Skip to main content
Top
Published in: Annals of Hematology 4/2021

01-04-2021 | Acute Lymphoblastic Leukemia | Original Article

Anti-CD19 CAR-T cell therapy bridge to HSCT decreases the relapse rate and improves the long-term survival of R/R B-ALL patients: a systematic review and meta-analysis

Authors: Linhui Hu, Alice Charwudzi, Qian Li, Weiwei Zhu, Qianshan Tao, Shudao Xiong, Zhimin Zhai

Published in: Annals of Hematology | Issue 4/2021

Login to get access

Abstract

Chimeric antigen receptor (CAR) T cell therapy improves the remission rate of refractory/relapsed B-acute lymphoblastic leukemia (R/R B-ALL) patients, but the relapse rate remains high. Recent studies suggest patients who underwent post-chimeric antigen receptor T cell therapy hematopoietic stem cell transplantation (post- HSCT) would achieve durable remission and better survival, but this remains controversial. To this end, we conducted a meta-analysis to assess the role of post-HSCT in R/R B-ALL. The Cochrane Library, Embase, and PubMed were used to identify relevant studies; the latest search update was on July 05, 2020. We used the Cochran Q test and I-squared statistics to test for heterogeneity among the studies analyzed. The fixed model and random model were used to combine results when appropriate. We performed all statistical analyses with Stata 12, and P < 0.05 was considered statistically significant. We included 18 studies with 758 patients in the meta-analysis. Our results indicated that post-HSCT was associated with lower relapse rate (RR: 0.40, 95% CI: 0.32–0.50, P = 0.000), better overall survival (HR: 0.37, 95% CI: 0.19–0.71, P = 0.003), better leukemia-free survival (HR: 0.20, 95% CI: 0.10–0.40, P = 0.000). However, post-HSCT did not influence OS in Caucasians, and CAR-T cells with CD28 co-stimulation factor bridged to HSCT did not influence OS. Post-HSCT decreased the relapse rate and improved the long-term survival of R/R B-ALL patients. R/R B-ALL patients would benefit from post-HSCT after CAR-T cell therapy.
Appendix
Available only for authorised users
Literature
1.
go back to reference Chen B, Wang YY, Shen Y, Zhang WN, He HY, Zhu YM, Chen HM, Gu CH, Fan X, Chen JM, Cao Q, Yang G, Jiang CL, Weng XQ, Zhang XX, Xiong SM, Shen ZX, Jiang H, Gu LJ, Chen Z, Mi JQ, Chen SJ (2012) Newly diagnosed acute lymphoblastic leukemia in China (I): abnormal genetic patterns in 1346 childhood and adult cases and their comparison with the reports from Western countries. Leukemia 26(7):1608–1616PubMedCrossRef Chen B, Wang YY, Shen Y, Zhang WN, He HY, Zhu YM, Chen HM, Gu CH, Fan X, Chen JM, Cao Q, Yang G, Jiang CL, Weng XQ, Zhang XX, Xiong SM, Shen ZX, Jiang H, Gu LJ, Chen Z, Mi JQ, Chen SJ (2012) Newly diagnosed acute lymphoblastic leukemia in China (I): abnormal genetic patterns in 1346 childhood and adult cases and their comparison with the reports from Western countries. Leukemia 26(7):1608–1616PubMedCrossRef
2.
go back to reference Liu K, Chu J, Dai Y, Jiang A, Yang L, Xie Z et al (2020) (2020) Long-term follow-up of acute lymphoblastic leukemia in young children treated by the SCMC-ALL-2009 protocol. Leuk Lymphoma. 61(12):2850–2858PubMedCrossRef Liu K, Chu J, Dai Y, Jiang A, Yang L, Xie Z et al (2020) (2020) Long-term follow-up of acute lymphoblastic leukemia in young children treated by the SCMC-ALL-2009 protocol. Leuk Lymphoma. 61(12):2850–2858PubMedCrossRef
3.
go back to reference Vrooman LM, Blonquist TM, Harris MH, Stevenson KE, Place AE, Hunt SK, O’Brien JE, Asselin BL, Athale UH, Clavell LA, Cole PD, Kelly KM, Laverdiere C, Leclerc JM, Michon B, Schorin MA, Sulis ML, Welch JJG, Neuberg DS, Sallan SE, Silverman LB (2018) Refining risk classification in childhood B acute lymphoblastic leukemia: results of DFCI ALL Consortium Protocol 05-001. Blood Adv 2(12):1449–1458PubMedPubMedCentralCrossRef Vrooman LM, Blonquist TM, Harris MH, Stevenson KE, Place AE, Hunt SK, O’Brien JE, Asselin BL, Athale UH, Clavell LA, Cole PD, Kelly KM, Laverdiere C, Leclerc JM, Michon B, Schorin MA, Sulis ML, Welch JJG, Neuberg DS, Sallan SE, Silverman LB (2018) Refining risk classification in childhood B acute lymphoblastic leukemia: results of DFCI ALL Consortium Protocol 05-001. Blood Adv 2(12):1449–1458PubMedPubMedCentralCrossRef
4.
go back to reference Moricke A, Zimmermann M, Valsecchi MG, Stanulla M, Biondi A, Mann G et al (2016) Dexamethasone vs prednisone in induction treatment of pediatric ALL: results of the randomized trial AIEOP-BFM ALL 2000. Blood 127(17):2101–2112PubMedCrossRef Moricke A, Zimmermann M, Valsecchi MG, Stanulla M, Biondi A, Mann G et al (2016) Dexamethasone vs prednisone in induction treatment of pediatric ALL: results of the randomized trial AIEOP-BFM ALL 2000. Blood 127(17):2101–2112PubMedCrossRef
5.
go back to reference Takahashi H, Kajiwara R, Kato M, Hasegawa D, Tomizawa D, Noguchi Y, Koike K, Toyama D, Yabe H, Kajiwara M, Fujimura J, Sotomatsu M, Ota S, Maeda M, Goto H, Kato Y, Mori T, Inukai T, Shimada H, Fukushima K, Ogawa C, Makimoto A, Fukushima T, Ohki K, Koh K, Kiyokawa N, Manabe A, Ohara A (2018) Treatment outcome of children with acute lymphoblastic leukemia: the Tokyo Children's Cancer Study Group (TCCSG) Study L04-16. Int J Hematol 108(1):98–108PubMedCrossRef Takahashi H, Kajiwara R, Kato M, Hasegawa D, Tomizawa D, Noguchi Y, Koike K, Toyama D, Yabe H, Kajiwara M, Fujimura J, Sotomatsu M, Ota S, Maeda M, Goto H, Kato Y, Mori T, Inukai T, Shimada H, Fukushima K, Ogawa C, Makimoto A, Fukushima T, Ohki K, Koh K, Kiyokawa N, Manabe A, Ohara A (2018) Treatment outcome of children with acute lymphoblastic leukemia: the Tokyo Children's Cancer Study Group (TCCSG) Study L04-16. Int J Hematol 108(1):98–108PubMedCrossRef
6.
go back to reference Gokbuget N, Stanze D, Beck J, Diedrich H, Horst HA, Huttmann A et al (2012) Outcome of relapsed adult lymphoblastic leukemia depends on response to salvage chemotherapy, prognostic factors, and performance of stem cell transplantation. Blood 120(10):2032–2041PubMedCrossRef Gokbuget N, Stanze D, Beck J, Diedrich H, Horst HA, Huttmann A et al (2012) Outcome of relapsed adult lymphoblastic leukemia depends on response to salvage chemotherapy, prognostic factors, and performance of stem cell transplantation. Blood 120(10):2032–2041PubMedCrossRef
7.
go back to reference Hu Y, Wu Z, Luo Y, Shi J, Yu J, Pu C, Liang Z, Wei G, Cui Q, Sun J, Jiang J, Xie J, Tan Y, Ni W, Tu J, Wang J, Jin A, Zhang H, Cai Z, Xiao L, Huang H (2017) Potent Anti-leukemia Activities of Chimeric Antigen Receptor-Modified T Cells against CD19 in Chinese Patients with Relapsed/Refractory Acute Lymphocytic Leukemia. Clin Cancer Res 23(13):3297–3306PubMedCrossRef Hu Y, Wu Z, Luo Y, Shi J, Yu J, Pu C, Liang Z, Wei G, Cui Q, Sun J, Jiang J, Xie J, Tan Y, Ni W, Tu J, Wang J, Jin A, Zhang H, Cai Z, Xiao L, Huang H (2017) Potent Anti-leukemia Activities of Chimeric Antigen Receptor-Modified T Cells against CD19 in Chinese Patients with Relapsed/Refractory Acute Lymphocytic Leukemia. Clin Cancer Res 23(13):3297–3306PubMedCrossRef
8.
go back to reference Pan J, Yang JF, Deng BP, Zhao XJ, Zhang X, Lin YH, Wu YN, Deng ZL, Zhang YL, Liu SH, Wu T, Lu PH, Lu DP, Chang AH, Tong CR (2017) High efficacy and safety of low-dose CD19-directed CAR-T cell therapy in 51 refractory or relapsed B acute lymphoblastic leukemia patients. Leukemia 31(12):2587–2593PubMedCrossRef Pan J, Yang JF, Deng BP, Zhao XJ, Zhang X, Lin YH, Wu YN, Deng ZL, Zhang YL, Liu SH, Wu T, Lu PH, Lu DP, Chang AH, Tong CR (2017) High efficacy and safety of low-dose CD19-directed CAR-T cell therapy in 51 refractory or relapsed B acute lymphoblastic leukemia patients. Leukemia 31(12):2587–2593PubMedCrossRef
10.
go back to reference Zhang X, Lu XA, Yang J, Zhang G, Li J, Song L, Su Y, Shi Y, Zhang M, He J, Song D, Lv F, Li W, Wu Y, Wang H, Liu H, Zhou X, He T, Lu P (2020) Efficacy and safety of anti-CD19 CAR T cell therapy in 110 patients with B cell acute lymphoblastic leukemia with high-risk features. Blood Adv 4(10):2325–2338PubMedPubMedCentralCrossRef Zhang X, Lu XA, Yang J, Zhang G, Li J, Song L, Su Y, Shi Y, Zhang M, He J, Song D, Lv F, Li W, Wu Y, Wang H, Liu H, Zhou X, He T, Lu P (2020) Efficacy and safety of anti-CD19 CAR T cell therapy in 110 patients with B cell acute lymphoblastic leukemia with high-risk features. Blood Adv 4(10):2325–2338PubMedPubMedCentralCrossRef
11.
go back to reference Jiang H, Li C, Yin P, Guo T, Liu L, Xia L, Wu Y, Zhou F, Ai L, Shi W, Lu X, Wang H, Tang L, Wei Q, Deng J, Jin R, Xiong W, Dong J, Mei H, Hu Y (2019) Anti-CD19 chimeric antigen receptor-modified T cell therapy bridging to allogeneic hematopoietic stem cell transplantation for relapsed/refractory B cell acute lymphoblastic leukemia: an open-label pragmatic clinical trial. Am J Hematol 94(10):1113–1122PubMedCrossRef Jiang H, Li C, Yin P, Guo T, Liu L, Xia L, Wu Y, Zhou F, Ai L, Shi W, Lu X, Wang H, Tang L, Wei Q, Deng J, Jin R, Xiong W, Dong J, Mei H, Hu Y (2019) Anti-CD19 chimeric antigen receptor-modified T cell therapy bridging to allogeneic hematopoietic stem cell transplantation for relapsed/refractory B cell acute lymphoblastic leukemia: an open-label pragmatic clinical trial. Am J Hematol 94(10):1113–1122PubMedCrossRef
12.
go back to reference Park JH, Rivière I, Gonen M, Wang X, Sénéchal B, Curran KJ, Sauter C, Wang Y, Santomasso B, Mead E, Roshal M, Maslak P, Davila M, Brentjens RJ, Sadelain M (2018) Long-Term Follow-up of CD19 CAR Therapy in Acute Lymphoblastic Leukemia. N Engl J Med 378(5):449–459PubMedPubMedCentralCrossRef Park JH, Rivière I, Gonen M, Wang X, Sénéchal B, Curran KJ, Sauter C, Wang Y, Santomasso B, Mead E, Roshal M, Maslak P, Davila M, Brentjens RJ, Sadelain M (2018) Long-Term Follow-up of CD19 CAR Therapy in Acute Lymphoblastic Leukemia. N Engl J Med 378(5):449–459PubMedPubMedCentralCrossRef
13.
go back to reference Saadeh SS, Litzow MR (2018) Hematopoietic stem cell transplant in adults with acute lymphoblastic leukemia: the present state. Expert Rev Hematol 11(3):195–207PubMedCrossRef Saadeh SS, Litzow MR (2018) Hematopoietic stem cell transplant in adults with acute lymphoblastic leukemia: the present state. Expert Rev Hematol 11(3):195–207PubMedCrossRef
14.
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(19):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(19):2941–2951PubMedCrossRef
15.
go back to reference Bouziana S, Bouzianas D (2020) Exploring the dilemma of allogeneic hematopoietic cell transplantation after chimeric antigen receptor T cell herapy: to transplant or not? Biol Blood Marrow Transplant 26(8):e183–e191PubMedCrossRef Bouziana S, Bouzianas D (2020) Exploring the dilemma of allogeneic hematopoietic cell transplantation after chimeric antigen receptor T cell herapy: to transplant or not? Biol Blood Marrow Transplant 26(8):e183–e191PubMedCrossRef
16.
go back to reference Hay KA, Gauthier J, Hirayama AV, Voutsinas JM, Wu Q, Li D, Gooley TA, Cherian S, Chen X, Pender BS, Hawkins RM, Vakil A, Steinmetz RN, Schoch G, Chapuis AG, Till BG, Kiem HP, Ramos JD, Shadman M, Cassaday RD, Acharya UH, Riddell SR, Maloney DG, Turtle CJ (2019) Factors associated with durable EFS in adult B cell ALL patients achieving MRD-negative CR after CD19 CAR T cell therapy. Blood 133(15):1652–1663PubMedPubMedCentralCrossRef Hay KA, Gauthier J, Hirayama AV, Voutsinas JM, Wu Q, Li D, Gooley TA, Cherian S, Chen X, Pender BS, Hawkins RM, Vakil A, Steinmetz RN, Schoch G, Chapuis AG, Till BG, Kiem HP, Ramos JD, Shadman M, Cassaday RD, Acharya UH, Riddell SR, Maloney DG, Turtle CJ (2019) Factors associated with durable EFS in adult B cell ALL patients achieving MRD-negative CR after CD19 CAR T cell therapy. Blood 133(15):1652–1663PubMedPubMedCentralCrossRef
17.
go back to reference Zhao H, Wei J, Wei G, Luo Y, Shi J, Cui Q, Zhao M, Liang A, Zhang Q, Yang J, Li X, Chen J, Song X, Jing H, Li Y, Hao S, Wu W, Tan Y, Yu J, Zhao Y, Lai X, Yin ETS, Wei Y, Li P, Huang J, Wang T, Blaise D, Xiao L, Chang AH, Nagler A, Mohty M, Huang H, Hu Y (2020) Pre-transplant MRD negativity predicts favorable outcomes of CAR-T therapy followed by haploidentical HSCT for relapsed/refractory acute lymphoblastic leukemia: a multi-center retrospective study. J Hematol Oncol 13(1):42PubMedPubMedCentralCrossRef Zhao H, Wei J, Wei G, Luo Y, Shi J, Cui Q, Zhao M, Liang A, Zhang Q, Yang J, Li X, Chen J, Song X, Jing H, Li Y, Hao S, Wu W, Tan Y, Yu J, Zhao Y, Lai X, Yin ETS, Wei Y, Li P, Huang J, Wang T, Blaise D, Xiao L, Chang AH, Nagler A, Mohty M, Huang H, Hu Y (2020) Pre-transplant MRD negativity predicts favorable outcomes of CAR-T therapy followed by haploidentical HSCT for relapsed/refractory acute lymphoblastic leukemia: a multi-center retrospective study. J Hematol Oncol 13(1):42PubMedPubMedCentralCrossRef
18.
go back to reference Tu S, Huang R, Guo Z, Deng L, Song C, Zhou X, Yue C, Zhang L, He Y, Yang J, Liang Z, du J, Cao P, Li Y, Chang LJ, Li Y (2019) Shortening the ex vivo culture of CD19-specific CAR T cells retains potent efficacy against acute lymphoblastic leukemia without CAR T cell-related encephalopathy syndrome or severe cytokine release syndrome. Am J Hematol 94(12):E322–E325PubMedCrossRef Tu S, Huang R, Guo Z, Deng L, Song C, Zhou X, Yue C, Zhang L, He Y, Yang J, Liang Z, du J, Cao P, Li Y, Chang LJ, Li Y (2019) Shortening the ex vivo culture of CD19-specific CAR T cells retains potent efficacy against acute lymphoblastic leukemia without CAR T cell-related encephalopathy syndrome or severe cytokine release syndrome. Am J Hematol 94(12):E322–E325PubMedCrossRef
19.
go back to reference Hu L, Li M, Ding Y, Pu L, Liu J, Xie J, Cabanero M, Li J, Xiang R, Xiong S (2017) Prognostic value of RDW in cancers: a systematic review and meta-analysis. Oncotarget 8(9):16027–16035PubMedCrossRef Hu L, Li M, Ding Y, Pu L, Liu J, Xie J, Cabanero M, Li J, Xiang R, Xiong S (2017) Prognostic value of RDW in cancers: a systematic review and meta-analysis. Oncotarget 8(9):16027–16035PubMedCrossRef
20.
go back to reference Lee DW III, Stetler-Stevenson M, Yuan CM, Shah NN, Delbrook C, Yates B et al (2016) Long-term outcomes following CD19 CAR T cell therapy for B-ALL are superior in patients receiving a fludarabine/cyclophosphamide preparative regimen and post-CAR hematopoietic stem cell transplantation. Blood 128(22):218–218CrossRef Lee DW III, Stetler-Stevenson M, Yuan CM, Shah NN, Delbrook C, Yates B et al (2016) Long-term outcomes following CD19 CAR T cell therapy for B-ALL are superior in patients receiving a fludarabine/cyclophosphamide preparative regimen and post-CAR hematopoietic stem cell transplantation. Blood 128(22):218–218CrossRef
21.
go back to reference Turtle CJ, Hanafi LA, Berger C, Gooley TA, Cherian S, Hudecek M, Sommermeyer D, Melville K, Pender B, Budiarto TM, Robinson E, Steevens NN, Chaney C, Soma L, Chen X, Yeung C, Wood B, Li D, Cao J, Heimfeld S, Jensen MC, Riddell SR, Maloney DG (2016) CD19 CAR-T cells of defined CD4+:CD8+ composition in adult B cell ALL patients. J Clin Invest 126(6):2123–2138PubMedPubMedCentralCrossRef Turtle CJ, Hanafi LA, Berger C, Gooley TA, Cherian S, Hudecek M, Sommermeyer D, Melville K, Pender B, Budiarto TM, Robinson E, Steevens NN, Chaney C, Soma L, Chen X, Yeung C, Wood B, Li D, Cao J, Heimfeld S, Jensen MC, Riddell SR, Maloney DG (2016) CD19 CAR-T cells of defined CD4+:CD8+ composition in adult B cell ALL patients. J Clin Invest 126(6):2123–2138PubMedPubMedCentralCrossRef
22.
go back to reference Zhai Z (2018) Factors influencing efficacy of CD19-CAR-T cells in children and adults with relapsed/refractory B cell lymphoblastic leukemia. Blood 132(Supplement 1):2656CrossRef Zhai Z (2018) Factors influencing efficacy of CD19-CAR-T cells in children and adults with relapsed/refractory B cell lymphoblastic leukemia. Blood 132(Supplement 1):2656CrossRef
23.
go back to reference Jacoby E, Bielorai B, Avigdor A, Itzhaki O, Hutt D, Nussboim V, Meir A, Kubi A, Levy M, Zikich D, Zeltzer LA, Brezinger K, Schachter J, Nagler A, Besser MJ, Toren A (2018) Locally produced CD19 CAR T cells leading to clinical remissions in medullary and extramedullary relapsed acute lymphoblastic leukemia. Am J Hematol 93(12):1485–1492PubMedCrossRef Jacoby E, Bielorai B, Avigdor A, Itzhaki O, Hutt D, Nussboim V, Meir A, Kubi A, Levy M, Zikich D, Zeltzer LA, Brezinger K, Schachter J, Nagler A, Besser MJ, Toren A (2018) Locally produced CD19 CAR T cells leading to clinical remissions in medullary and extramedullary relapsed acute lymphoblastic leukemia. Am J Hematol 93(12):1485–1492PubMedCrossRef
24.
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(5):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(5):439–448PubMedPubMedCentralCrossRef
25.
go back to reference Cao J, Cheng H, Qi K, Chen W, Shi M, Zheng J, Xu K (2019) Humanized CD19-specific chimeric antigen receptor T cells for acute lymphoblastic leukemia. Blood 134:3872CrossRef Cao J, Cheng H, Qi K, Chen W, Shi M, Zheng J, Xu K (2019) Humanized CD19-specific chimeric antigen receptor T cells for acute lymphoblastic leukemia. Blood 134:3872CrossRef
26.
go back to reference Curran KJ, Margossian SP, Kernan NA, Silverman LB, Williams DA, Shukla N, Kobos R, Forlenza CJ, Steinherz P, Prockop S, Boulad F, Spitzer B, Cancio MI, Boelens JJ, Kung AL, Khakoo Y, Szenes V, Park JH, Sauter CS, Heller G, Wang X, Senechal B, O’Reilly RJ, Riviere I, Sadelain M, Brentjens RJ (2019) Toxicity and response after CD19-specific CAR T cell therapy in pediatric/young adult relapsed/refractory B-ALL. Blood 134(26):2361–2368PubMedPubMedCentralCrossRef Curran KJ, Margossian SP, Kernan NA, Silverman LB, Williams DA, Shukla N, Kobos R, Forlenza CJ, Steinherz P, Prockop S, Boulad F, Spitzer B, Cancio MI, Boelens JJ, Kung AL, Khakoo Y, Szenes V, Park JH, Sauter CS, Heller G, Wang X, Senechal B, O’Reilly RJ, Riviere I, Sadelain M, Brentjens RJ (2019) Toxicity and response after CD19-specific CAR T cell therapy in pediatric/young adult relapsed/refractory B-ALL. Blood 134(26):2361–2368PubMedPubMedCentralCrossRef
27.
go back to reference Finney OC, Brakke HM, Rawlings-Rhea S, Hicks R, Doolittle D, Lopez M et al (2019) CD19 CAR T cell product and disease attributes predict leukemia remission durability. J Clin Invest 129(5):2123–2132PubMedPubMedCentralCrossRef Finney OC, Brakke HM, Rawlings-Rhea S, Hicks R, Doolittle D, Lopez M et al (2019) CD19 CAR T cell product and disease attributes predict leukemia remission durability. J Clin Invest 129(5):2123–2132PubMedPubMedCentralCrossRef
28.
go back to reference Zuo YX, Jia YP, Wu J, Wang JB, Lu AD, Dong LJ et al (2019) Chimeric antigen receptors T cells for treatment of 48 relapsed or refractory acute lymphoblastic leukemia children: long term follow-up outcomes. Zhonghua Xue Ye Xue Za Zhi 40(4):270–275PubMed Zuo YX, Jia YP, Wu J, Wang JB, Lu AD, Dong LJ et al (2019) Chimeric antigen receptors T cells for treatment of 48 relapsed or refractory acute lymphoblastic leukemia children: long term follow-up outcomes. Zhonghua Xue Ye Xue Za Zhi 40(4):270–275PubMed
29.
go back to reference Frey NV, Shaw PA, Hexner EO, Pequignot E, Gill S, Luger SM, Mangan JK, Loren AW, Perl AE, Maude SL, Grupp SA, Shah NN, Gilmore J, Lacey SF, Melenhorst JJ, Levine BL, June CH, Porter DL (2020) Optimizing chimeric antigen receptor T cell therapy for adults with acute lymphoblastic leukemia. J Clin Oncol 38(5):415–422PubMedCrossRef Frey NV, Shaw PA, Hexner EO, Pequignot E, Gill S, Luger SM, Mangan JK, Loren AW, Perl AE, Maude SL, Grupp SA, Shah NN, Gilmore J, Lacey SF, Melenhorst JJ, Levine BL, June CH, Porter DL (2020) Optimizing chimeric antigen receptor T cell therapy for adults with acute lymphoblastic leukemia. J Clin Oncol 38(5):415–422PubMedCrossRef
30.
go back to reference Wang J, Mou N, Yang Z, Li Q, Jiang Y, Meng J, Liu X, Deng Q (2020) Efficacy and safety of humanized anti-CD19-CAR-T therapy following intensive lymphodepleting chemotherapy for refractory/relapsed B acute lymphoblastic leukaemia. Br J Haematol 191:212–222PubMedPubMedCentralCrossRef Wang J, Mou N, Yang Z, Li Q, Jiang Y, Meng J, Liu X, Deng Q (2020) Efficacy and safety of humanized anti-CD19-CAR-T therapy following intensive lymphodepleting chemotherapy for refractory/relapsed B acute lymphoblastic leukaemia. Br J Haematol 191:212–222PubMedPubMedCentralCrossRef
31.
go back to reference Liu J, Zhang X, Zhong JF, Zhang C (2017) CAR-T cells and allogeneic hematopoietic stem cell transplantation for relapsed/refractory B cell acute lymphoblastic leukemia. Immunotherapy 9(13):1115–1125PubMedCrossRef Liu J, Zhang X, Zhong JF, Zhang C (2017) CAR-T cells and allogeneic hematopoietic stem cell transplantation for relapsed/refractory B cell acute lymphoblastic leukemia. Immunotherapy 9(13):1115–1125PubMedCrossRef
32.
go back to reference June CH, Maus MV, Plesa G, Johnson LA, Zhao Y, Levine BL, Grupp SA, Porter DL (2014) Engineered T cells for cancer therapy. Cancer Immunol Immunother 63(9):969–975PubMedPubMedCentralCrossRef June CH, Maus MV, Plesa G, Johnson LA, Zhao Y, Levine BL, Grupp SA, Porter DL (2014) Engineered T cells for cancer therapy. Cancer Immunol Immunother 63(9):969–975PubMedPubMedCentralCrossRef
33.
go back to reference Pan J, Niu Q, Deng B, Liu S, Wu T, Gao Z, Liu Z, Zhang Y, Qu X, Zhang Y, Liu S, Ling Z, Lin Y, Zhao Y, Song Y, Tan X, Zhang Y, Li Z, Yin Z, Chen B, Yu X, Yan J, Zheng Q, Zhou X, Gao J, Chang AH, Feng X, Tong C (2019) CD22 CAR T cell therapy in refractory or relapsed B acute lymphoblastic leukemia. Leukemia 33(12):2854–2866PubMedCrossRef Pan J, Niu Q, Deng B, Liu S, Wu T, Gao Z, Liu Z, Zhang Y, Qu X, Zhang Y, Liu S, Ling Z, Lin Y, Zhao Y, Song Y, Tan X, Zhang Y, Li Z, Yin Z, Chen B, Yu X, Yan J, Zheng Q, Zhou X, Gao J, Chang AH, Feng X, Tong C (2019) CD22 CAR T cell therapy in refractory or relapsed B acute lymphoblastic leukemia. Leukemia 33(12):2854–2866PubMedCrossRef
34.
go back to reference Jia H, Wang Z, Wang Y, Liu Y, Dai H, Tong C, Guo Y, Guo B, Ti D, Han X, Yang Q, Wu Z, Han W (2019) Haploidentical CD19/CD22 bispecific CAR-T cells induced MRD-negative remission in a patient with relapsed and refractory adult B-ALL after haploidentical hematopoietic stem cell transplantation. J Hematol Oncol 12(1):57PubMedPubMedCentralCrossRef Jia H, Wang Z, Wang Y, Liu Y, Dai H, Tong C, Guo Y, Guo B, Ti D, Han X, Yang Q, Wu Z, Han W (2019) Haploidentical CD19/CD22 bispecific CAR-T cells induced MRD-negative remission in a patient with relapsed and refractory adult B-ALL after haploidentical hematopoietic stem cell transplantation. J Hematol Oncol 12(1):57PubMedPubMedCentralCrossRef
35.
go back to reference Pehlivan KC, Duncan BB, Lee DW (2018) CAR-T cell therapy for acute lymphoblastic leukemia: transforming the treatment of relapsed and refractory Disease. Curr Hematol Malig Rep 13(5):396–406PubMedCrossRef Pehlivan KC, Duncan BB, Lee DW (2018) CAR-T cell therapy for acute lymphoblastic leukemia: transforming the treatment of relapsed and refractory Disease. Curr Hematol Malig Rep 13(5):396–406PubMedCrossRef
36.
go back to reference Li L, Liu J, Xu M, Yu H, Lv C, Cao F, Wang Z, Fu Y, Zhang M, Meng H, Zhang X, Kang L, Zhang Z, Li J, Feng J, Lian X, Yu L, Zhou J (2020) Treatment response, survival, safety, and predictive factors to chimeric antigen receptor T cell therapy in Chinese relapsed or refractory B cell acute lymphoblast leukemia patients. Cell Death Dis 11(3):207PubMedPubMedCentralCrossRef Li L, Liu J, Xu M, Yu H, Lv C, Cao F, Wang Z, Fu Y, Zhang M, Meng H, Zhang X, Kang L, Zhang Z, Li J, Feng J, Lian X, Yu L, Zhou J (2020) Treatment response, survival, safety, and predictive factors to chimeric antigen receptor T cell therapy in Chinese relapsed or refractory B cell acute lymphoblast leukemia patients. Cell Death Dis 11(3):207PubMedPubMedCentralCrossRef
37.
go back to reference Lin JK, Lerman BJ, Barnes JI, Boursiquot BC, Tan YJ, Robinson AQL, Davis KL, Owens DK, Goldhaber-Fiebert JD (2018) Cost effectiveness of chimeric antigen receptor T cell therapy in relapsed or refractory pediatric B cell acute lymphoblastic leukemia. J Clin Oncol 36(32):3192–3202PubMedCrossRef Lin JK, Lerman BJ, Barnes JI, Boursiquot BC, Tan YJ, Robinson AQL, Davis KL, Owens DK, Goldhaber-Fiebert JD (2018) Cost effectiveness of chimeric antigen receptor T cell therapy in relapsed or refractory pediatric B cell acute lymphoblastic leukemia. J Clin Oncol 36(32):3192–3202PubMedCrossRef
38.
go back to reference Whittington MD, McQueen RB, Ollendorf DA, Kumar VM, Chapman RH, Tice JA, Pearson SD, Campbell JD (2018) Long-term survival and value of chimeric antigen receptor T cell therapy for pediatric patients with relapsed or refractory leukemia. JAMA Pediatr 172(12):1161–1168PubMedPubMedCentralCrossRef Whittington MD, McQueen RB, Ollendorf DA, Kumar VM, Chapman RH, Tice JA, Pearson SD, Campbell JD (2018) Long-term survival and value of chimeric antigen receptor T cell therapy for pediatric patients with relapsed or refractory leukemia. JAMA Pediatr 172(12):1161–1168PubMedPubMedCentralCrossRef
39.
go back to reference Sarkar RR, Gloude NJ, Schiff D, Murphy JD (2019) Cost-effectiveness of chimeric antigen receptor T cell therapy in pediatric relapsed/refractory B cell acute lymphoblastic leukemia. J Natl Cancer Inst 111(7):719–726PubMedCrossRef Sarkar RR, Gloude NJ, Schiff D, Murphy JD (2019) Cost-effectiveness of chimeric antigen receptor T cell therapy in pediatric relapsed/refractory B cell acute lymphoblastic leukemia. J Natl Cancer Inst 111(7):719–726PubMedCrossRef
40.
go back to reference Zhao Z, Condomines M, van der Stegen SJC, Perna F, Kloss CC, Gunset G, Plotkin J, Sadelain M (2015) Structural design of engineered costimulation determines tumor rejection kinetics and persistence of CAR T cell. Cancer Cell 28(4):415–428PubMedPubMedCentralCrossRef Zhao Z, Condomines M, van der Stegen SJC, Perna F, Kloss CC, Gunset G, Plotkin J, Sadelain M (2015) Structural design of engineered costimulation determines tumor rejection kinetics and persistence of CAR T cell. Cancer Cell 28(4):415–428PubMedPubMedCentralCrossRef
41.
go back to reference Kawalekar OU, O'Connor RS, Fraietta JA, Guo L, McGettigan SE, Posey AD Jr et al (2016) Distinct signaling of coreceptors regulates specific metabolism pathways and impacts memory development in CAR T cells. Immunity 44(2):380–390PubMedCrossRef Kawalekar OU, O'Connor RS, Fraietta JA, Guo L, McGettigan SE, Posey AD Jr et al (2016) Distinct signaling of coreceptors regulates specific metabolism pathways and impacts memory development in CAR T cells. Immunity 44(2):380–390PubMedCrossRef
42.
go back to reference Salter AI, Ivey RG, Kennedy JJ, Voillet V, Rajan A, Alderman EJ et al (2018) Phosphoproteomic analysis of chimeric antigen receptor signaling reveals kinetic and quantitative differences that affect cell function. Sci Signal 11(544):eaat6753 Salter AI, Ivey RG, Kennedy JJ, Voillet V, Rajan A, Alderman EJ et al (2018) Phosphoproteomic analysis of chimeric antigen receptor signaling reveals kinetic and quantitative differences that affect cell function. Sci Signal 11(544):eaat6753
43.
go back to reference Hematology Oncology Committee, C.A.-C.A., Leukemia, and C.S.o.H.C.M.A. Lymphoma Group (2016) Chinese guidelines for diagnosis and treatment of acute lymphoblastic leukemia(2016). Zhonghua Xue Ye Xue Za Zhi 37(10):837–845 Hematology Oncology Committee, C.A.-C.A., Leukemia, and C.S.o.H.C.M.A. Lymphoma Group (2016) Chinese guidelines for diagnosis and treatment of acute lymphoblastic leukemia(2016). Zhonghua Xue Ye Xue Za Zhi 37(10):837–845
44.
go back to reference Brown PA, Wieduwilt M, Logan A, DeAngelo DJ, Wang ES, Fathi A, Cassaday RD, Litzow M, Advani A, Aoun P, Bhatnagar B, Boyer MW, Bryan T, Burke PW, Coccia PF, Coutre SE, Jain N, Kirby S, Liu A, Massaro S, Mattison RJ, Oluwole O, Papadantonakis N, Park J, Rubnitz JE, Uy GL, Gregory KM, Ogba N, Shah B (2019) Guidelines insights: acute lymphoblastic leukemia, version 1.2019. J Natl Compr Cancer Netw 17(5):414–423CrossRef Brown PA, Wieduwilt M, Logan A, DeAngelo DJ, Wang ES, Fathi A, Cassaday RD, Litzow M, Advani A, Aoun P, Bhatnagar B, Boyer MW, Bryan T, Burke PW, Coccia PF, Coutre SE, Jain N, Kirby S, Liu A, Massaro S, Mattison RJ, Oluwole O, Papadantonakis N, Park J, Rubnitz JE, Uy GL, Gregory KM, Ogba N, Shah B (2019) Guidelines insights: acute lymphoblastic leukemia, version 1.2019. J Natl Compr Cancer Netw 17(5):414–423CrossRef
45.
go back to reference Inaba H, Greaves M, Mullighan CG (2013) Acute lymphoblastic leukaemia. Lancet 381(9881):1943–1955PubMedCrossRef Inaba H, Greaves M, Mullighan CG (2013) Acute lymphoblastic leukaemia. Lancet 381(9881):1943–1955PubMedCrossRef
46.
go back to reference Putter H, van Houwelingen HC (2017) Understanding landmarking and its relation with time-dependent Cox Regression. Stat Biosci 9(2):489–503PubMedCrossRef Putter H, van Houwelingen HC (2017) Understanding landmarking and its relation with time-dependent Cox Regression. Stat Biosci 9(2):489–503PubMedCrossRef
47.
go back to reference Mi X, Hammill BG, Curtis LH, Lai EC, Setoguchi S (2016) Use of the landmark method to address immortal person-time bias in comparative effectiveness research: a simulation study. Stat Med 35(26):4824–4836PubMedCrossRef Mi X, Hammill BG, Curtis LH, Lai EC, Setoguchi S (2016) Use of the landmark method to address immortal person-time bias in comparative effectiveness research: a simulation study. Stat Med 35(26):4824–4836PubMedCrossRef
Metadata
Title
Anti-CD19 CAR-T cell therapy bridge to HSCT decreases the relapse rate and improves the long-term survival of R/R B-ALL patients: a systematic review and meta-analysis
Authors
Linhui Hu
Alice Charwudzi
Qian Li
Weiwei Zhu
Qianshan Tao
Shudao Xiong
Zhimin Zhai
Publication date
01-04-2021
Publisher
Springer Berlin Heidelberg
Published in
Annals of Hematology / Issue 4/2021
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-021-04451-w

Other articles of this Issue 4/2021

Annals of Hematology 4/2021 Go to the issue