Allogeneic hematopoietic cell transplantation in patients with myeloid/lymphoid neoplasm with FGFR1-rearrangement: a study of the Chronic Malignancies Working Party of EBMT.

Graft vs Host Disease / etiology Hematopoietic Stem Cell Transplantation / methods Humans Leukemia, Myeloid, Acute / therapy Lymphoma / complications Receptor, Fibroblast Growth Factor, Type 1 / genetics Retrospective Studies Transplantation Conditioning / adverse effects Transplantation, Homologous / adverse effects

Journal

Bone marrow transplantation

ISSN: 1476-5365

Titre abrégé: Bone Marrow Transplant

Pays: England

ID NLM: 8702459

Informations de publication

Date de publication:
03 2022

Historique:

received: 08 08 2021

accepted: 09 12 2021

revised: 26 11 2021

pubmed: 24 1 2022

medline: 5 4 2022

entrez: 23 1 2022

Statut: ppublish

Résumé

Allogeneic hematopoietic cell transplantation (allo-HCT) is the only curative treatment for patients with myeloid/lymphoid neoplasm (MLN) with FGFR1 rearrangement, but data on overall results are limited. We report on the largest series of patients (n = 22) with FGFR1-rearranged MLN undergoing allo-HCT. Distribution according to cytogenetic subtype was: t(8;13) in 11 cases, t(8;22) in 7 cases, t(6;8) in 2 cases, and other (n = 2). Over a third of patients displayed a chronic myeloproliferative (MPN) phenotype, another third showed MPN features with concomitant lymphoma or acute leukemia, and the remaining ones presented as acute leukemia. After a median follow-up of 4.1 years from transplant, the estimated 5-year survival rate, progression-free survival, non-relapse mortality and relapse incidence was 74%, 63%, 14% and 23%, respectively. Causes of death were relapse/progression (n = 4), graft-versus-host disease (n = 2) and organ toxicity (n = 1). Six patients experienced disease relapse at a median of 6.1 months (range: 2.3-119.6). Two of them achieved complete remission with ponatinib or pemigatinib and were alive at 34.5 and 37 months from relapse, respectively. These data highlight the significant curative potential of allo-HCT in this aggressive disease. Maintenance with tyrosine kinase inhibitors may be a promising approach, at least in cases with detectable residual disease after transplant.

Identifiants

DOI: 10.1038/s41409-021-01553-x PMID: 35066569

pubmed: 35066569

doi: 10.1038/s41409-021-01553-x

pii: 10.1038/s41409-021-01553-x

doi:

Substances chimiques

FGFR1 protein, human EC 2.7.10.1

Receptor, Fibroblast Growth Factor, Type 1 EC 2.7.10.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

Pagination

416-422

Commentaires et corrections

Type : ErratumIn

Informations de copyright

Références

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.

doi: 10.1182/blood-2016-03-643544 pubmed: 27069254

Patnaik MM, Gangat N, Knudson RA, Keefe JG, Hanson CA, Pardanani A, et al. Chromosome 8p11.2 translocations: prevalence, FISH analysis for FGFR1 and MYST3, and clinicopathologic correlates in a consecutive cohort of 13 cases from a single institution. Am J Hematol. 2010;85:238–42.

doi: 10.1002/ajh.21631 pubmed: 20143402

Strati P, Tang G, Duose DY, Mallampati S, Luthra R, Patel KP, et al. Myeloid/lymphoid neoplasms with FGFR1 rearrangement. Leuk Lymphoma. 2018;59:1672–6.

doi: 10.1080/10428194.2017.1397663 pubmed: 29119847

Roumiantsev S, Krause DS, Neumann CA, Dimitri CA, Asiedu F, Cross NC, et al. Distinct stem cell myeloproliferative/T lymphoma syndromes induced by ZNF198-FGFR1 and BCR-FGFR1 fusion genes from 8p11 translocations. Cancer Cell. 2004;5:287–98.

doi: 10.1016/S1535-6108(04)00053-4 pubmed: 15050920

Inhorn RC, Aster JC, Roach SA, Slapak CA, Soiffer R, Tantravahi R, et al. A syndrome of lymphoblastic lymphoma, eosinophilia, and myeloid hyperplasia/malignancy associated with t(8;13)(p11;q11): description of a distinctive clinicopathologic entity. Blood. 1995;85:1881–7.

doi: 10.1182/blood.V85.7.1881.bloodjournal8571881 pubmed: 7661940

Reiter A, Sohal J, Kulkarni S, Chase A, Macdonald DH, Aguiar RC, et al. Consistent fusion of ZNF198 to the fibroblast growth factor receptor-1 in the t(8;13)(p11;q12) myeloproliferative syndrome. Blood. 1998;92:1735–42.

doi: 10.1182/blood.V92.5.1735 pubmed: 9716603

Jackson CC, Medeiros LJ, Miranda RN. 8p11 myeloproliferative syndrome: a review. Hum Pathol. 2010;41:461–76.

doi: 10.1016/j.humpath.2009.11.003 pubmed: 20226962

Macdonald D, Aguiar RC, Mason PJ, Goldman JM, Cross NC. A new myeloproliferative disorder associated with chromosomal translocations involving 8p11: a review. Leukemia 1995;9:1628–30.

pubmed: 7564500

Baer C, Muehlbacher V, Kern W, Haferlach C, Haferlach T. Molecular genetic characterization of myeloid/lymphoid neoplasms associated with eosinophilia and rearrangement of PDGFRA, PDGFRB, FGFR1 or PCM1-JAK2. Haematologica. 2018;103:e348–e50.

doi: 10.3324/haematol.2017.187302 pubmed: 29567772 pmcid: 6068021

Khodadoust MS, Luo B, Medeiros BC, Johnson RC, Ewalt MD, Schalkwyk AS, et al. Clinical activity of ponatinib in a patient with FGFR1-rearranged mixed-phenotype acute leukemia. Leukemia. 2016;30:947–50.

doi: 10.1038/leu.2015.136 pubmed: 26055304

Kasbekar M, Nardi V, Dal Cin P, Brunner AM, Burke M, Chen YB, et al. Targeted FGFR inhibition results in a durable remission in an FGFR1-driven myeloid neoplasm with eosinophilia. Blood Adv. 2020;4:3136–40.

doi: 10.1182/bloodadvances.2020002308 pubmed: 32649766 pmcid: 7362377

Verstovsek S, Subbiah V, Masarova L, Yin CC, Tang G, Manshouri T, et al. Treatment of the myeloid/lymphoid neoplasm with FGFR1 rearrangement with FGFR1 inhibitor. Ann Oncol. 2018;29:1880–2.

doi: 10.1093/annonc/mdy173 pubmed: 29767670 pmcid: 6887683

Verstovsek S, Vannucchi A, Rambaldi A, Gotlib J, Mead A, Hochhaus A, et al. Interim results from fight-203, a phase 2, open-label, multicenter study evaluating the efficacy and safety of pemigatinib (INCB054828) in patients with myeloid/lymphoid neoplasms with rearrangement of fibroblast growth factor receptor 1 (FGFR1). Blood. 2018;132 :(abstract 690).

Dolan M, Cioc A, Cross NC, Neglia JP, Tolar J. Favorable outcome of allogeneic hematopoietic cell transplantation for 8p11 myeloproliferative syndrome associated with BCR-FGFR1 gene fusion. Pediatr Blood Cancer. 2012;59:194–6.

doi: 10.1002/pbc.23404 pubmed: 22106025

Konishi Y, Kondo T, Nakao K, Asagoe K, Otsuka Y, Nishikori M, et al. Allogeneic hematopoietic stem cell transplantation for 8p11 myeloproliferative syndrome with BCR-FGFR1 gene rearrangement: a case report and literature review. Bone Marrow Transpl. 2019;54:326–9.

doi: 10.1038/s41409-018-0287-1

Katagiri S, Umezu T, Azuma K, Kobayashi C, Akahane D, Suguro T, et al. Maintenance 5-azacytidine therapy by MRD monitoring after allogeneic HSCT in myeloid/lymphoid neoplasms with FGFR1 rearrangement. Bone Marrow Transpl. 2019;54:1148–50.

doi: 10.1038/s41409-019-0436-1

Townsend W, Cross NC, Waghorn K, Somana K, Ramsay A, Thomson K, et al. Clinical evidence for a graft-versus-tumour effect following allogeneic HSCT for t(8;13) atypical myeloproliferative disorder. Bone Marrow Transpl. 2009;44:197–9.

doi: 10.1038/bmt.2008.448

Suzan F, Guasch G, Terre C, Garcia I, Bastie JN, Maarek O, et al. Long-term complete haematological and molecular remission after allogeneic bone marrow transplantation in a patient with a stem cell myeloproliferative disorder associated with t(8;13)(p12;q12). Br J Haematol. 2003;121:312–4.

doi: 10.1046/j.1365-2141.2003.04269.x pubmed: 12694254

Holtan SG, DeFor TE, Lazaryan A, Bejanyan N, Arora M, Brunstein CG, et al. Composite end point of graft-versus-host disease-free, relapse-free survival after allogeneic hematopoietic cell transplantation. Blood. 2015;125:1333–8.

doi: 10.1182/blood-2014-10-609032 pubmed: 25593335 pmcid: 4335084

Demiroglu A, Steer EJ, Heath C, Taylor K, Bentley M, Allen SL, et al. The t(8;22) in chronic myeloid leukemia fuses BCR to FGFR1: transforming activity and specific inhibition of FGFR1 fusion proteins. Blood. 2001;98:3778–83.

doi: 10.1182/blood.V98.13.3778 pubmed: 11739186

Montenegro-Garreaud X, Miranda RN, Reynolds A, Tang G, Wang SA, Yabe M, et al. Myeloproliferative neoplasms with t(8;22)(p11.2;q11.2)/BCR-FGFR1: a meta-analysis of 20 cases shows cytogenetic progression with B-lymphoid blast phase. Hum Pathol. 2017;65:147–56.

Gupta V, Kennedy JA, Capo-Chichi JM, Kim S, Hu ZH, Alyea EP, et al. Genetic factors rather than blast reduction determine outcomes of allogeneic HCT in BCR-ABL-negative MPN in blast phase. Blood Adv. 2020;4:5562–73.

doi: 10.1182/bloodadvances.2020002727 pubmed: 33170935 pmcid: 7656913