Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Optimal timing and impact of allogeneic peripheral blood stem cell transplantation in adult T-cell lymphoblastic lymphoma: insights from a large cohort multi-center real-world study in Shanghai

Abstract

In this real-world study, 153 adult T-cell lymphoblastic lymphoma (T-LBL) patients from sixteen centers in Shanghai were enrolled. Out of them, 103 (67.3%) achieved complete remission (CR). The 2-year overall survival (OS) and progression-free survival (PFS) were 56.3% and 47.6%, respectively. In multivariate analysis, CR after induction treatment significantly improved the OS (p = 0.002) and PFS (p = 0.001). Among CR patients, allogeneic peripheral blood stem cell transplantation (allo-PBSCT) significantly lowered the cumulative incidence of relapse (CIR) compared to autologous PBSCT (p = 0.043) and non-SCT (p = 0.001). Among patients undergoing allo-PBSCT in CR, early (within four induction courses) and late CR (after four induction courses) didn’t impact the prognosis with similar 2-year OS (p = 0.590), PFS (p = 0.858), CIR (p = 0.50), and non-relapse mortality (NRM) (p = 0.110). Early and deferred allo-PBSCT for early CR patients also yielded similar 2-year OS (p = 0.640), PFS (p = 0.970), CIR (p = 0.994), and NRM (p = 0.974). As a time-dependent covariate, allo-PBSCT presented a positive effect on PFS (p = 0.018) and had a trend toward better OS (p = 0.064). These data suggested that allo-PBSCT should be considered for T-LBL patients upon achieving CR to enhance survival and reduce relapse risk.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Flowchart of induction treatment response and survival in adult T-LBL patients.
Fig. 2: Outcomes of adult T-LBL patients achieving CR based on auto-, allo-PBSCT, and non-SCT.
Fig. 3: Outcomes of adult T-LBL patients based on early/ late CR before allo-PBSCT.
Fig. 4: Outcomes of adult T-LBL patients based on early/ deferred allo-PBSCT after achieving early CR.

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Cortelazzo S, Ferreri A, Hoelzer D, Ponzoni M. Lymphoblastic lymphoma. Crit Rev Oncol Hematol. 2017;113:304–17.

    Article  PubMed  Google Scholar 

  2. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al. WHO classification of tumours of haematopoietic and lymphoid tissues. vol 2. International agency for research on cancer Lyon, France; 2008.

  3. Thomas DA, O’Brien S, Cortes J, Giles FJ, Faderl S, Verstovsek S, et al. Outcome with the hyper-CVAD regimens in lymphoblastic lymphoma. Blood. 2004;104:1624–30.

    Article  PubMed  CAS  Google Scholar 

  4. Hoelzer D, Gökbuget N, Digel W, Faak T, Kneba M, Reutzel R, et al. Outcome of adult patients with T-lymphoblastic lymphoma treated according to protocols for acute lymphoblastic leukemia. Blood. 2002;99:4379–85.

    Article  PubMed  CAS  Google Scholar 

  5. Huguet F, Leguay T, Raffoux E, Thomas X, Beldjord K, Delabesse E, et al. Pediatric-inspired therapy in adults with Philadelphia chromosome-negative acute lymphoblastic leukemia: the GRAALL-2003 study. J Clin Oncol. 2009;27:911–8.

    Article  PubMed  CAS  Google Scholar 

  6. Burkhardt B, Reiter A, Landmann E, Lang P, Lassay L, Dickerhoff R, et al. Poor outcome for children and adolescents with progressive disease or relapse of lymphoblastic lymphoma: a report from the Berlin-Frankfurt-Muenster group. J Clin Oncol. 2009;27:3363–9.

    Article  PubMed  Google Scholar 

  7. Song KW, Barnett MJ, Gascoyne RD, Chhanabhai M, Forrest DL, Hogge DE, et al. Primary therapy for adults with T-cell lymphoblastic lymphoma with hematopoietic stem-cell transplantation results in favorable outcomes. Ann Oncol. 2007;18:535–40.

    Article  PubMed  CAS  Google Scholar 

  8. Yang L, Tan Y, Shi J, Zhao Y, Zhu Y, Hu Y, et al. Allogeneic hematopoietic stem cell transplantation should be in preference to conventional chemotherapy as post-remission treatment for adults with lymphoblastic lymphoma. Bone Marrow Transpl. 2018;53:1340–4.

    Article  CAS  Google Scholar 

  9. Li Z, Zhang B, Fan X, Gui R, Yu F, Wang J, et al. Selection of hematopoietic stem cell transplantation for T-cell lymphoblastic lymphoma. Front Oncol. 2023;13:1193237.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Levine JE, Harris RE, Loberiza FR Jr, Armitage JO, Vose JM, Van Besien K, et al. A comparison of allogeneic and autologous bone marrow transplantation for lymphoblastic lymphoma. Blood. 2003;101:2476–82.

    Article  PubMed  CAS  Google Scholar 

  11. Hunault M, Truchan-Graczyk M, Caillot D, Harousseau JL, Bologna S, Himberlin C, et al. Outcome of adult T-lymphoblastic lymphoma after acute lymphoblastic leukemia-type treatment: a GOELAMS trial. Haematologica. 2007;92:1623–30.

    Article  PubMed  CAS  Google Scholar 

  12. Luo L, Jiao Y, Li Y, Yang P, Gao J, Huang S, et al. Efficacy and prognostic factors of allogeneic hematopoietic stem cell transplantation treatment for adolescent and adult Tlymphoblastic leukemia /lymphoma: a large cohort multicenter study in China. Ann Hematol. 2024;103:2073–87.

    Article  PubMed  CAS  Google Scholar 

  13. Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, Le Beau MM, et al. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016;127:2391–405.

    Article  PubMed  CAS  Google Scholar 

  14. Shi Y, Liu P, Zhou S, Yang J, Han X, He X, et al. Comparison of CBV, BEAM and BEAC high-dose chemotherapy followed by autologous hematopoietic stem cell transplantation in non-Hodgkin lymphoma: Efficacy and toxicity. Asia Pac J Clin Oncol. 2017;13:e423–e429.

    Article  PubMed  Google Scholar 

  15. Niu J, Chen Z, Gao J, Qiu H, Wan L, Wang Y, et al. Total body irradiation-based conditioning regimen improved the survival of adult patients with T-Cell lymphoblastic lymphoma after allogeneic peripheral blood stem cell transplantation. Cell Transpl. 2022;31:9636897221108890.

  16. Xu X, Yang J, Cai Y, Li S, Niu J, Zhou K, et al. Low dose anti-thymocyte globulin with low dose posttransplant cyclophosphamide (low dose ATG/PTCy) can reduce the risk of graft-versus-host disease as compared with standard-dose anti-thymocyte globulin in haploidentical peripheral hematopoietic stem cell transplantation combined with unrelated cord blood. Bone Marrow Transpl. 2021;56:705–8.

    Article  CAS  Google Scholar 

  17. Yang J, Jiang J, Cai Y, Li S, Wan L, Zhu J, et al. Low-dose anti-thymocyte globulin plus low-dose posttransplant cyclophosphamide as graft-versus-host disease prophylaxis in haploidentical peripheral blood stem cell transplantation combined with unrelated cord blood for patients with hematologic malignancies: a prospective, phase II study. Bone Marrow Transpl. 2019;54:1049–57.

    Article  CAS  Google Scholar 

  18. Grommes C, Rubenstein JL, DeAngelis LM, Ferreri AJM, Batchelor TT. Comprehensive approach to diagnosis and treatment of newly diagnosed primary CNS lymphoma. Neuro Oncol. 2019;21:296–305.

    Article  PubMed  Google Scholar 

  19. Li C, Wuxiao ZJ, Chen X, Chen G, Lu Y, Xia Z, et al. A Modified NHL-BFM-95 Regimen Produces Better Outcome Than HyperCVAD in adult patients with T-Lymphoblastic lymphoma, a two-institution experience. Cancer Res Treat. 2020;52:573–85.

    Article  PubMed  CAS  Google Scholar 

  20. Coustan-Smith E, Mullighan CG, Onciu M, Behm FG, Raimondi SC, Pei D, et al. Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. Lancet Oncol. 2009;10:147–56.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Zucca E, et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32:3059–68.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Przepiorka D, Weisdorf D, Martin P, Klingemann HG, Beatty P, Hows J, et al. Consensus conference on acute GVHD grading. Bone Marrow Transpl. 1995;15:825–8.

    CAS  Google Scholar 

  23. Martin PJ, Lee SJ, Przepiorka D, Horowitz MM, Koreth J, Vogelsang GB, et al. National Institutes of Health Consensus development project on criteria for clinical trials in chronic graft-versus-host disease: VI. The 2014 clinical trial design working group report. Biol Blood Marrow Transpl. 2015;21:1343–59.

    Article  Google Scholar 

  24. Lepretre S, Touzart A, Vermeulin T, Picquenot JM, Tanguy-Schmidt A, Salles G, et al. Pediatric-Like Acute Lymphoblastic Leukemia Therapy in Adults With Lymphoblastic Lymphoma: The GRAALL-LYSA LL03 Study. J Clin Oncol. 2016;34:572–80.

    Article  PubMed  CAS  Google Scholar 

  25. Jeong SH, Moon JH, Kim JS, Yang DH, Park Y, Cho SG, et al. Multicenter analysis of treatment outcomes in adult patients with lymphoblastic lymphoma who received hyper-CVAD induction followed by hematopoietic stem cell transplantation. Ann Hematol. 2015;94:617–25.

    Article  PubMed  CAS  Google Scholar 

  26. Zhu MY, Wang H, Huang CY, Xia ZJ, Chen XQ, Geng QR, et al. A childhood chemotherapy protocol improves overall survival among adults with T-lymphoblastic lymphoma. Oncotarget. 2016;7:38884–91.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Jain N, Lamb AV, O’Brien S, Ravandi F, Konopleva M, Jabbour E, et al. Early T-cell precursor acute lymphoblastic leukemia/lymphoma (ETP-ALL/LBL) in adolescents and adults: a high-risk subtype. Blood. 2016;127:1863–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Morita K, Jain N, Kantarjian H, Takahashi K, Fang H, Konopleva M, et al. Outcome of T-cell acute lymphoblastic leukemia/lymphoma: Focus on near-ETP phenotype and differential impact of nelarabine. Am J Hematol. 2021;96:589–98.

    Article  PubMed  CAS  Google Scholar 

  29. Zappone E, Cencini E, Defina M, Sicuranza A, Gozzetti A, Ciofini S, et al. Venetoclax in association with decitabine as effective bridge to transplant in a case of relapsed early T-cell lymphoblastic leukemia. Clin Case Rep. 2020;8:2000–2.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Numan Y, Alfayez M, Maiti A, Alvarado Y, Jabbour EJ, Ferrajoli A, et al. First report of clinical response to Venetoclax in Early T-cell Precursor Acute Lymphoblastic Leukemia. JCO Precis Oncol. 2018;2:PO.18.00127.

  31. Chonghaile TN, Roderick JE, Glenfield C, Ryan J, Sallan SE, Silverman LB, et al. Maturation stage of T-cell acute lymphoblastic leukemia determines BCL-2 versus BCL-XL dependence and sensitivity to ABT-199. Cancer Discov. 2014;4:1074–87.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Goldstone AH, Richards SM, Lazarus HM, Tallman MS, Buck G, Fielding AK, et al. In adults with standard-risk acute lymphoblastic leukemia, the greatest benefit is achieved from a matched sibling allogeneic transplantation in first complete remission, and an autologous transplantation is less effective than conventional consolidation/maintenance chemotherapy in all patients: final results of the International ALL Trial (MRC UKALL XII/ECOG E2993). Blood. 2008;111:1827–33.

    Article  PubMed  CAS  Google Scholar 

  33. Lv M, Shen M, Mo X. Development of allogeneic hematopoietic stem cell transplantation in 2022: Regenerating “Groot” to heal the world. Innovation. 2023;4:100373

    PubMed  PubMed Central  Google Scholar 

  34. Hochberg J, Khaled S, Forman SJ, Cairo MS. Criteria for and outcomes of allogeneic haematopoietic stem cell transplant in children, adolescents and young adults with acute lymphoblastic leukaemia in first complete remission. Br J Haematol. 2013;161:27–42.

    Article  PubMed  CAS  Google Scholar 

  35. Herzig RH, Bortin MM, Barrett AJ, Blume KG, Gluckman E, Horowitz MM, et al. Bone-marrow transplantation in high-risk acute lymphoblastic leukaemia in first and second remission. Lancet. 1987;1:786–9.

    Article  PubMed  CAS  Google Scholar 

  36. Marks DI, Alonso L, Radia R. Allogeneic hematopoietic cell transplantation in adult patients with acute lymphoblastic leukemia. Hematol Oncol Clin North Am. 2014;28:995–1009.

    Article  PubMed  Google Scholar 

  37. Gossai NP, Devidas M, Chen Z, Wood BL, Zweidler-McKay PA, Rabin KR, et al. Central nervous system status is prognostic in T-cell acute lymphoblastic leukemia: a Children’s Oncology Group report. Blood. 2023;141:1802–11.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge all authors and patients participating in this study. This work was supported by National Key R&D Program of China (2019YFA0111000 for Song X), a three-year development project from Shanghai Shen Kang Hospital Development Center (SHDC2020CR1012B for Song X), the National Natural Science Foundation of China (81570148 for Song X), and the Clinical Research Innovation Plan of Shanghai General Hospital (CCTR-2022C04 for Niu J).

Author information

Authors and Affiliations

Contributions

Xianmin Song and Rong Tao conceptualized and/or supervised the study. Fangfang Yu and Jiahua Niu analyzed the data and plotted the figures. Jianmin Yang, Jian Hou, Siguo Hao, Aibin Liang, Hong Xiong, Qi Zhu, Ligen Liu, Jun Shi, Juan Du, Bobin Chen, Rong Wei, Wenli Zhao, Lihua Sun, and Yunhua Hou provided patients’ clinical data. Fangfang Yu wrote the manuscript. Xianmin Song revised the manuscript. All authors have read and approved the final version of the manuscript.

Corresponding authors

Correspondence to Rong Tao or Xianmin Song.

Ethics declarations

Competing interests

The authors declare no competing interests.

Patient consent statement

The studies involving humans were approved by Ethics Committee of Shanghai General Hospital. The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent for participation was not required from the participants or the participants’ legal guardians/next of kin in accordance with national legislation and institutional requirements.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, F., Niu, J., Yang, J. et al. Optimal timing and impact of allogeneic peripheral blood stem cell transplantation in adult T-cell lymphoblastic lymphoma: insights from a large cohort multi-center real-world study in Shanghai. Bone Marrow Transplant 60, 380–388 (2025). https://doi.org/10.1038/s41409-024-02500-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41409-024-02500-2

Search

Quick links