Second unmanipulated allogeneic transplantation could be used as a salvage option for patients with relapsed acute leukemia post-chemotherapy plus modified donor lymphocyte infusion

Tingting Han, Yuqian Sun, Yang Liu, Chenhua Yan, Yu Wang, Lanping Xu, Kaiyan Liu, Xiaojun Huang, Xiaohui Zhang

PDF(376 KB)
PDF(376 KB)
Front. Med. ›› 2021, Vol. 15 ›› Issue (5) : 728-739. DOI: 10.1007/s11684-021-0833-x
RESEARCH ARTICLE
RESEARCH ARTICLE

Second unmanipulated allogeneic transplantation could be used as a salvage option for patients with relapsed acute leukemia post-chemotherapy plus modified donor lymphocyte infusion

Author information +
History +

Abstract

Relapse is the main problem after allogeneic hematopoietic stem cell transplantation (allo-HSCT). The outcome of a second allo-HSCT (HSCT2) for relapse post-HSCT has shown promising results in some previous studies. However, little is known about the efficacy of HSCT2 in patients with relapsed/refractory acute leukemia (AL) post-chemotherapy plus modified donor lymphocyte infusion (post-Chemo+m-DLI) after the first allo-HSCT (HSCT1). Therefore, we retrospectively analyzed the efficacy of HSCT2 in 28 patients with relapsed/refractory AL post-Chemo+m-DLI in our center. With a median follow-up of 918 (457–1732) days, 26 patients (92.9%) achieved complete remission, and 2 patients exhibited persistent disease. The probabilities of overall survival (OS) and disease-free survival (DFS) 1 year after HSCT2 were 25.0% and 21.4%, respectively. The cumulative incidences of nonrelapse mortality on day 100 and at 1 year post-HSCT2 were 7.1%±4.9% and 25.0%±8.4%. The cumulative incidences of relapse were 50.0%±9.8% and 53.5%±9.9% at 1 and 2 years post-HSCT2, respectively. Risk stratification prior to HSCT1 and percentage of blasts before HSCT2 were independent risk factors for OS post-HSCT2, and relapse within 6 months post-HSCT1 was an independent risk factor for DFS and relapse post-HSCT2. Our findings suggest that HSCT2 could be a salvage option for patients with relapsed AL post-Chemo+m-DLI.

Keywords

second hematopoietic stem cell transplantation / acute leukemia / relapse / chemotherapy / modified donor lymphocyte infusion

Cite this article

Download citation ▾
Tingting Han, Yuqian Sun, Yang Liu, Chenhua Yan, Yu Wang, Lanping Xu, Kaiyan Liu, Xiaojun Huang, Xiaohui Zhang. Second unmanipulated allogeneic transplantation could be used as a salvage option for patients with relapsed acute leukemia post-chemotherapy plus modified donor lymphocyte infusion. Front. Med., 2021, 15(5): 728‒739 https://doi.org/10.1007/s11684-021-0833-x

References

[1]
Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med 2006; 354(17): 1813–1826
CrossRef Pubmed Google scholar
[2]
Wang Y, Liu QF, Xu LP, Liu KY, Zhang XH, Ma X, Fan ZP, Wu DP, Huang XJ. Haploidentical vs identical-sibling transplant for AML in remission: a multicenter, prospective study. Blood 2015; 125(25): 3956–3962
CrossRef Pubmed Google scholar
[3]
Kanakry CG, Fuchs EJ, Luznik L. Modern approaches to HLA-haploidentical blood or marrow transplantation. Nat Rev Clin Oncol 2016; 13(1): 10–24
CrossRef Pubmed Google scholar
[4]
Yan CH, Liu DH, Liu KY, Xu LP, Liu YR, Chen H, Han W, Wang Y, Qin YZ, Huang XJ. Risk stratification-directed donor lymphocyte infusion could reduce relapse of standard-risk acute leukemia patients after allogeneic hematopoietic stem cell transplantation. Blood 2012; 119(14): 3256–3262
CrossRef Pubmed Google scholar
[5]
Chang YJ, Wang Y, Huang XJ. Haploidentical stem cell transplantation for the treatment of leukemia: current status. Expert Rev Hematol 2014; 7(5): 635–647
CrossRef Pubmed Google scholar
[6]
Oran B, de Lima M. Prevention and treatment of acute myeloid leukemia relapse after allogeneic stem cell transplantation. Curr Opin Hematol 2011; 18(6): 388–394
CrossRef Pubmed Google scholar
[7]
Mielcarek M, Storer BE, Flowers ME, Storb R, Sandmaier BM, Martin PJ. Outcomes among patients with recurrent high-risk hematologic malignancies after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant 2007; 13(10): 1160–1168
CrossRef Pubmed Google scholar
[8]
Levine JE, Braun T, Penza SL, Beatty P, Cornetta K, Martino R, Drobyski WR, Barrett AJ, Porter DL, Giralt S, Leis J, Holmes HE, Johnson M, Horowitz M, Collins RH Jr. Prospective trial of chemotherapy and donor leukocyte infusions for relapse of advanced myeloid malignancies after allogeneic stem-cell transplantation. J Clin Oncol 2002; 20(2): 405–412
CrossRef Pubmed Google scholar
[9]
Choi SJ, Lee JH, Lee JH, Kim S, Seol M, Lee YS, Lee JS, Kim WK, Chi HS, Lee KH. Treatment of relapsed acute myeloid leukemia after allogeneic bone marrow transplantation with chemotherapy followed by G-CSF-primed donor leukocyte infusion: a high incidence of isolated extramedullary relapse. Leukemia 2004; 18(11): 1789–1797
CrossRef Pubmed Google scholar
[10]
Schmid C, Labopin M, Nagler A, Bornhäuser M, Finke J, Fassas A, Volin L, Gürman G, Maertens J, Bordigoni P, Holler E, Ehninger G, Polge E, Gorin NC, Kolb HJ, Rocha V; EBMT Acute Leukemia Working Party. Donor lymphocyte infusion in the treatment of first hematological relapse after allogeneic stem-cell transplantation in adults with acute myeloid leukemia: a retrospective risk factors analysis and comparison with other strategies by the EBMT Acute Leukemia Working Party. J Clin Oncol 2007; 25(31): 4938–4945
CrossRef Pubmed Google scholar
[11]
Lübbert M, Bertz H, Wäsch R, Marks R, Rüter B, Claus R, Finke J. Efficacy of a 3-day, low-dose treatment with 5-azacytidine followed by donor lymphocyte infusions in older patients with acute myeloid leukemia or chronic myelomonocytic leukemia relapsed after allografting. Bone Marrow Transplant 2010; 45(4): 627–632
CrossRef Pubmed Google scholar
[12]
Huang XJ, Liu DH, Liu KY, Xu LP, Chen H, Han W. Donor lymphocyte infusion for the treatment of leukemia relapse after HLA-mismatched/haploidentical T-cell-replete hematopoietic stem cell transplantation. Haematologica 2007; 92(3): 414–417
CrossRef Pubmed Google scholar
[13]
Michallet M, Tanguy ML, Socié G, Thiébaut A, Belhabri A, Milpied N, Reiffers J, Kuentz M, Cahn JY, Blaise D, Demeocq F, Jouet JP, Michallet AS, Ifrah N, Vilmer E, Molina L, Michel G, Lioure B, Cavazzana-Calvo M, Pico JL, Sadoun A, Guyotat D, Attal M, Curé H, Bordigoni P, Sutton L, Buzyn-Veil A, Tilly M, Keoirruer N, Feguex N. Second allogeneic haematopoietic stem cell transplantation in relapsed acute and chronic leukaemias for patients who underwent a first allogeneic bone marrow transplantation: a survey of the Société Française de Greffe de moelle (SFGM). Br J Haematol 2000; 108(2): 400–407
CrossRef Pubmed Google scholar
[14]
Tomonari A, Iseki T, Ooi J, Nagayama H, Sato H, Takahashi T, Ito K, Nagamura F, Uchimaru K, Takahashi S, Shirafuji N, Tojo A, Tani K, Asano S. Second allogeneic hematopoietic stem cell transplantation for leukemia relapse after first allogeneic transplantation: outcome of 16 patients in a single institution. Int J Hematol 2002; 75(3): 318–323
CrossRef Pubmed Google scholar
[15]
Tsirigotis P, Byrne M, Schmid C, Baron F, Ciceri F, Esteve J, Gorin NC, Giebel S, Mohty M, Savani BN, Nagler A. Relapse of AML after hematopoietic stem cell transplantation: methods of monitoring and preventive strategies. A review from the ALWP of the EBMT. Bone Marrow Transplant 2016; 51(11): 1431–1438
CrossRef Pubmed Google scholar
[16]
Yan CH, Wang Y, Wang JZ, Chen YH, Chen Y, Wang FR, Sun YQ, Mo XD, Han W, Chen H, Zhang XH, Xu LP, Liu KY, Huang XJ. 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 2016; 9(1): 87
CrossRef Pubmed Google scholar
[17]
Yan CH, Wang JZ, Liu DH, Xu LP, Chen H, Liu KY, Huang XJ. Chemotherapy followed by modified donor lymphocyte infusion as a treatment for relapsed acute leukemia after haploidentical hematopoietic stem cell transplantation without in vitro T-cell depletion: superior outcomes compared with chemotherapy alone and an analysis of prognostic factors. Eur J Haematol 2013; 91(4): 304–314
CrossRef Pubmed Google scholar
[18]
Miyamoto T, Fukuda T, Nakashima M, Henzan T, Kusakabe S, Kobayashi N, Sugita J, Mori T, Kurokawa M, Mori SI. Donor lymphocyte infusion for relapsed hematological malignancies after unrelated allogeneic bone marrow transplantation facilitated by the japan marrow donor program. Biol Blood Marrow Transplant 2017; 23(6): 938–944
CrossRef Pubmed Google scholar
[19]
Ruutu T, de Wreede LC, van Biezen A, Brand R, Mohty M, Dreger P, Duarte R, Peters C, Garderet L, Schönland S, Gratwohl A, Niederwieser D, de Witte T, Kröger N; European Society for Blood and Marrow Transplantation (EBMT). Second allogeneic transplantation for relapse of malignant disease: retrospective analysis of outcome and predictive factors by the EBMT. Bone Marrow Transplant 2015; 50(12): 1542–1550
CrossRef Pubmed Google scholar
[20]
Vrhovac R, Labopin M, Ciceri F, Finke J, Holler E, Tischer J, Lioure B, Gribben J, Kanz L, Blaise D, Dreger P, Held G, Arnold R, Nagler A, Mohty M; Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation (EBMT). Second reduced intensity conditioning allogeneic transplant as a rescue strategy for acute leukaemia patients who relapse after an initial RIC allogeneic transplantation: analysis of risk factors and treatment outcomes. Bone Marrow Transplant 2016; 51(2): 186–193
CrossRef Pubmed Google scholar
[21]
Huang XJ, Liu DH, Liu KY, Xu LP, Chen H, Han W, Chen YH, Wang JZ, Gao ZY, Zhang YC, Jiang Q, Shi HX, Lu DP. Haploidentical hematopoietic stem cell transplantation without in vitro T-cell depletion for the treatment of hematological malignancies. Bone Marrow Transplant 2006; 38(4): 291–297
CrossRef Pubmed Google scholar
[22]
Huang XJ, Liu DH, Liu KY, Xu LP, Chen H, Han W, Chen YH, Zhang XH, Lu DP. Treatment of acute leukemia with unmanipulated HLA-mismatched/haploidentical blood and bone marrow transplantation. Biol Blood Marrow Transplant 2009; 15(2): 257–265
CrossRef Pubmed Google scholar
[23]
Yan CH, Liu QF, Wu DP, Zhang X, Xu LP, Zhang XH, Wang Y, Huang H, Bai H, Huang F, Ma X, Huang XJ. Prophylactic donor lymphocyte infusion (DLI) followed by minimal residual disease and graft-versus-host disease-guided multiple DLIs could improve outcomes after allogeneic hematopoietic stem cell transplantation in patients with refractory/relapsed acute leukemia. Biol Blood Marrow Transplant 2017; 23(8): 1311–1319
CrossRef Pubmed Google scholar
[24]
Huang XJ, Wang Y, Liu DH, Xu LP, Chen H, Chen YH, Han W, Shi HX, Liu KY. Modified donor lymphocyte infusion (DLI) for the prophylaxis of leukemia relapse after hematopoietic stem cell transplantation in patients with advanced leukemia—feasibility and safety study. J Clin Immunol 2008; 28(4): 390–397
CrossRef Pubmed Google scholar
[25]
Brüggemann M, Kotrova M. Minimal residual disease in adult ALL: technical aspects and implications for correct clinical interpretation. Blood Adv 2017; 1(25): 2456–2466
CrossRef Pubmed Google scholar
[26]
Wang Y, Chen H, Chen J, Han M, Hu J, 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. The consensus on the monitoring, treatment, and prevention of leukemia relapse after allogeneic hematopoietic stem cell transplantation in China. Cancer Lett 2018; 438: 63–75
CrossRef Pubmed Google scholar
[27]
Przepiorka D, Nath R, Ippoliti C, Mehra R, Hagemeister F, Diener K, Dimopoulos M, Giralt S, Khouri I, Samuels B, . A phase I–II study of high-dose thiotepa, busulfan and cyclophosphamide as a preparative regimen for autologous transplantation for malignant lymphoma. Leuk Lymphoma 1995; 17(5–6): 427–433
CrossRef Pubmed Google scholar
[28]
Glucksberg H, Storb R, Fefer A, Buckner CD, Neiman PE, Clift RA, Lerner KG, Thomas ED. Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation 1974; 18(4): 295–304
CrossRef Pubmed Google scholar
[29]
Eapen M, Giralt SA, Horowitz MM, Klein JP, Wagner JE, Zhang MJ, Tallman MS, Marks DI, Camitta BM, Champlin RE, Ringdén O, Bredeson CN, Martino R, Gale RP, Cairo MS, Litzow MR, deLima M. Second transplant for acute and chronic leukemia relapsing after first HLA-identical sibling transplant. Bone Marrow Transplant 2004; 34(8): 721–727
CrossRef Pubmed Google scholar
[30]
Duncan CN, Majhail NS, Brazauskas R, Wang Z, Cahn JY, Frangoul HA, Hayashi RJ, Hsu JW, Kamble RT, Kasow KA, Khera N, Lazarus HM, Loren AW, Marks DI, Maziarz RT, Mehta P, Myers KC, Norkin M, Pidala JA, Porter DL, Reddy V, Saber W, Savani BN, Schouten HC, Steinberg A, Wall DA, Warwick AB, Wood WA, Yu LC, Jacobsohn DA, Sorror ML. Long-term survival and late effects among one-year survivors of second allogeneic hematopoietic cell transplantation for relapsed acute leukemia and myelodysplastic syndromes. Biol Blood Marrow Transplant 2015; 21(1): 151–158
CrossRef Pubmed Google scholar
[31]
Al-Qurashi F, Ayas M, Al Sharif F, Ibrahim E, Sahovic E, Al Mahr M, Chaudhri N, Al Mohareb F, Al Zahrani H, Al Jefri A, Al Omar H, Al Shanqeeti A, Seth P, Aslam M, El Solh H, Aljurf M. Second allogeneic bone marrow transplantation after myeloablative conditioning analysis of 43 cases from single institution. Hematology 2004; 9(2): 123–129
CrossRef Pubmed Google scholar
[32]
Pawson R, Potter MN, Theocharous P, Lawler M, Garg M, Yin JA, Rezvani K, Craddock C, Rassam S, Prentice HG. Treatment of relapse after allogeneic bone marrow transplantation with reduced intensity conditioning (FLAG± Ida) and second allogeneic stem cell transplant. Br J Haematol 2001; 115(3): 622–629
CrossRef Pubmed Google scholar
[33]
Shaw BE, Mufti GJ, Mackinnon S, Cavenagh JD, Pearce RM, Towlson KE, Apperley JF, Chakraverty R, Craddock CF, Kazmi MA, Littlewood TJ, Milligan DW, Pagliuca A, Thomson KJ, Marks DI, Russell NH. Outcome of second allogeneic transplants using reduced-intensity conditioning following relapse of haematological malignancy after an initial allogeneic transplant. Bone Marrow Transplant 2008; 42(12): 783–789
CrossRef Pubmed Google scholar
[34]
Zeidan AM, Forde PM, Symons H, Chen A, Smith BD, Pratz K, Carraway H, Gladstone DE, Fuchs EJ, Luznik L, Jones RJ, Bolaños-Meade J. HLA-haploidentical donor lymphocyte infusions for patients with relapsed hematologic malignancies after related HLA-haploidentical bone marrow transplantation. Biol Blood Marrow Transplant 2014; 20(3): 314–318
CrossRef Pubmed Google scholar
[35]
Goldsmith SR, Slade M, DiPersio JF, Westervelt P, Schroeder MA, Gao F, Romee R. Donor-lymphocyte infusion following haploidentical hematopoietic cell transplantation with peripheral blood stem cell grafts and PTCy. Bone Marrow Transplant 2017; 52(12): 1623–1628
CrossRef Pubmed Google scholar
[36]
Bejanyan N, Weisdorf DJ, Logan BR, Wang HL, Devine SM, de Lima M, Bunjes DW, Zhang MJ. Survival of patients with acute myeloid leukemia relapsing after allogeneic hematopoietic cell transplantation: a center for international blood and marrow transplant research study. Biol Blood Marrow Transplant 2015; 21(3): 454–459
CrossRef Pubmed Google scholar
[37]
Christopeit M, Kuss O, Finke J, Bacher U, Beelen DW, Bornhäuser M, Schwerdtfeger R, Bethge WA, Basara N, Gramatzki M, Tischer J, Kolb HJ, Uharek L, Meyer RG, Bunjes D, Scheid C, Martin H, Niederwieser D, Kröger N, Bertz H, Schrezenmeier H, Schmid C. Second allograft for hematologic relapse of acute leukemia after first allogeneic stem-cell transplantation from related and unrelated donors: the role of donor change. J Clin Oncol 2013; 31(26): 3259–3271
CrossRef Pubmed Google scholar
[38]
Horstmann K, Boumendil A, Finke J, Finel H, Kanfer E, Milone G, Russell N, Bacigalupo A, Chalandon Y, Diez-Martin JL, Ifrah N, Chacon MJ, Dreger P. Second allo-SCT in patients with lymphoma relapse after a first allogeneic transplantation. A retrospective study of the EBMT Lymphoma Working Party. Bone Marrow Transplant 2015; 50(6): 790–794
CrossRef Pubmed Google scholar
[39]
Meshinchi S, Leisenring WM, Carpenter PA, Woolfrey AE, Sievers EL, Radich JP, Sanders JE. Survival after second hematopoietic stem cell transplantation for recurrent pediatric acute myeloid leukemia. Biol Blood Marrow Transplant 2003; 9(11): 706–713
CrossRef Pubmed Google scholar
[40]
Bosi A, Laszlo D, Labopin M, Reffeirs J, Michallet M, Gluckman E, Alessandrino PE, Locatelli F, Vernant JP, Sierra J, Jouet JP, Frassoni F; Acute Leukemia Working Party of the European Blood and Marrow Transplant Group. Second allogeneic bone marrow transplantation in acute leukemia: results of a survey by the European Cooperative Group for Blood and Marrow Transplantation. J Clin Oncol 2001; 19(16): 3675–3684
CrossRef Pubmed Google scholar
[41]
Keil F, Prinz E, Kalhs P, Lechner K, Moser K, Schwarzinger I, Jäger U, Fonatsch C, Worel N, Mannhalter C, Rabitsch W, Loidolt H, Schulenburg A, Mitterbauer M, Höcker P, Greinix HT. Treatment of leukemic relapse after allogeneic stem cell transplantation with cytotoreductive chemotherapy and/or immunotherapy or second transplants. Leukemia 2001; 15(3): 355–361
CrossRef Pubmed Google scholar
[42]
Blau IW, Basara N, Bischoff M, Günzelmann S, Römer E, Kirsten D, Schmetzer B, Kiehl MG, Fauser AA. Second allogeneic hematopoietic stem cell transplantation as treatment for leukemia relapsing following a first transplant. Bone Marrow Transplant 2000; 25(1): 41–45
CrossRef Pubmed Google scholar
[43]
Radich JP, Sanders JE, Buckner CD, Martin PJ, Petersen FB, Bensinger W, McDonald GB, Mori M, Schoch G, Hansen JA. Second allogeneic marrow transplantation for patients with recurrent leukemia after initial transplant with total-body irradiation-containing regimens. J Clin Oncol 1993; 11(2): 304–313
CrossRef Pubmed Google scholar
[44]
Arellano ML, Langston A, Winton E, Flowers CR, Waller EK. Treatment of relapsed acute leukemia after allogeneic transplantation: a single center experience. Biol Blood Marrow Transplant 2007; 13(1): 116–123
CrossRef Pubmed Google scholar
[45]
Muñoz A, Badell I, Olivé T, Verdeguer A, Gómez P, Bureo E;Spanish Working Party for Bone Marrow Transplantation in Children (GETMON). Second allogeneic hematopoietic stem cell transplantation in hematologic malignancies in children: long-term results of a multicenter study of the Spanish Working Party for Bone Marrow Transplantation in Children (GETMON). Haematologica 2002; 87(3): 331–332
Pubmed
[46]
Kato M, Horikoshi Y, Okamoto Y, Takahashi Y, Hasegawa D, Koh K, Takita J, Inoue M, Kigasawa H, Ogawa A, Sasahara Y, Kawa K, Yabe H, Sakamaki H, Suzuki R, Kato K. Second allogeneic hematopoietic SCT for relapsed ALL in children. Bone Marrow Transplant 2012; 47(10): 1307–1311
CrossRef Pubmed Google scholar
[47]
McIver ZA, Yin F, Hughes T, Battiwalla M, Ito S, Koklanaris E, Haggerty J, Hensel NF, Barrett AJ. Second hematopoietic SCT for leukemia relapsing after myeloablative T cell-depleted transplants does not prolong survival. Bone Marrow Transplant 2013; 48(9): 1192–1197
CrossRef Pubmed Google scholar
[48]
Naik S, Martinez C, Leung K, Sasa G, Nguyen NY, Wu MF, Gottschalk S, Brenner M, Heslop H, Krance R. Outcomes after second hematopoietic stem cell transplantations in pediatric patients with relapsed hematological malignancies. Biol Blood Marrow Transplant 2015; 21(7): 1266–1272
CrossRef Pubmed Google scholar
[49]
Chueh HW, Lee SH, Sung KW, Yoo KH, Koo HH. Second allogeneic stem cell transplantation in hematologic malignancies: a single-center experience. J Pediatr Hematol Oncol 2013; 35(6): 424–429
CrossRef Pubmed Google scholar
[50]
Castagna L, Sarina B, Bramanti S, Perseghin P, Mariotti J, Morabito L. Donor lymphocyte infusion after allogeneic stem cell transplantation. Transfus Apheresis Sci 2016; 54(3): 345–355
CrossRef Pubmed Google scholar
[51]
Spyridonidis A, Labopin M, Schmid C, Volin L, Yakoub-Agha I, Stadler M, Milpied N, Socie G, Browne P, Lenhoff S, Sanz MA, Aljurf M, Mohty M, Rocha V; Immunotherapy Subcommittee of Acute Leukemia Working Party. Outcomes and prognostic factors of adults with acute lymphoblastic leukemia who relapse after allogeneic hematopoietic cell transplantation. An analysis on behalf of the Acute Leukemia Working Party of EBMT. Leukemia 2012; 26(6): 1211–1217
CrossRef Pubmed Google scholar
[52]
Brouwer RE, van der Heiden P, Schreuder GM, Mulder A, Datema G, Anholts JD, Willemze R, Claas FH, Falkenburg JH. Loss or downregulation of HLA class I expression at the allelic level in acute leukemia is infrequent but functionally relevant, and can be restored by interferon. Hum Immunol 2002; 63(3): 200–210
CrossRef Pubmed Google scholar
[53]
Choi SJ, Lee JH, Lee JH, Kim S, Lee YS, Seol M, Ryu SG, Lee JS, Kim WK, Jang S, Park CJ, Chi HS, Lee KH. Treatment of relapsed acute lymphoblastic leukemia after allogeneic bone marrow transplantation with chemotherapy followed by G-CSF-primed donor leukocyte infusion: a prospective study. Bone Marrow Transplant 2005; 36(2): 163–169
CrossRef Pubmed Google scholar
[54]
Deol A, Lum LG. Role of donor lymphocyte infusions in relapsed hematological malignancies after stem cell transplantation revisited. Cancer Treat Rev 2010; 36(7): 528–538
CrossRef Pubmed Google scholar
[55]
Hosing C, Saliba RM, Shahjahan M, Estey EH, Couriel D, Giralt S, Andersson B, Champlin RE, De Lima M. Disease burden may identify patients more likely to benefit from second allogeneic hematopoietic stem cell transplantation to treat relapsed acute myelogenous leukemia. Bone Marrow Transplant 2005; 36(2): 157–162
CrossRef Pubmed Google scholar
[56]
Imus PH, Blackford AL, Bettinotti M, Iglehart B, Dietrich A, Tucker N, Symons H, Cooke KR, Luznik L, Fuchs EJ, Brodsky RA, Matsui WH, Huff CA, Gladstone D, Ambinder RF, Borrello IM, Swinnen LJ, Jones RJ, Bolaños-Meade J. Major histocompatibility mismatch and donor choice for second allogeneic bone marrow transplantation. Biol Blood Marrow Transplant 2017; 23(11): 1887–1894
CrossRef Pubmed Google scholar
[57]
Schmid C, Schleuning M, Ledderose G, Tischer J, Kolb HJ. Sequential regimen of chemotherapy, reduced-intensity conditioning for allogeneic stem-cell transplantation, and prophylactic donor lymphocyte transfusion in high-risk acute myeloid leukemia and myelodysplastic syndrome. J Clin Oncol 2005; 23(24): 5675–5687
CrossRef Pubmed Google scholar
[58]
Schmid C, Schleuning M, Schwerdtfeger R, Hertenstein B, Mischak-Weissinger E, Bunjes D, Harsdorf SV, Scheid C, Holtick U, Greinix H, Keil F, Schneider B, Sandherr M, Bug G, Tischer J, Ledderose G, Hallek M, Hiddemann W, Kolb HJ. Long-term survival in refractory acute myeloid leukemia after sequential treatment with chemotherapy and reduced-intensity conditioning for allogeneic stem cell transplantation. Blood 2006; 108(3): 1092–1099
CrossRef Pubmed Google scholar
[59]
Saraceni F, Labopin M, Brecht A, Kröger N, Eder M, Tischer J, Labussière-Wallet H, Einsele H, Beelen D, Bunjes D, Niederwieser D, Bochtler T, Savani BN, Mohty M, Nagler A. Fludarabine-treosulfan compared to thiotepa-busulfan-fludarabine or FLAMSA as conditioning regimen for patients with primary refractory or relapsed acute myeloid leukemia: a study from the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation (EBMT). J Hematol Oncol 2019; 12(1): 44
CrossRef Pubmed Google scholar
[60]
Ram R, Scheid C, Amit O, Chemnitz JM, Moshe Y, Hallek M, Wolf D, Avivi I, Holtick U. Sequential therapy for patients with primary refractory acute myeloid leukemia: a historical prospective analysis of the German and Israeli experience. Haematologica 2019; 104(9): 1798–1803
CrossRef Pubmed Google scholar
[61]
Kono N, Ohashi K, Sasaki E, Okoshi Y, Mizuchi D, Mori S, Akiyama H, Karasawa K, Kaku H, Okamoto R, Maeda Y, Sasaki T, Okuyama Y, Hiruma K, Sakamaki H. Second allogeneic peripheral blood stem cell transplantation with fludarabine-based low-intensity conditioning regimen for relapsed myelodysplastic syndrome after allogeneic bone marrow transplantation. Int J Hematol 2001; 73(1): 122–125
CrossRef Pubmed Google scholar
[62]
Grüllich C, Bertz H, Spyridonidis A, Müller CI, Finke J. A fludarabine, thiotepa reduced toxicity conditioning regimen designed specifically for allogeneic second haematopoietic cell transplantation after failure of previous autologous or allogeneic transplantation. Bone Marrow Transplant 2008; 41(10): 845–850
CrossRef Pubmed Google scholar
[63]
Kishi K, Takahashi S, Gondo H, Shiobara S, Kanamaru A, Kato S, Hirabayashi N, Moriyama Y, Harada M, Asano S, Hara H, Shibata A. Second allogeneic bone marrow transplantation for post-transplant leukemia relapse: results of a survey of 66 cases in 24 Japanese institutes. Bone Marrow Transplant 1997; 19(5): 461–466
CrossRef Pubmed Google scholar

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 81670116), Key Program of National Natural Science Foundation of China (No. 81730004), Beijing Natural Science Foundation (No. 7171013), and Foundation for Innovative Research Groups of the National Natural Science Foundation of China (No. 81621001). We thank all the faculty members who participated in these studies. We would also like to thank American Journal Experts for their assistance in editing this manuscript.

Compliance with ethics guidelines

Tingting Han, Yuqian Sun, Yang Liu, Chenhua Yan, Yu Wang, Lanping Xu, Kaiyan Liu, Xiaojun Huang, and Xiaohui Zhang declare that they have no conflict of interest. All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000 (5). Informed consent was obtained from all patients for being included in the study.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11684-021-0833-x and is accessible for authorized users.

RIGHTS & PERMISSIONS

2021 Higher Education Press
AI Summary AI Mindmap
PDF(376 KB)

Accesses

Citations

Detail

Sections
Recommended

/