Allogeneic hematopoietic stem cell transplantation for NK/T-cell lymphoma: an international collaborative analysis.


Journal

Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895

Informations de publication

Date de publication:
07 2023
Historique:
received: 13 03 2023
accepted: 27 04 2023
revised: 22 04 2023
medline: 5 7 2023
pubmed: 9 5 2023
entrez: 8 5 2023
Statut: ppublish

Résumé

Natural killer/T-cell lymphomas (NKTCL) represent rare and aggressive lymphoid malignancies. Patients (pts) with relapsed/refractory disease after Asparaginase (ASPA)-based chemotherapy have a dismal prognosis. To better define the role of allogeneic hematopoietic stem cell transplantation (allo-HSCT), we conducted a retrospective analysis of data shared with the European Society for Blood and Marrow Transplantation (EBMT) and cooperating Asian centers. We identified 135 pts who received allo-HSCT between 2010 and 2020. Median age was 43.4 years at allo-HSCT, 68.1% were male. Ninety-seven pts (71.9 %) were European, 38 pts (28.1%) Asian. High Prognostic Index for NKTCL (PINK) scores were reported for 44.4%; 76.3% had >1 treatment, 20.7% previous auto-HSCT, and 74.1% ASPA-containing regimens prior to allo-HSCT. Most (79.3%) pts were transplanted in CR/PR. With a median follow-up of 4.8 years, 3-year progression-free(PFS) and overall survival were 48.6% (95%-CI:39.5-57%) and 55.6% (95%-CI:46.5-63.8%). Non-relapse mortality at 1 year was 14.8% (95%-CI:9.3-21.5%) and 1-year relapse incidence 29.6% (95%-CI:21.9-37.6%). In multivariate analyses, shorter time interval (0-12 months) between diagnosis and allo-HSCT [HR = 2.12 (95%-CI:1.03-4.34); P = 0.04] and transplantation not in CR/PR [HR = 2.20 (95%-CI:0.98-4.95); P = 0.056] reduced PFS. Programmed cell death protein 1(PD-1/PD-L1) treatment before HSCT neither increased GVHD nor impacted survival. We demonstrate that allo-HSCT can achieve long-term survival in approximately half of pts allografted for NKTCL.

Identifiants

pubmed: 37157017
doi: 10.1038/s41375-023-01924-x
pii: 10.1038/s41375-023-01924-x
pmc: PMC10166457
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1511-1520

Informations de copyright

© 2023. The Author(s).

Références

Alaggio R, Amador C, Anagnostopoulos I, Attygalle AD, Araujo IBO, Berti E, et al. The 5th edition of the World Health Organization Classification of haematolymphoid tumours: lymphoid neoplasms. Leukemia. 2022;36:1720–48.
doi: 10.1038/s41375-022-01620-2 pubmed: 35732829 pmcid: 9214472
Kwong YL, Anderson BO, Advani R, Kim WS, Levine AM, Lim ST, et al. Management of T-cell and natural-killer-cell neoplasms in Asia: consensus statement from the Asian Oncology Summit 2009. Lancet Oncol. 2009;10:1093–101.
doi: 10.1016/S1470-2045(09)70265-7 pubmed: 19880063
Kim SJ, Choi JY, Hyun SH, Ki CS, Oh D, Ahn YC, et al. Risk stratification on the basis of Deauville score on PET-CT and the presence of Epstein-Barr virus DNA after completion of primary treatment for extranodal natural killer/T-cell lymphoma, nasal type: a multicentre, retrospective analysis. Lancet Haematol. 2015;2:e66–74.
doi: 10.1016/S2352-3026(15)00002-2 pubmed: 26687611
Yamaguchi M, Kita K, Miwa H, Nishii K, Oka K, Ohno T, et al. Frequent expression of P-glycoprotein/MDR1 by nasal T-cell lymphoma cells. Cancer. 1995;76:2351–6.
doi: 10.1002/1097-0142(19951201)76:11<2351::AID-CNCR2820761125>3.0.CO;2-1 pubmed: 8635042
Qi SN, Yang Y, Song YQ, Wang Y, He X, Hu C, et al. First-line non-anthracycline-based chemotherapy for extranodal nasal-type NK/T-cell lymphoma: a retrospective analysis from the CLCG. Blood Adv. 2020;4:3141–53.
doi: 10.1182/bloodadvances.2020001852 pubmed: 32658985 pmcid: 7362384
Yamaguchi M, Kwong YL, Kim WS, Maeda Y, Hashimoto C, Suh C, et al. Phase II study of SMILE chemotherapy for newly diagnosed stage IV, relapsed, or refractory extranodal natural killer (NK)/T-cell lymphoma, nasal type: the NK-Cell Tumor Study Group study. J Clin Oncol. 2011;29:4410–6.
doi: 10.1200/JCO.2011.35.6287 pubmed: 21990393
Wei W, Wu P, Li L, Zhang ZH. Effectiveness of pegaspargase, gemcitabine, and oxaliplatin (P-GEMOX) chemotherapy combined with radiotherapy in newly diagnosed, stage IE to IIE, nasal-type, extranodal natural killer/T-cell lymphoma. Hematology. 2017;22:320–9.
doi: 10.1080/10245332.2016.1264163 pubmed: 27917702
Li X, Cui Y, Sun Z, Zhang L, Li L, Wang X, et al. DDGP versus SMILE in newly diagnosed advanced natural killer/T-cell lymphoma: a randomized controlled, multicenter, open-label study in China. Clin Cancer Res. 2016;22:5223–8.
doi: 10.1158/1078-0432.CCR-16-0153 pubmed: 27060152
Kwong YL, Kim SJ, Tse E, Oh SY, Kwak JY, Eom HS, et al. Sequential chemotherapy/radiotherapy was comparable with concurrent chemoradiotherapy for stage I/II NK/T-cell lymphoma. Ann Oncol. 2018;29:256–63.
doi: 10.1093/annonc/mdx684 pubmed: 29077846
Kwong YL, Kim WS, Lim ST, Kim SJ, Tang T, Tse E, et al. SMILE for natural killer/T-cell lymphoma: analysis of safety and efficacy from the Asia Lymphoma Study Group. Blood. 2012;120:2973–80.
doi: 10.1182/blood-2012-05-431460 pubmed: 22919026
Lim SH, Hong JY, Lim ST, Hong H, Arnoud J, Zhao W, et al. Beyond first-line non-anthracycline-based chemotherapy for extranodal NK/T-cell lymphoma: clinical outcome and current perspectives on salvage therapy for patients after first relapse and progression of disease. Ann Oncol. 2017;28:2199–205.
doi: 10.1093/annonc/mdx316 pubmed: 28911074
Song GY, Yoon DH, Suh C, Moon JH, Baek DW, Kim JS, et al. Open-label, single arm, multicenter phase II study of VIDL induction chemotherapy followed by upfront autologous stem cell transplantation in patients with advanced stage extranodal NK/T-cell lymphoma. Bone Marrow Transpl. 2021;56:1205–8.
doi: 10.1038/s41409-020-01160-2
Yhim HY, Kim JS, Mun YC, Moon JH, Chae YS, Park Y, et al. Clinical outcomes and prognostic factors of up-front autologous stem cell transplantation in patients with extranodal natural killer/T cell lymphoma. Biol Blood Marrow Transpl. 2015;21:1597–604.
doi: 10.1016/j.bbmt.2015.05.003
Kwong YL, Chan TSY, Tan D, Kim SJ, Poon LM, Mow B, et al. PD1 blockade with pembrolizumab is highly effective in relapsed or refractory NK/T-cell lymphoma failing l-asparaginase. Blood. 2017;129:2437–42.
doi: 10.1182/blood-2016-12-756841 pubmed: 28188133
Li X, Cheng Y, Zhang M, Yan J, Li L, Fu X, et al. Activity of pembrolizumab in relapsed/refractory NK/T-cell lymphoma. J Hematol Oncol. 2018;11:15.
doi: 10.1186/s13045-018-0559-7 pubmed: 29386072 pmcid: 5793390
Murashige N, Kami M, Kishi Y, Kim SW, Takeuchi M, Matsue K, et al. Allogeneic haematopoietic stem cell transplantation as a promising treatment for natural killer-cell neoplasms. Br J Haematol. 2005;130:561–7.
doi: 10.1111/j.1365-2141.2005.05651.x pubmed: 16098071
Ennishi D, Maeda Y, Fujii N, Kondo E, Shinagawa K, Ikeda K, et al. Allogeneic hematopoietic stem cell transplantation for advanced extranodal natural killer/T-cell lymphoma, nasal type. Leuk Lymphoma. 2011;52:1255–61.
doi: 10.3109/10428194.2011.572322 pubmed: 21599584
Kharfan-Dabaja MA, Kumar A, Ayala E, Hamadani M, Reimer P, Gisselbrecht C, et al. Clinical practice recommendations on indication and timing of hematopoietic cell transplantation in mature T Cell and NK/T cell lymphomas: an international collaborative effort on Behalf of the Guidelines Committee of the American Society for Blood and Marrow Transplantation. Biol Blood Marrow Transpl. 2017;23:1826–38.
doi: 10.1016/j.bbmt.2017.07.027
d’Amore F, Gaulard P, Trumper L, Corradini P, Kim WS, Specht L, et al. Peripheral T-cell lymphomas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2015;26:v108–115.
doi: 10.1093/annonc/mdv201 pubmed: 26314772
Tse E, Chan TS, Koh LP, Chng WJ, Kim WS, Tang T, et al. Allogeneic haematopoietic SCT for natural killer/T-cell lymphoma: a multicentre analysis from the Asia Lymphoma Study Group. Bone Marrow Transpl. 2014;49:902–6.
doi: 10.1038/bmt.2014.65
Kanate AS, DiGilio A, Ahn KW, Al Malki M, Jacobsen E, Steinberg A, et al. Allogeneic haematopoietic cell transplantation for extranodal natural killer/T-cell lymphoma, nasal type: a CIBMTR analysis. Br J Haematol. 2018;182:916–20.
doi: 10.1111/bjh.14879 pubmed: 28771676
Cwynarski K, van Biezen A, de Wreede L, Stilgenbauer S, Bunjes D, Metzner B, et al. Autologous and allogeneic stem-cell transplantation for transformed chronic lymphocytic leukemia (Richter’s syndrome): a retrospective analysis from the chronic lymphocytic leukemia subcommittee of the chronic leukemia working party and lymphoma working party of the European Group for Blood and Marrow Transplantation. J Clin Oncol. 2012;30:2211–7.
doi: 10.1200/JCO.2011.37.4108 pubmed: 22547610
Kim SJ, Yoon DH, Jaccard A, Chng WJ, Lim ST, Hong H, et al. A prognostic index for natural killer cell lymphoma after non-anthracycline-based treatment: a multicentre, retrospective analysis. Lancet Oncol. 2016;17:389–400.
doi: 10.1016/S1470-2045(15)00533-1 pubmed: 26873565
Bacigalupo A, Ballen K, Rizzo D, Giralt S, Lazarus H, Ho V, et al. Defining the intensity of conditioning regimens: working definitions. Biol Blood Marrow Transpl. 2009;15:1628–33.
doi: 10.1016/j.bbmt.2009.07.004
Jagasia MH, Greinix HT, Arora M, Williams KM, Wolff D, Cowen EW, et al. National Institutes of Health Consensus Development Project on criteria for clinical trials in chronic graft-versus-host disease: I. The 2014 Diagnosis and Staging Working Group report. Biol Blood Marrow Transpl. 2015;21:389–401.e381.
doi: 10.1016/j.bbmt.2014.12.001
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.
Yamaguchi M, Suzuki R, Oguchi M, Asano N, Amaki J, Akiba T, et al. Treatments and outcomes of patients with extranodal natural killer/t-cell lymphoma diagnosed between 2000 and 2013: a cooperative study in Japan. J Clin Oncol. 2017;35:32–9.
doi: 10.1200/JCO.2016.68.1619 pubmed: 28034070
Kanate AS, Mussetti A, Kharfan-Dabaja MA, Ahn KW, DiGilio A, Beitinjaneh A, et al. Reduced-intensity transplantation for lymphomas using haploidentical related donors vs HLA-matched unrelated donors. Blood. 2016;127:938–47.
doi: 10.1182/blood-2015-09-671834 pubmed: 26670632 pmcid: 4760094
Castagna L, Pagliardini T, Bramanti S, Schiano de Colella JM, Montes de Oca C, Bouabdallah R, et al. Allogeneic stem cell transplantation in poor prognosis peripheral T-cell lymphoma: the impact of different donor type on outcome. Bone Marrow Transpl. 2021;56:883–9.
doi: 10.1038/s41409-020-01133-5
Hamadani M, Ngoya M, Sureda A, Bashir Q, Litovich CA, Finel H, et al. Outcome of allogeneic transplantation for mature T-cell lymphomas: impact of donor source and disease characteristics. Blood Adv. 2022;6:920–30.
doi: 10.1182/bloodadvances.2021005899 pubmed: 34861680 pmcid: 8945300
Suzuki R, Suzumiya J, Nakamura S, Kagami Y, Kameoka JI, Sakai C, et al. Hematopoietic stem cell transplantation for natural killer-cell lineage neoplasms. Bone Marrow Transpl. 2006;37:425–31.
doi: 10.1038/sj.bmt.1705244
Philippe Walter L, Couronne L, Jais JP, Nguyen PD, Blaise D, Pigneux A, et al. Outcome after hematopoietic stem cell transplantation in patients with extranodal natural killer/T-Cell lymphoma, nasal type: A French study from the Societe Francophone de Greffe de Moelle et de Therapie Cellulaire (SFGM-TC). Am J Hematol. 2021;96:834–45.
doi: 10.1002/ajh.26200 pubmed: 33864708
Hwang WY, Koh LP, Lim ST, Linn YC, Loh YS, Koh MB, et al. Multicenter study of comparative outcomes of hematopoietic stem cell transplant for peripheral T cell lymphoma and natural killer/T-cell lymphoma. Leuk Lymphoma. 2011;52:1382–6.
doi: 10.3109/10428194.2011.569038 pubmed: 21599577
Luznik L, Jalla S, Engstrom LW, Iannone R, Fuchs EJ. Durable engraftment of major histocompatibility complex-incompatible cells after nonmyeloablative conditioning with fludarabine, low-dose total body irradiation, and posttransplantation cyclophosphamide. Blood. 2001;98:3456–64.
doi: 10.1182/blood.V98.12.3456 pubmed: 11719388
Haverkos BM, Abbott D, Hamadani M, Armand P, Flowers ME, Merryman R, et al. PD-1 blockade for relapsed lymphoma post-allogeneic hematopoietic cell transplant: high response rate but frequent GVHD. Blood. 2017;130:221–8.
doi: 10.1182/blood-2017-01-761346 pubmed: 28468799 pmcid: 5510790
Schoch LK, Cooke KR, Wagner-Johnston ND, Gojo I, Swinnen LJ, Imus P, et al. Immune checkpoint inhibitors as a bridge to allogeneic transplantation with posttransplant cyclophosphamide. Blood Adv. 2018;2:2226–9.
doi: 10.1182/bloodadvances.2018019208 pubmed: 30190282 pmcid: 6134225
Bobillo S, Nieto JC, Barba P. Use of checkpoint inhibitors in patients with lymphoid malignancies receiving allogeneic cell transplantation: a review. Bone Marrow Transpl. 2021;56:1784–93.
doi: 10.1038/s41409-021-01268-z
Merryman RW, Castagna L, Giordano L, Ho VT, Corradini P, Guidetti A, et al. Allogeneic transplantation after PD-1 blockade for classic Hodgkin lymphoma. Leukemia. 2021;35:2672–83.
doi: 10.1038/s41375-021-01193-6 pubmed: 33658659
Herbaux C, Gauthier J, Brice P, Drumez E, Ysebaert L, Doyen H, et al. Efficacy and tolerability of nivolumab after allogeneic transplantation for relapsed Hodgkin lymphoma. Blood. 2017;129:2471–8.
doi: 10.1182/blood-2016-11-749556 pubmed: 28270452

Auteurs

Philipp Berning (P)

Department of Hematology and Oncology, University Hospital Muenster, Muenster, Germany. philipp.berning@ukmuenster.de.

Norbert Schmitz (N)

Department of Hematology and Oncology, University Hospital Muenster, Muenster, Germany.

Maud Ngoya (M)

European Society for Blood and Marrow Transplantation, Hôpital St. Antoine, Paris, France.

Hervé Finel (H)

European Society for Blood and Marrow Transplantation, Hôpital St. Antoine, Paris, France.

Ariane Boumendil (A)

European Society for Blood and Marrow Transplantation, Hôpital St. Antoine, Paris, France.

Fengrong Wang (F)

Beijing University, Institute of Hematology, National Clinical Research Center for Hematologic Disease, Beijing, China.

Xiao-Jun Huang (XJ)

Beijing University, Institute of Hematology, National Clinical Research Center for Hematologic Disease, Beijing, China.

Olivier Hermine (O)

Department of Hematology, Hôpital Necker, Assistance Publique Hôpitaux de Paris, University Paris Descartes, Paris, France.

Laure Philippe (L)

Department of Hematology, Hôpital Necker, Assistance Publique Hôpitaux de Paris, University Paris Descartes, Paris, France.

Lucile Couronné (L)

Laboratory of Onco-Hematology, Necker Children's Hospital, Assistance Publique-Hôpitaux de Paris (APHP), Université Paris Cité, Paris, France.

Arnaud Jaccard (A)

Department of Hematology, CHU Dupuytren, Limoges, France.

Daihong Liu (D)

General Hospital of People's Liberation Army of China, Beijing, China.

Depei Wu (D)

National Clinical Research Center for Hematologic Diseases, Jiangsu Institute of Hematology, The First Affiliated Hospital of Soochow University, Soochow, China.

Hans Christian Reinhardt (HC)

Department of Hematology and Stem Cell Transplantation, University Hospital Essen, University Duisburg-Essen, Essen, Germany.

Yves Chalandon (Y)

Division of Hematology, Hôpitaux Universitaires de Genève and Faculty of Medicine, University of Geneva, Geneva, Switzerland.

Eva Wagner-Drouet (E)

Department of Medicine III, Johannes Gutenberg-University Mainz, Mainz, Germany.

Mi Kwon (M)

Department of Hematology, Gregorio Marañón General University Hospital, Institute of Health Research Gregorio Marañón, Madrid, Spain.

Xi Zhang (X)

Medical Center of Hematology, Xinqiao Hospital, Army Medical University, Chongqing, China.

Ben Carpenter (B)

Department of Haematology, University College London Hospitals, London, UK.

Ibrahim Yakoub-Agha (I)

CHU de Lille, INSERM U1286, Infinite, Université de Lille, Lille, France.

Gerald Wulf (G)

Department of Hematology/Oncology, Georg-August-University Göttingen, Göttingen, Germany.

Javier López-Jiménez (J)

Hematology Department, Hospital Universitario Ramón y Cajal, Madrid, Spain.

Jaime Sanz (J)

Department of Hematology, Hospital Universitario y Politécnico La Fe, Valencia, Spain.

Hélène Labussière-Wallet (H)

Centre Hospitalier Lyon Sud, Pavillon Marcel Bérard, Service Hematologie, Lyon, France.

Avichai Shimoni (A)

Division of Hematology and Bone Marrow Transplantation, Chaim Sheba Medical Center, Tel-Hashomer, Israel.

Peter Dreger (P)

Department of Medicine V, University of Heidelberg, Heidelberg, Germany.

Anna Sureda (A)

Hematology Department, Institut Català d'Oncologia Hospitalet, IDIBELL, Universitat de Barcelona, Barcelona, Spain.

Won Seog Kim (WS)

Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.

Bertram Glass (B)

Department of Hematology and Stem Cell Transplantation, Helios Clinic, Berlin-Buch, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH