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Published in: Annals of Hematology 1/2021

01-01-2021 | Acute Lymphoblastic Leukemia | Original Article

Outcome predictors after retransplantation in relapsed acute lymphoblastic leukemia: a multicenter, retrospective study

Authors: Yasuo Mori, Kensuke Sasaki, Yoshikiyo Ito, Takuro Kuriyama, Toshiyuki Ueno, Masanori Kadowaki, Takatoshi Aoki, Takeshi Sugio, Goichi Yoshimoto, Koji Kato, Takahiro Maeda, Koji Nagafuji, Koichi Akashi, Toshihiro Miyamoto, Fukuoka Blood and Marrow Transplantation Group

Published in: Annals of Hematology | Issue 1/2021

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Abstract

Retransplantation is the only curative treatment option for patients with acute lymphoblastic leukemia (ALL) that has relapsed after allogeneic hematopoietic cell transplantation (allo-HCT); however, data in this setting remain scant. Hence, this multicenter, retrospective study aims to determine outcome predictors after retransplantation in relapsed ALL. We examined 55 recipients who underwent multiple allo-HCTs during 2006–2018. The 2-year overall survival (OS), progression-free survival (PFS), and non-relapse mortality rates were 35.9%, 29.1%, and 23.6%, respectively. We observed a trend of better outcome in Ph + ALL (n = 22) patients compared with non-Ph ALL (n = 33) patients; the 2-year PFS was 40.9% versus 21.2%, indicating a beneficial effect of more potent second- or third-generation tyrosine kinase inhibitors. Univariate analysis revealed that late relapse after the previous transplant was the only significant predictor of better transplant outcome among Ph + ALL patients, whereas factors related to prolonged OS/PFS in non-Ph ALL patients were late relapse after the previous transplant, longer duration from disease relapse/progression to second or more allo-HCT, disease status at the transplantation, and good performance status. Nevertheless, further investigations are warranted to determine whether novel molecular-targeted agents with higher efficacy and fewer toxicities could exceed conventional chemotherapies as a bridging strategy to next allo-HCT and improve the outcomes of non-Ph ALL patients.
Literature
1.
go back to reference Brisco J, Hughes E, Neoh SH, Sykes PJ, Bradstock K, Enno A, Szer J, McCaul K, Morley AA (1996) Relationships between minimal residual disease and outcome in adult acute lymphoblastic leukemia. Blood. 87:5251–5256PubMedCrossRef Brisco J, Hughes E, Neoh SH, Sykes PJ, Bradstock K, Enno A, Szer J, McCaul K, Morley AA (1996) Relationships between minimal residual disease and outcome in adult acute lymphoblastic leukemia. Blood. 87:5251–5256PubMedCrossRef
2.
go back to reference Gokbuget N, Kneba M, Raff T et al (2012) Adult patients with acute lymphoblastic leukemia and molecular failure display a poor prognosis and are candidates for stem cell transplantation and targeted therapies. Blood. 120:1868–1876PubMedCrossRef Gokbuget N, Kneba M, Raff T et al (2012) Adult patients with acute lymphoblastic leukemia and molecular failure display a poor prognosis and are candidates for stem cell transplantation and targeted therapies. Blood. 120:1868–1876PubMedCrossRef
3.
go back to reference Ribera J-M, Oriol A, Morgades M, Montesinos P, Sarrà J, González-Campos J, Brunet S, Tormo M, Fernández-Abellán P, Guàrdia R, Bernal MT, Esteve J, Barba P, Moreno MJ, Bermúdez A, Cladera A, Escoda L, García-Boyero R, del Potro E, Bergua J, Amigo ML, Grande C, Rabuñal MJ, Hernández-Rivas JM, Feliu E (2014) Treatment of high-risk Philadelphia chromosome-negative acute lymphoblastic leukemia in adolescents and adults according to early cytologic response and minimal residual disease after consolidation assessed by flow cytometry: final results of the PETHEMA ALL-AR-3 trial. J Clin Oncol 32:1595–1604PubMedCrossRef Ribera J-M, Oriol A, Morgades M, Montesinos P, Sarrà J, González-Campos J, Brunet S, Tormo M, Fernández-Abellán P, Guàrdia R, Bernal MT, Esteve J, Barba P, Moreno MJ, Bermúdez A, Cladera A, Escoda L, García-Boyero R, del Potro E, Bergua J, Amigo ML, Grande C, Rabuñal MJ, Hernández-Rivas JM, Feliu E (2014) Treatment of high-risk Philadelphia chromosome-negative acute lymphoblastic leukemia in adolescents and adults according to early cytologic response and minimal residual disease after consolidation assessed by flow cytometry: final results of the PETHEMA ALL-AR-3 trial. J Clin Oncol 32:1595–1604PubMedCrossRef
4.
go back to reference Beldjord K, Chevret S, Asnafi V, Huguet F, Boulland ML, Leguay T, Thomas X, Cayuela JM, Grardel N, Chalandon Y, Boissel N, Schaefer B, Delabesse E, Cavé H, Chevallier P, Buzyn A, Fest T, Reman O, Vernant JP, Lhéritier V, Béné MC, Lafage M, Macintyre E, Ifrah N, Dombret H, Group for Research on Adult Acute Lymphoblastic Leukemia (GRAALL) (2014) Oncogenetics and minimal residual disease are independent outcome predictors in adult patients with acute lymphoblastic leukemia. Blood. 123:3739–3749PubMedCrossRef Beldjord K, Chevret S, Asnafi V, Huguet F, Boulland ML, Leguay T, Thomas X, Cayuela JM, Grardel N, Chalandon Y, Boissel N, Schaefer B, Delabesse E, Cavé H, Chevallier P, Buzyn A, Fest T, Reman O, Vernant JP, Lhéritier V, Béné MC, Lafage M, Macintyre E, Ifrah N, Dombret H, Group for Research on Adult Acute Lymphoblastic Leukemia (GRAALL) (2014) Oncogenetics and minimal residual disease are independent outcome predictors in adult patients with acute lymphoblastic leukemia. Blood. 123:3739–3749PubMedCrossRef
5.
go back to reference Nagafuji K, Miyamoto T, Eto T, Kamimura T, Taniguchi S, Okamura T, Ohtsuka E, Yoshida T, Higuchi M, Yoshimoto G, Fujisaki T, Abe Y, Takamatsu Y, Yokota S, Akashi K, Harada M (2013) Monitoring of minimal residual disease (MRD) is useful to predict prognosis of adult patients with Ph-negative ALL: results of a prospective study (ALL MRD2002 Study). J Hematol Oncol 6:14PubMedPubMedCentralCrossRef Nagafuji K, Miyamoto T, Eto T, Kamimura T, Taniguchi S, Okamura T, Ohtsuka E, Yoshida T, Higuchi M, Yoshimoto G, Fujisaki T, Abe Y, Takamatsu Y, Yokota S, Akashi K, Harada M (2013) Monitoring of minimal residual disease (MRD) is useful to predict prognosis of adult patients with Ph-negative ALL: results of a prospective study (ALL MRD2002 Study). J Hematol Oncol 6:14PubMedPubMedCentralCrossRef
6.
go back to reference Nagafuji K, Miyamoto T, Eto T, Ogawa R, Okumura H, Takase K, Kawano N, Miyazaki Y, Fujisaki T, Wake A, Ohno Y, Kurokawa T, Kamimura T, Takamatsu Y, Yokota S, Akashi K (2019) Prospective evaluation of minimal residual disease monitoring to predict prognosis of adult patients with Ph-negative acute lymphoblastic leukemia. Eur J Haematol 103:164–171PubMedCrossRef Nagafuji K, Miyamoto T, Eto T, Ogawa R, Okumura H, Takase K, Kawano N, Miyazaki Y, Fujisaki T, Wake A, Ohno Y, Kurokawa T, Kamimura T, Takamatsu Y, Yokota S, Akashi K (2019) Prospective evaluation of minimal residual disease monitoring to predict prognosis of adult patients with Ph-negative acute lymphoblastic leukemia. Eur J Haematol 103:164–171PubMedCrossRef
7.
go back to reference Fielding AK, Richards SM, Chopra R, Lazarus HM, Litzow MR, Buck G, Durrant IJ, Luger SM, Marks DI, Franklin IM, McMillan A, Tallman MS, Rowe JM, Goldstone AH, Medical Research Council of the United Kingdom Adult ALL Working Party, Eastern Cooperative Oncology Group (2007) Outcome of 609 adults after relapse of acute lymphoblastic leukemia (ALL); an MRC UKALL12/ECOG 2993 study. Blood. 109:944–950PubMedCrossRef Fielding AK, Richards SM, Chopra R, Lazarus HM, Litzow MR, Buck G, Durrant IJ, Luger SM, Marks DI, Franklin IM, McMillan A, Tallman MS, Rowe JM, Goldstone AH, Medical Research Council of the United Kingdom Adult ALL Working Party, Eastern Cooperative Oncology Group (2007) Outcome of 609 adults after relapse of acute lymphoblastic leukemia (ALL); an MRC UKALL12/ECOG 2993 study. Blood. 109:944–950PubMedCrossRef
8.
go back to reference Gupta V, Richards S, Rowe J (2013) Allogenic, but not autologous, hematopoietic cell transplantation improves survival only among younger adults with acute lymphoblastic leukemia in first remission: an individual patient data meta-analysis. Blood. 121:339–350PubMedPubMedCentralCrossRef Gupta V, Richards S, Rowe J (2013) Allogenic, but not autologous, hematopoietic cell transplantation improves survival only among younger adults with acute lymphoblastic leukemia in first remission: an individual patient data meta-analysis. Blood. 121:339–350PubMedPubMedCentralCrossRef
9.
go back to reference Rosko A, Wang HL, de Lima M et al (2017) Reduced intensity conditioned allograft yields favorable survival for older adults with B-cell acute lymphoblastic leukemia. Am J Hematol 92:42–49PubMedCrossRef Rosko A, Wang HL, de Lima M et al (2017) Reduced intensity conditioned allograft yields favorable survival for older adults with B-cell acute lymphoblastic leukemia. Am J Hematol 92:42–49PubMedCrossRef
10.
go back to reference Marks DI, Wang T, Peres WS et al (2010) The outcome of full-intensity and reduced-intensity conditioning matched sibling or unrelated donor transplantation in adults with Philadelphia chromosome-negative acute lymphoblastic leukemia in first and second complete remission. Blood. 116:366–374PubMedPubMedCentralCrossRef Marks DI, Wang T, Peres WS et al (2010) The outcome of full-intensity and reduced-intensity conditioning matched sibling or unrelated donor transplantation in adults with Philadelphia chromosome-negative acute lymphoblastic leukemia in first and second complete remission. Blood. 116:366–374PubMedPubMedCentralCrossRef
11.
go back to reference Nishiwaki S, Miyamura K, Ohashi K, Kurokawa M, Taniguchi S, Fukuda T, Ikegame K, Takahashi S, Mori T, Imai K, Iida H, Hidaka M, Sakamaki H, Morishima Y, Kato K, Suzuki R, Tanaka J, Adult Acute Lymphoblastic Leukemia Working Group of the Japan Society for Hematopoietic Cell Transplantation (2013) Impact of a donor source on adult Philadelphia chromosome-negative acute lymphoblastic leukemia: a retrospective analysis from the Adult Acute Lymphoblastic Leukemia Working Group of the Japan Society for Hematopoietic Cell Transplantation. Ann Oncol 24:1594–1602PubMedCrossRef Nishiwaki S, Miyamura K, Ohashi K, Kurokawa M, Taniguchi S, Fukuda T, Ikegame K, Takahashi S, Mori T, Imai K, Iida H, Hidaka M, Sakamaki H, Morishima Y, Kato K, Suzuki R, Tanaka J, Adult Acute Lymphoblastic Leukemia Working Group of the Japan Society for Hematopoietic Cell Transplantation (2013) Impact of a donor source on adult Philadelphia chromosome-negative acute lymphoblastic leukemia: a retrospective analysis from the Adult Acute Lymphoblastic Leukemia Working Group of the Japan Society for Hematopoietic Cell Transplantation. Ann Oncol 24:1594–1602PubMedCrossRef
12.
go back to reference Spyridonidis A, Labopin M, Schmid C et al (2012) Outcomes and prognostic factors of adults with acute lymphoblastic leukemia who relapse after allogeneic hematopoietic cell transplantation. Leukemia. 26:1211–1217PubMedCrossRef Spyridonidis A, Labopin M, Schmid C et al (2012) Outcomes and prognostic factors of adults with acute lymphoblastic leukemia who relapse after allogeneic hematopoietic cell transplantation. Leukemia. 26:1211–1217PubMedCrossRef
13.
go back to reference Chen R, Campbell JL, Chen B (2015) Prophylaxis and treatment of acute lymphoblastic leukemia relapse after allogeneic hematopoietic stem cell transplantation. Onco Targets Ther 8:405–412PubMedPubMedCentralCrossRef Chen R, Campbell JL, Chen B (2015) Prophylaxis and treatment of acute lymphoblastic leukemia relapse after allogeneic hematopoietic stem cell transplantation. Onco Targets Ther 8:405–412PubMedPubMedCentralCrossRef
14.
go back to reference Kishi K, Takahashi S, Gondo H, Shiobara S, Kanamaru A, Kato S, Hirabayashi N, Moriyama Y, Harada M, Asano S, Hara H, Shibata A (1997) Second allogeneic bone marrow transplantation for post-transplant leukemia relapse: results of a survey of 66 cases in 24 Japanese institutes. Bone Marrow Transplant 19:461–466PubMedCrossRef Kishi K, Takahashi S, Gondo H, Shiobara S, Kanamaru A, Kato S, Hirabayashi N, Moriyama Y, Harada M, Asano S, Hara H, Shibata A (1997) Second allogeneic bone marrow transplantation for post-transplant leukemia relapse: results of a survey of 66 cases in 24 Japanese institutes. Bone Marrow Transplant 19:461–466PubMedCrossRef
15.
go back to reference 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 (2004) Second transplant for acute and chronic leukemia relapsing after first HLA-identical sibling transplant. Bone Marrow Transplant 34:721–727PubMedCrossRef 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 (2004) Second transplant for acute and chronic leukemia relapsing after first HLA-identical sibling transplant. Bone Marrow Transplant 34:721–727PubMedCrossRef
16.
go back to reference Poon LM, Bassett R Jr, Rondon G et al (2013) Outcomes of second allogeneic hematopoietic stem cell transplantation for patients with acute lymphoblastic leukemia. Bone Marrow Transplant 48:666–670PubMedCrossRef Poon LM, Bassett R Jr, Rondon G et al (2013) Outcomes of second allogeneic hematopoietic stem cell transplantation for patients with acute lymphoblastic leukemia. Bone Marrow Transplant 48:666–670PubMedCrossRef
17.
go back to reference Ruutu T, de Wreede LC, van Biezen A et al (2015) Second allogeneic transplantation for relapse of malignant disease: retrospective analysis of outcome abd predictive factors by the EBMT. Bone Marrow Transplant 50:1542–1550PubMedCrossRef Ruutu T, de Wreede LC, van Biezen A et al (2015) Second allogeneic transplantation for relapse of malignant disease: retrospective analysis of outcome abd predictive factors by the EBMT. Bone Marrow Transplant 50:1542–1550PubMedCrossRef
18.
go back to reference Al Malki MM, Aldoss I, Stiller T et al (2016) Outcome of second allogeneic hematopoietic cell transplantation in patients with acute lymphoblastic leukemia. Clin Lymphoma Myeloma Leuk 16:519–522PubMedCrossRef Al Malki MM, Aldoss I, Stiller T et al (2016) Outcome of second allogeneic hematopoietic cell transplantation in patients with acute lymphoblastic leukemia. Clin Lymphoma Myeloma Leuk 16:519–522PubMedCrossRef
19.
go back to reference 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 (2017) Major histocompatibility mismatch and donor choice for second allogeneic bone marrow transplantation. Biol Blood Marrow Transplant 23:1887–1894PubMedPubMedCentralCrossRef 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 (2017) Major histocompatibility mismatch and donor choice for second allogeneic bone marrow transplantation. Biol Blood Marrow Transplant 23:1887–1894PubMedPubMedCentralCrossRef
20.
go back to reference Schneidawind C, Hagmaier V, Faul C, Kanz L, Bethge W, Schneidawind D (2018) Second allogeneic hematopoietic cell transplantation enables long-term disease-free survival in relapsed acute leukemia. Ann Hematol 97:2491–2500PubMedCrossRef Schneidawind C, Hagmaier V, Faul C, Kanz L, Bethge W, Schneidawind D (2018) Second allogeneic hematopoietic cell transplantation enables long-term disease-free survival in relapsed acute leukemia. Ann Hematol 97:2491–2500PubMedCrossRef
21.
go back to reference Orti G, Sanz J, Garcia-Cadenas I et al (2018) Analysis of relapse after transplantation in acute leukemia: a comparative on second allogeneic hematopoietic cell transplantation and donor lymphocyte infusions. Exp Hematol 62:24–32PubMedCrossRef Orti G, Sanz J, Garcia-Cadenas I et al (2018) Analysis of relapse after transplantation in acute leukemia: a comparative on second allogeneic hematopoietic cell transplantation and donor lymphocyte infusions. Exp Hematol 62:24–32PubMedCrossRef
22.
go back to reference Lund TC, Ahn KW, Tecca HR, Hilgers MV, Abdel-Azim H, Abraham A, Diaz MA, Badawy SM, Broglie L, Brown V, Dvorak CC, Gonzalez-Vicent M, Hashem H, Hayashi RJ, Jacobsohn DA, Kent MW, Li CK, Margossian SP, Martin PL, Mehta P, Myers K, Olsson R, Page K, Pulsipher MA, Shaw PJ, Smith AR, Triplett BM, Verneris MR, Eapen M (2019) Outcomes after second hematopoietic cell transplantation in children and young adults with relapsed acute leukemia. Biol Blood Marrow Transplant 25:301–306PubMedCrossRef Lund TC, Ahn KW, Tecca HR, Hilgers MV, Abdel-Azim H, Abraham A, Diaz MA, Badawy SM, Broglie L, Brown V, Dvorak CC, Gonzalez-Vicent M, Hashem H, Hayashi RJ, Jacobsohn DA, Kent MW, Li CK, Margossian SP, Martin PL, Mehta P, Myers K, Olsson R, Page K, Pulsipher MA, Shaw PJ, Smith AR, Triplett BM, Verneris MR, Eapen M (2019) Outcomes after second hematopoietic cell transplantation in children and young adults with relapsed acute leukemia. Biol Blood Marrow Transplant 25:301–306PubMedCrossRef
23.
go back to reference Nagler A, Labopin M, Dholaria B, Finke J, Brecht A, Schanz U, Niittyvuopio R, Neubauer A, Bornhäuser M, Santarone S, Beelen D, Shimoni A, Rösler W, Giebel S, Savani BN, Mohty M (2019) Second allogeneic stem cell transplantation in patients with acute lymphoblastic leukaemia: a study on behalf of the Acute Leukaemia Working Party of the European Society for Blood and Marrow Transplantation. Br J Haematol 186:767–776PubMedCrossRef Nagler A, Labopin M, Dholaria B, Finke J, Brecht A, Schanz U, Niittyvuopio R, Neubauer A, Bornhäuser M, Santarone S, Beelen D, Shimoni A, Rösler W, Giebel S, Savani BN, Mohty M (2019) Second allogeneic stem cell transplantation in patients with acute lymphoblastic leukaemia: a study on behalf of the Acute Leukaemia Working Party of the European Society for Blood and Marrow Transplantation. Br J Haematol 186:767–776PubMedCrossRef
24.
go back to reference Kantarjian H, DeAngelo D, Stelljes M et al (2016) Inotuzumab ozogamicin versus standard therapy for acute lymphoblastic leukemia. N Engl J Med 375:740–753PubMedPubMedCentralCrossRef Kantarjian H, DeAngelo D, Stelljes M et al (2016) Inotuzumab ozogamicin versus standard therapy for acute lymphoblastic leukemia. N Engl J Med 375:740–753PubMedPubMedCentralCrossRef
25.
26.
go back to reference Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H, Bader P, Verneris MR, Stefanski HE, Myers GD, Qayed M, de Moerloose B, Hiramatsu H, Schlis K, Davis KL, Martin PL, Nemecek ER, Yanik GA, Peters C, Baruchel A, Boissel N, Mechinaud F, Balduzzi A, Krueger J, June CH, Levine BL, Wood P, Taran T, Leung M, Mueller KT, Zhang Y, Sen K, Lebwohl D, Pulsipher MA, Grupp SA (2018) Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med 378:439–448PubMedPubMedCentralCrossRef Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H, Bader P, Verneris MR, Stefanski HE, Myers GD, Qayed M, de Moerloose B, Hiramatsu H, Schlis K, Davis KL, Martin PL, Nemecek ER, Yanik GA, Peters C, Baruchel A, Boissel N, Mechinaud F, Balduzzi A, Krueger J, June CH, Levine BL, Wood P, Taran T, Leung M, Mueller KT, Zhang Y, Sen K, Lebwohl D, Pulsipher MA, Grupp SA (2018) Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med 378:439–448PubMedPubMedCentralCrossRef
27.
go back to reference Yanada M, Konuma T, Kuwatsuka Y, Kondo T, Kawata T, Takahashi S, Uchida N, Miyakoshi S, Tanaka M, Ozawa Y, Sawa M, Nakamae H, Aotsuka N, Kanda J, Takanashi M, Kanda Y, Atsuta Y, Yano S (2019) Unit selection for umbilical cord blood transplantation for adults with acute myeloid leukemia in complete remission: a Japanese experience. Bone Marrow Tlansplant 54:1789–1798CrossRef Yanada M, Konuma T, Kuwatsuka Y, Kondo T, Kawata T, Takahashi S, Uchida N, Miyakoshi S, Tanaka M, Ozawa Y, Sawa M, Nakamae H, Aotsuka N, Kanda J, Takanashi M, Kanda Y, Atsuta Y, Yano S (2019) Unit selection for umbilical cord blood transplantation for adults with acute myeloid leukemia in complete remission: a Japanese experience. Bone Marrow Tlansplant 54:1789–1798CrossRef
28.
go back to reference Ogawa H, Yoshida T, Yoshihara S et al (2015) Unmanipulated haploidentical reduced-intensity stem cell transplantation using fludarabine, busulfan, low-dose antithymocyte globulin, and steroids for patients in non-complete remission or at high risk of relapse: a prospective multicenter phase I/II study in Japan. Biol Blood Marrow Transplant 21:1495–1505PubMedCrossRef Ogawa H, Yoshida T, Yoshihara S et al (2015) Unmanipulated haploidentical reduced-intensity stem cell transplantation using fludarabine, busulfan, low-dose antithymocyte globulin, and steroids for patients in non-complete remission or at high risk of relapse: a prospective multicenter phase I/II study in Japan. Biol Blood Marrow Transplant 21:1495–1505PubMedCrossRef
29.
go back to reference Sugita J, Kawashima N, Fujisaki T, Kakihana K, Ota S, Matsuo K, Miyamoto T, Akashi K, Taniguchi S, Harada M, Teshima T (2015) HLA-haploidentical peripheral blood stem cell transplantation with post-transplant cyclophosphamide after busulfan-containing reduced-intensity conditioning. Biol Blood Marrow Transplant 21:1646–1652PubMedCrossRef Sugita J, Kawashima N, Fujisaki T, Kakihana K, Ota S, Matsuo K, Miyamoto T, Akashi K, Taniguchi S, Harada M, Teshima T (2015) HLA-haploidentical peripheral blood stem cell transplantation with post-transplant cyclophosphamide after busulfan-containing reduced-intensity conditioning. Biol Blood Marrow Transplant 21:1646–1652PubMedCrossRef
30.
go back to reference Kanda Y (2013) Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Trasnplant 48:452–458CrossRef Kanda Y (2013) Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Trasnplant 48:452–458CrossRef
31.
go back to reference Sorror ML, Maris MB, Storb R, Baron F, Sandmaier BM, Maloney DG, Storer B (2005) Hematopoietic cell transplantation (HCT)-specific comorbidity index: a new tool for risk assessment before allogeneic HCT. Blood. 106:2912–2919PubMedPubMedCentralCrossRef Sorror ML, Maris MB, Storb R, Baron F, Sandmaier BM, Maloney DG, Storer B (2005) Hematopoietic cell transplantation (HCT)-specific comorbidity index: a new tool for risk assessment before allogeneic HCT. Blood. 106:2912–2919PubMedPubMedCentralCrossRef
32.
go back to reference Richard-Carpentier G, Kantarjian H, Jabbour E (2019) Recent advances in adult acute lymphoblastic leukemia. Curr Hematol Malig Rep 14:106–118PubMed Richard-Carpentier G, Kantarjian H, Jabbour E (2019) Recent advances in adult acute lymphoblastic leukemia. Curr Hematol Malig Rep 14:106–118PubMed
33.
go back to reference Ravandi F, O’Brien S, Thomas D et al (2010) First report of phase 2 study of dasatinib with hyper-CVAD for the frontline treatment of Philadelphia chromosome-positive (Ph+) acute lymphoblastic leukemia. Blood. 116:2070–2077PubMedPubMedCentralCrossRef Ravandi F, O’Brien S, Thomas D et al (2010) First report of phase 2 study of dasatinib with hyper-CVAD for the frontline treatment of Philadelphia chromosome-positive (Ph+) acute lymphoblastic leukemia. Blood. 116:2070–2077PubMedPubMedCentralCrossRef
34.
go back to reference Jabbour E, Kantarjian H, Ravandi F, Thomas D, Huang X, Faderl S, Pemmaraju N, Daver N, Garcia-Manero G, Sasaki K, Cortes J, Garris R, Yin CC, Khoury JD, Jorgensen J, Estrov Z, Bohannan Z, Konopleva M, Kadia T, Jain N, DiNardo C, Wierda W, Jeanis V, O'Brien S (2015) Combination of hyper-CVAD with ponatinib as first-line therapy for patients with Philadelphia chromosome-positive acute lymphoblastic leukaemia: a single-centre, phase 2 study. Lancet Oncol 16:1547–1555PubMedPubMedCentralCrossRef Jabbour E, Kantarjian H, Ravandi F, Thomas D, Huang X, Faderl S, Pemmaraju N, Daver N, Garcia-Manero G, Sasaki K, Cortes J, Garris R, Yin CC, Khoury JD, Jorgensen J, Estrov Z, Bohannan Z, Konopleva M, Kadia T, Jain N, DiNardo C, Wierda W, Jeanis V, O'Brien S (2015) Combination of hyper-CVAD with ponatinib as first-line therapy for patients with Philadelphia chromosome-positive acute lymphoblastic leukaemia: a single-centre, phase 2 study. Lancet Oncol 16:1547–1555PubMedPubMedCentralCrossRef
35.
go back to reference Kiyoi H, Morris JD, Oh I et al (2020) Phase 1b/2 study of blinatumomab in Japanese adults with relapsed/refractory acute lymphoblastic leukemia. Cancer Sci 111:1314–1323 Kiyoi H, Morris JD, Oh I et al (2020) Phase 1b/2 study of blinatumomab in Japanese adults with relapsed/refractory acute lymphoblastic leukemia. Cancer Sci 111:1314–1323
36.
go back to reference Giebel S, Czyz A, Ottmann O, Baron F, Brissot E, Ciceri F, Cornelissen JJ, Esteve J, Gorin NC, Savani B, Schmid C, Mohty M, Nagler A (2016) Use of tyrosine kinase inhibitors to prevent relapse after allogeneic hematopoietic stem cell transplantation for patients with Philadelphia chromosome-positive acute lymphoblastic leukemia: a position statement of the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation. Cancer. 122:2941–2951PubMedCrossRef Giebel S, Czyz A, Ottmann O, Baron F, Brissot E, Ciceri F, Cornelissen JJ, Esteve J, Gorin NC, Savani B, Schmid C, Mohty M, Nagler A (2016) Use of tyrosine kinase inhibitors to prevent relapse after allogeneic hematopoietic stem cell transplantation for patients with Philadelphia chromosome-positive acute lymphoblastic leukemia: a position statement of the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation. Cancer. 122:2941–2951PubMedCrossRef
38.
go back to reference Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, le Beau MM, Bloomfield CD, Cazzola M, Vardiman JW (2016) The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 127:2391–2405CrossRefPubMed Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, le Beau MM, Bloomfield CD, Cazzola M, Vardiman JW (2016) The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 127:2391–2405CrossRefPubMed
39.
go back to reference Mullighan CG, Su X, Zhang J, Radtke I, Phillips LA, Miller CB, Ma J, Liu W, Cheng C, Schulman BA, Harvey RC, Chen IM, Clifford RJ, Carroll WL, Reaman G, Bowman WP, Devidas M, Gerhard DS, Yang W, Relling MV, Shurtleff SA, Campana D, Borowitz MJ, Pui CH, Smith M, Hunger SP, Willman CL, Downing JR, Children's Oncology Group (2009) Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med 360:470–480PubMedPubMedCentralCrossRef Mullighan CG, Su X, Zhang J, Radtke I, Phillips LA, Miller CB, Ma J, Liu W, Cheng C, Schulman BA, Harvey RC, Chen IM, Clifford RJ, Carroll WL, Reaman G, Bowman WP, Devidas M, Gerhard DS, Yang W, Relling MV, Shurtleff SA, Campana D, Borowitz MJ, Pui CH, Smith M, Hunger SP, Willman CL, Downing JR, Children's Oncology Group (2009) Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med 360:470–480PubMedPubMedCentralCrossRef
40.
go back to reference Den Boer ML, van Slegtenhorst M, De Menezes RX et al (2009) A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol 10:125–134CrossRef Den Boer ML, van Slegtenhorst M, De Menezes RX et al (2009) A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol 10:125–134CrossRef
41.
go back to reference Roberts KG, Li Y, Payne-Turner D, Harvey RC, Yang YL, Pei D, McCastlain K, Ding L, Lu C, Song G, Ma J, Becksfort J, Rusch M, Chen SC, Easton J, Cheng J, Boggs K, Santiago-Morales N, Iacobucci I, Fulton RS, Wen J, Valentine M, Cheng C, Paugh SW, Devidas M, Chen IM, Reshmi S, Smith A, Hedlund E, Gupta P, Nagahawatte P, Wu G, Chen X, Yergeau D, Vadodaria B, Mulder H, Winick NJ, Larsen EC, Carroll WL, Heerema NA, Carroll AJ, Grayson G, Tasian SK, Moore AS, Keller F, Frei-Jones M, Whitlock JA, Raetz EA, White DL, Hughes TP, Guidry Auvil JM, Smith MA, Marcucci G, Bloomfield CD, Mrózek K, Kohlschmidt J, Stock W, Kornblau SM, Konopleva M, Paietta E, Pui CH, Jeha S, Relling MV, Evans WE, Gerhard DS, Gastier-Foster JM, Mardis E, Wilson RK, Loh ML, Downing JR, Hunger SP, Willman CL, Zhang J, Mullighan CG (2014) Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. N Engl J Med 371:1005–1015PubMedPubMedCentralCrossRef Roberts KG, Li Y, Payne-Turner D, Harvey RC, Yang YL, Pei D, McCastlain K, Ding L, Lu C, Song G, Ma J, Becksfort J, Rusch M, Chen SC, Easton J, Cheng J, Boggs K, Santiago-Morales N, Iacobucci I, Fulton RS, Wen J, Valentine M, Cheng C, Paugh SW, Devidas M, Chen IM, Reshmi S, Smith A, Hedlund E, Gupta P, Nagahawatte P, Wu G, Chen X, Yergeau D, Vadodaria B, Mulder H, Winick NJ, Larsen EC, Carroll WL, Heerema NA, Carroll AJ, Grayson G, Tasian SK, Moore AS, Keller F, Frei-Jones M, Whitlock JA, Raetz EA, White DL, Hughes TP, Guidry Auvil JM, Smith MA, Marcucci G, Bloomfield CD, Mrózek K, Kohlschmidt J, Stock W, Kornblau SM, Konopleva M, Paietta E, Pui CH, Jeha S, Relling MV, Evans WE, Gerhard DS, Gastier-Foster JM, Mardis E, Wilson RK, Loh ML, Downing JR, Hunger SP, Willman CL, Zhang J, Mullighan CG (2014) Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. N Engl J Med 371:1005–1015PubMedPubMedCentralCrossRef
42.
go back to reference Roberts KG, Gu Z, Payne-Turner D, McCastlain K, Harvey RC, Chen IM, Pei D, Iacobucci I, Valentine M, Pounds SB, Shi L, Li Y, Zhang J, Cheng C, Rambaldi A, Tosi M, Spinelli O, Radich JP, Minden MD, Rowe JM, Luger S, Litzow MR, Tallman MS, Wiernik PH, Bhatia R, Aldoss I, Kohlschmidt J, Mrózek K, Marcucci G, Bloomfield CD, Stock W, Kornblau S, Kantarjian HM, Konopleva M, Paietta E, Willman CL, Mullighan CG (2017) High frequency and poor outcome of Philadelphia chromosome-like acute lymphoblastic leukemia in adults. J Clin Oncol 35:394–401PubMedCrossRef Roberts KG, Gu Z, Payne-Turner D, McCastlain K, Harvey RC, Chen IM, Pei D, Iacobucci I, Valentine M, Pounds SB, Shi L, Li Y, Zhang J, Cheng C, Rambaldi A, Tosi M, Spinelli O, Radich JP, Minden MD, Rowe JM, Luger S, Litzow MR, Tallman MS, Wiernik PH, Bhatia R, Aldoss I, Kohlschmidt J, Mrózek K, Marcucci G, Bloomfield CD, Stock W, Kornblau S, Kantarjian HM, Konopleva M, Paietta E, Willman CL, Mullighan CG (2017) High frequency and poor outcome of Philadelphia chromosome-like acute lymphoblastic leukemia in adults. J Clin Oncol 35:394–401PubMedCrossRef
43.
go back to reference Maude SL, Tasian SK, Vincent T, Hall JW, Sheen C, Roberts KG, Seif AE, Barrett DM, Chen IM, Collins JR, Mullighan CG, Hunger SP, Harvey RC, Willman CL, Fridman JS, Loh ML, Grupp SA, Teachey DT (2012) Targeting JAK1/2 and mTOR in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood. 120:3510–3518PubMedPubMedCentralCrossRef Maude SL, Tasian SK, Vincent T, Hall JW, Sheen C, Roberts KG, Seif AE, Barrett DM, Chen IM, Collins JR, Mullighan CG, Hunger SP, Harvey RC, Willman CL, Fridman JS, Loh ML, Grupp SA, Teachey DT (2012) Targeting JAK1/2 and mTOR in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood. 120:3510–3518PubMedPubMedCentralCrossRef
44.
go back to reference Roberts KG, Yang YL, Payne-Turner D et al (2017) Oncogenic role and therapeutic targeting of ABL-class and JAK-STAT activating kinase alterations in Ph-like ALL. Blood Adv 1:1657–1671PubMedPubMedCentralCrossRef Roberts KG, Yang YL, Payne-Turner D et al (2017) Oncogenic role and therapeutic targeting of ABL-class and JAK-STAT activating kinase alterations in Ph-like ALL. Blood Adv 1:1657–1671PubMedPubMedCentralCrossRef
Metadata
Title
Outcome predictors after retransplantation in relapsed acute lymphoblastic leukemia: a multicenter, retrospective study
Authors
Yasuo Mori
Kensuke Sasaki
Yoshikiyo Ito
Takuro Kuriyama
Toshiyuki Ueno
Masanori Kadowaki
Takatoshi Aoki
Takeshi Sugio
Goichi Yoshimoto
Koji Kato
Takahiro Maeda
Koji Nagafuji
Koichi Akashi
Toshihiro Miyamoto
Fukuoka Blood and Marrow Transplantation Group
Publication date
01-01-2021
Publisher
Springer Berlin Heidelberg
Published in
Annals of Hematology / Issue 1/2021
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-020-04310-0

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