites. We thank all colleagues for participating in the research.


This work was supported by the National Natural Science Foundation of China (grant no. 81770189, 82070189), the National Key Research and Development Program of China (2019YFC0840606) from the Ministry of Science and Technology, the Science and Technology Project of Guangdong Province of China 2016B030230003, the project of health collaborative innovation of Guangzhou city (no. 201704020214).

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Correspondence to Yu Wang.

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Ma, YR., Xu, LP., Zhang, XH. et al. Allogeneic hematopoietic stem cell transplantation for intermediate-risk acute myeloid leukemia in the first remission: outcomes using haploidentical donors are similar to those using matched siblings. Ann Hematol 100, 555–562 (2021).

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  • Haploidentical donor
  • Matched sibling donor
  • Intermediate-risk
  • Acute myeloid leukemia