Long-term survival of 1338 MM patients treated with tandem autologous vs. autologous-allogeneic transplantation.
Journal
Bone marrow transplantation
ISSN: 1476-5365
Titre abrégé: Bone Marrow Transplant
Pays: England
ID NLM: 8702459
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
02
02
2020
accepted:
25
03
2020
revised:
19
03
2020
pubmed:
15
4
2020
medline:
22
6
2021
entrez:
15
4
2020
Statut:
ppublish
Résumé
Contrary to tandem autologous transplant (auto-auto), autologous followed by reduced intensity conditioning allogenic transplantation (auto-allo) offers graft-versus-myeloma (GVM) effect but with higher toxicity. Trials comparing these two strategies relied on availability of HLA-matched sibling donors for arm allocation (biological randomization) and yielded conflicting results. A pooled analysis of multiple trials with extended follow up provides an opportunity to compare these strategies. We obtained individual patient data from participants of four trials comparing auto-auto vs. auto-allo after induction therapy. There were 899 patients in auto-auto and 439 in auto-allo. Median follow up of survivors was 118.5 months. Median overall survival (OS) was 78.0 months in auto-auto and 98.3 months in auto-allo (HR = 0.84, P = 0.02). OS was 36.4% vs. 44.1% at 10 years (P = 0.01) for auto-auto and auto-allo, respectively. Progression-free survival was also improved in auto-allo (HR = 0.84, P = 0.004). Risk of non-relapse mortality was higher in auto-allo (10 year 8.3% vs. 19.7%, P < 0.001), while risk of disease progression was higher in auto-auto (10 year 77.2% vs. 61.6%, P < 0.001). Median post relapse survival was 41.5 months in auto-auto and 62.3 months in auto-allo (HR = 0.71, P < 0.001). This supports the existence of durable GVM effect enhancing myeloma control with subsequent therapies.
Identifiants
pubmed: 32286506
doi: 10.1038/s41409-020-0887-4
pii: 10.1038/s41409-020-0887-4
pmc: PMC7483973
mid: NIHMS1589581
doi:
Types de publication
Journal Article
Meta-Analysis
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
1810-1816Subventions
Organisme : NHLBI NIH HHS
ID : UG1 HL069286
Pays : United States
Organisme : NHLBI NIH HHS
ID : UG1 HL069278
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NHLBI NIH HHS
ID : U01 HL069294
Pays : United States
Organisme : NCI NIH HHS
ID : U10 CA180888
Pays : United States
Organisme : NCI NIH HHS
ID : U24 CA076518
Pays : United States
Organisme : NHLBI NIH HHS
ID : U24 HL138660
Pays : United States
Références
Tricot G, Vesole DH, Jagannath S, Hilton J, Munshi N, Barlogie B. Graft-versus-myeloma effect: proof of principle. Blood. 1996;87:1196–8.
doi: 10.1182/blood.V87.3.1196.bloodjournal8731196
Lokhorst HM, Schattenberg A, Cornelissen JJ, van Oers MH, Fibbe W, Russell I, et al. Donor lymphocyte infusions for relapsed multiple myeloma after allogeneic stem-cell transplantation: predictive factors for response and long-term outcome. J Clin Oncol. 2000;18:3031–7.
doi: 10.1200/JCO.2000.18.16.3031
Lokhorst HM, Wu K, Verdonck LF, Laterveer LL, van de Donk NW, van Oers MH, et al. The occurrence of graft-versus-host disease is the major predictive factor for response to donor lymphocyte infusions in multiple myeloma. Blood. 2004;103:4362–4.
doi: 10.1182/blood-2003-11-3862
Aschan J, Lonnqvist B, Ringden O, Kumlien G, Gahrton G. Graft-versus-myeloma effect. Lancet. 1996;348:346.
doi: 10.1016/S0140-6736(05)64525-4
Barlogie B, Kyle RA, Anderson KC, Greipp PR, Lazarus HM, Hurd DD, et al. Standard chemotherapy compared with high-dose chemoradiotherapy for multiple myeloma: final results of phase III US Intergroup Trial S9321. J Clin Oncol. 2006;24:929–36.
doi: 10.1200/JCO.2005.04.5807
Gahrton G, Tura S, Ljungman P, Belanger C, Brandt L, Cavo M, et al. Allogeneic bone marrow transplantation in multiple myeloma. European Group for Bone Marrow Transplantation. N Engl J Med. 1991;325:1267–73.
doi: 10.1056/NEJM199110313251802
Gahrton G, Svensson H, Cavo M, Apperly J, Bacigalupo A, Bjorkstrand B, et al. Progress in allogenic bone marrow and peripheral blood stem cell transplantation for multiple myeloma: a comparison between transplants performed 1983-93 and 1994-8 at European Group for Blood and Marrow Transplantation centres. Br J Haematol. 2001;113:209–16.
doi: 10.1046/j.1365-2141.2001.02726.x
Armeson KE, Hill EG, Costa LJ. Tandem autologous vs autologous plus reduced intensity allogeneic transplantation in the upfront management of multiple myeloma: meta-analysis of trials with biological assignment. Bone Marrow Transplant. 2013;48:562–7.
doi: 10.1038/bmt.2012.173
Giralt S, Ballen K, Rizzo D, Bacigalupo A, Horowitz M, Pasquini M, et al. Reduced-intensity conditioning regimen workshop: defining the dose spectrum. Report of a workshop convened by the center for international blood and marrow transplant research. Biol Blood Marrow Transplant. 2009;15:367–9.
doi: 10.1016/j.bbmt.2008.12.497
Krishnan A, Pasquini MC, Logan B, Stadtmauer EA, Vesole DH, Alyea E 3rd, et al. Autologous haemopoietic stem-cell transplantation followed by allogeneic or autologous haemopoietic stem-cell transplantation in patients with multiple myeloma (BMT CTN 0102): a phase 3 biological assignment trial. Lancet Oncol. 2011;12:1195–203.
doi: 10.1016/S1470-2045(11)70243-1
Gahrton G, Iacobelli S, Bjorkstrand B, Hegenbart U, Gruber A, Greinix H, et al. Autologous/reduced-intensity allogeneic stem cell transplantation vs autologous transplantation in multiple myeloma: long-term results of the EBMT-NMAM2000 study. Blood. 2013;121:5055–63.
doi: 10.1182/blood-2012-11-469452
Giaccone L, Storer B, Patriarca F, Rotta M, Sorasio R, Allione B, et al. Long-term follow-up of a comparison of nonmyeloablative allografting with autografting for newly diagnosed myeloma. Blood. 2011;117:6721–7.
doi: 10.1182/blood-2011-03-339945
Bjorkstrand B, Iacobelli S, Hegenbart U, Gruber A, Greinix H, Volin L, et al. Tandem autologous/reduced-intensity conditioning allogeneic stem-cell transplantation versus autologous transplantation in myeloma: long-term follow-up. J Clin Oncol. 2011;29:3016–22.
doi: 10.1200/JCO.2010.32.7312
Rosinol L, Perez-Simon JA, Sureda A, de la Rubia J, de Arriba F, Lahuerta JJ, et al. A prospective PETHEMA study of tandem autologous transplantation versus autograft followed by reduced-intensity conditioning allogeneic transplantation in newly diagnosed multiple myeloma. Blood. 2008;112:3591–3.
doi: 10.1182/blood-2008-02-141598
Moreau P, Garban F, Attal M, Michallet M, Marit G, Hulin C, et al. Long-term follow-up results of IFM99-03 and IFM99-04 trials comparing nonmyeloablative allotransplantation with autologous transplantation in high-risk de novo multiple myeloma. Blood. 2008;112:3914–5.
doi: 10.1182/blood-2008-07-168823
Garban F, Attal M, Michallet M, Hulin C, Bourhis JH, Yakoub-Agha I, et al. Prospective comparison of autologous stem cell transplantation followed by dose-reduced allograft (IFM99-03 trial) with tandem autologous stem cell transplantation (IFM99-04 trial) in high-risk de novo multiple myeloma. Blood. 2006;107:3474–80.
doi: 10.1182/blood-2005-09-3869
Bruno B, Rotta M, Patriarca F, Mordini N, Allione B, Carnevale-Schianca F, et al. A comparison of allografting with autografting for newly diagnosed myeloma. N. Engl J Med. 2007;356:1110–20.
doi: 10.1056/NEJMoa065464
Giralt S, Costa LJ, Maloney D, Krishnan A, Fei M, Antin JH, et al. Tandem autologous-autologous versus autologous-allogeneic hematopoietic stem cell transplant for patients with multiple myeloma: long-term follow-up results from the blood and marrow transplant clinical trials network 0102 trial. Biol Blood Marrow Transplant. 2019; pii: S1083-8791(19)30785-2. https://doi.org/10.1016/j.bbmt.2019.11.018 . [Epub ahead of print].
Htut M, D’Souza A, Krishnan A, Bruno B, Zhang MJ, Fei M, et al. Autologous/allogeneic hematopoietic cell transplantation versus tandem autologous transplantation for multiple myeloma: comparison of long-term postrelapse survival. Biol Blood Marrow Transplant. 2018;24:478–85.
doi: 10.1016/j.bbmt.2017.10.024
Maffini E, Storer BE, Sandmaier BM, Bruno B, Sahebi F, Shizuru JA, et al. Long-term follow up of tandem autologous-allogeneic hematopoietic cell transplantation for multiple myeloma. Haematologica. 2019;104:380–91.
doi: 10.3324/haematol.2018.200253
Giaccone L, Evangelista A, Patriarca F, Sorasio R, Pini M, Carnevale-Schianca F, et al. Impact of new drugs on the long-term follow-up of upfront tandem autograft-allograft in multiple myeloma. Biol Blood Marrow Transplant. 2018;24:189–93.
doi: 10.1016/j.bbmt.2017.09.017
Kneppers E, van der Holt B, Kersten MJ, Zweegman S, Meijer E, Huls G, et al. Lenalidomide maintenance after nonmyeloablative allogeneic stem cell transplantation in multiple myeloma is not feasible: results of the HOVON 76 Trial. Blood. 2011;118:2413–9.
doi: 10.1182/blood-2011-04-348292
Kroger N, Zabelina T, Klyuchnikov E, Kropff M, Pfluger KH, Burchert A, et al. Toxicity-reduced, myeloablative allograft followed by lenalidomide maintenance as salvage therapy for refractory/relapsed myeloma patients. Bone Marrow Transplant. 2013;48:403–7.
doi: 10.1038/bmt.2012.142
Wolschke C, Stubig T, Hegenbart U, Schonland S, Heinzelmann M, Hildebrandt Y, et al. Postallograft lenalidomide induces strong NK cell-mediated antimyeloma activity and risk for T cell-mediated GvHD: results from a phase I/II dose-finding study. Exp Hematol. 2013;41:134–42. e133.
doi: 10.1016/j.exphem.2012.10.004
Alsina M, Becker PS, Zhong X, Adams A, Hari P, Rowley S, et al. Lenalidomide maintenance for high-risk multiple myeloma after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2014;20:1183–9.
doi: 10.1016/j.bbmt.2014.04.014
Greipp PR, San Miguel J, Durie BG, Crowley JJ, Barlogie B, Blade J, et al. International staging system for multiple myeloma. J Clin Oncol. 2005;23:3412–20.
doi: 10.1200/JCO.2005.04.242
Palumbo A, Avet-Loiseau H, Oliva S, Lokhorst HM, Goldschmidt H, Rosinol L, et al. Revised international staging system for multiple myeloma: a report from International Myeloma Working Group. J Clin Oncol. 2015;33:2863–9.
doi: 10.1200/JCO.2015.61.2267
Fonseca R, Bergsagel PL, Drach J, Shaughnessy J, Gutierrez N, Stewart AK, et al. International Myeloma Working Group molecular classification of multiple myeloma: spotlight review. Leukemia. 2009;23:2210–21.
doi: 10.1038/leu.2009.174
Ladetto M, Ferrero S, Drandi D, Festuccia M, Patriarca F, Mordini N, et al. Prospective molecular monitoring of minimal residual disease after non-myeloablative allografting in newly diagnosed multiple myeloma. Leukemia. 2016;30:1211–4.
doi: 10.1038/leu.2015.269
Moreau P, Hullin C, Garban F, Yakoub-Agha I, Benboubker L, Attal M, et al. Tandem autologous stem cell transplantation in high-risk de novo multiple myeloma: final results of the prospective and randomized IFM 99-04 protocol. Blood. 2006;107:397–403.
doi: 10.1182/blood-2005-06-2573
Lokhorst HM, van der Holt B, Cornelissen JJ, Kersten MJ, van Oers M, Raymakers R, et al. Donor versus no-donor comparison of newly diagnosed myeloma patients included in the HOVON-50 multiple myeloma study. Blood. 2012;119:6219–25. quiz 6399
doi: 10.1182/blood-2011-11-393801
Ghosh N, Ye X, Tsai HL, Bolanos-Meade J, Fuchs EJ, Luznik L, et al. Allogeneic blood or marrow transplantation with post-transplantation cyclophosphamide as graft-versus-host disease prophylaxis in multiple myeloma. Biol Blood Marrow Transplant. 2017;23:1903–9.
doi: 10.1016/j.bbmt.2017.07.003