Long-term outcome of imatinib 400 mg compared to imatinib 600 mg or imatinib 400 mg daily in combination with cytarabine or pegylated interferon alpha 2a for chronic myeloid leukaemia: results from the French SPIRIT phase III randomised trial.


Journal

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

Informations de publication

Date de publication:
08 2021
Historique:
received: 24 01 2020
accepted: 15 12 2020
revised: 20 11 2020
pubmed: 24 1 2021
medline: 1 9 2021
entrez: 23 1 2021
Statut: ppublish

Résumé

The STI571 prospective randomised trial (SPIRIT) French trial is a four-arm study comparing imatinib (IM) 400 mg versus IM 600 mg, IM 400 mg + cytarabine (AraC), and IM 400 mg + pegylated interferon alpha2a (PegIFN-α2a) for the front-line treatment of chronic-phase chronic myeloid leukaemia (CML). Long-term analyses included overall and progression-free survival, molecular responses to treatment, and severe adverse events. Starting in 2003, the trial included 787 evaluable patients. The median overall follow-up of the patients was 13.5 years (range 3 months to 16.7 years). Based on intention-to-treat analyses, at 15 years, overall and progression-free survival were similar across arms: 85%, 83%, 80%, and 82% and 84%, 87%, 79%, and 79% for the IM 400 mg (N = 223), IM 600 mg (N = 171), IM 400 mg + AraC (N = 172), and IM 400 mg + PegIFN-α2a (N = 221) arms, respectively. The rate of major molecular response at 12 months and deep molecular response (MR4) over time were significantly higher with the combination IM 400 mg + PegIFN-α2a than with IM 400 mg: p = 0.0001 and p = 0.0035, respectively. Progression to advanced phases and secondary malignancies were the most frequent causes of death. Toxicity was the main reason for stopping AraC or PegIFN-α2a treatment.

Identifiants

pubmed: 33483613
doi: 10.1038/s41375-020-01117-w
pii: 10.1038/s41375-020-01117-w
doi:

Substances chimiques

Interferon-alpha 0
Recombinant Proteins 0
Cytarabine 04079A1RDZ
Polyethylene Glycols 3WJQ0SDW1A
Imatinib Mesylate 8A1O1M485B
peginterferon alfa-2a Q46947FE7K

Types de publication

Clinical Trial, Phase III Comparative Study Journal Article Multicenter Study Randomized Controlled Trial Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2332-2345

Investigateurs

Francois Guilhot (F)
Francoise Rigal-Huguet (F)
Joëlle Guilhot (J)
Agnès-Paule Guerci-Bresler (AP)
Delphine Rea (D)
Valérie Coiteux (V)
Martine Gardembas (M)
Anne Vekhoff (A)
Marc Berger (M)
Laurence Legros (L)
Philippe Rousselot (P)
Pascal Lenain (P)
Martine Escoffre Barbe (M)
Viviane Dubruille (V)
Pascale Cony-Makhoul (P)
Hyacinthe Johnson-Ansah (H)
Melanie Mercier (M)
Charbonnier Aude (C)
Lydia Roy (L)
Nathalie Cambier (N)
Jean-Michel Cayuela (JM)
Jean-Claude Chomel (JC)
Marc Delord (M)
Claude Preudhomme (C)
Gabriel Etienne (G)
François-Xavier Mahon (FX)
Franck-Emmanuel Nicolini (FE)

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer Nature Limited part of Springer Nature.

Références

O’Brien S, Guilhot F, Larson RA, Gathmann I, Baccarani M, Cervantes F, et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2003;348:994–1004.
doi: 10.1056/NEJMoa022457
Druker BJ, Guilhot F, O’Brien SG, Gathmann I, Kantarjian H, Gattermann N, et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med. 2006;355:2408–17.
doi: 10.1056/NEJMoa062867
Guilhot F, Druker B, Larson RA, Gathmann I, So C, Waltzman R, O’brien SG. High rates of durable response are achieved with Imatinib after treatment with interferon alpha plus cytarabine: results from the international randomized study of interferon and STI571 (IRIS) trial. Haematologica. 2009;94:1669–75.
doi: 10.3324/haematol.2009.010629
Hochhaus A, Larson RA, Guilhot F, Radich JP, Branford S, Hughes TP, et al. Long-term outcomes of imatinib treatment for chronic myeloid leukemia. N Engl J Med. 2017;376:917–27.
doi: 10.1056/NEJMoa1609324
Graham SM, Jørgensen HG, Allan E, Pearson C, Alcorn MJ, Richmond L, et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood. 2002;99:319–25.
doi: 10.1182/blood.V99.1.319
Cortes J, Giles F, O’Brien S, Thomas D, Garcia-Manero G, Rios MB, et al. Result of high-dose imatinib mesylate in patients with Philadelphia chromosome—positive chronic myeloid leukemia after failure of interferon-α. Blood. 2003;102:83–6.
doi: 10.1182/blood-2003-01-0025
Kantarjian H, Talpaz M, O’Brien S, Garcia-Manero G. High-dose imatinib mesylate therapy in newly diagnosed Philadelphia chromosome–positive chronic phase chronic myeloid leukemia. Blood. 2004;103:2872–8.
doi: 10.1182/blood-2003-11-3800
Guilhot F, Chastang C, Michallet M, Guerci A, Harousseau JL, Maloisel F, et al. Interferon alpha-2b combined with Cytarabine versus Interferon alone in chronic myelogenous leukemia. N Engl J Med 1997;337:223–9.
doi: 10.1056/NEJM199707243370402
Guilhot F, Roy L, Guilhot J, Millot F. Interferon therapy in chronic myelogenous leukemia. Hematol Oncol Clin North Am. 2004;18:585–603.
doi: 10.1016/j.hoc.2004.03.002
Gardembas M, Rousselot P, Tulliez M, Vigier M, Buzyn A, Rigal-Huguet F, et al. Results of a prospective phase 2 study combining imatinib mesylate and cytarabine for the treatment of Philadelphia-positive patients with chronic myelogenous leukemia in chronic phase. Blood. 2003;102:4298–305.
doi: 10.1182/blood-2003-04-1010
Baccarani M, Martinelli G, Rosti G, Trabacchi E, Testoni N, Bassi S, et al. Imatinib an pegylated human recombinant interferon-a2b in early chronic-phase chronic myeloid leukemia. Blood. 2004;104:4245–51.
doi: 10.1182/blood-2004-03-0826
Preudhomme C, Guilhot J, Nicolini F, Guerci-Bresler A, Huguet F, Maloisel F, et al. Imatinib plus pegylated interferon-alpha2a in chronic myeloid leukemia. N Engl J Med. 2010;363:2511–21.
doi: 10.1056/NEJMoa1004095
Sokal JE, Cox EB, Baccarani M, Tura S, Gomez GA, Robertson JE, et al. Prognostic discrimination in “good-risk” chronic granulocytic leukemia. Blood 1984;63:789–99.
doi: 10.1182/blood.V63.4.789.789
Johnson-Ansah H, Guilhot J, Rousselot P, Rea D, Legros L, Rigal-Huguet F, et al. Tolerability and efficacy of pegylated interferon-α-2a in combination with imatinib for patients with chronic-phase chronic myeloid leukemia. Cancer. 2013;119:4284–9.
doi: 10.1002/cncr.28328
Guilhot J, Baccarani M, Clark RE, Cervantes F, Guilhot F, Hochhaus A, et al. Definitions, methodological and statistical issues for phase 3 clinical trials in chronic myeloid leukemia: a proposal by the European LeukemiaNet. Blood. 2012;119:5963–71.
doi: 10.1182/blood-2011-10-383711
Ederer F, Heise H. Instructions to Ibm 650 programmers in processing survival computations, Technical, End Results Evaluation Section, National Cancer Institute. 1959.
Gray RJ. A class of k-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat. 1988;16:1141–54.
doi: 10.1214/aos/1176350951
Marin D, Ibrahim AR, Lucas C, Gerrard G, Wang L, Szydlo RM, et al. Assessment of BCR-ABL1 transcript levels at 3 months is the only requirement for predicting outcome for patients with chronic myeloid leukemia treated with tyrosine kinase inhibitors. J Clin Oncol. 2012;30:232–8.
doi: 10.1200/JCO.2011.38.6565
Hanfstein B, Müller MC, Hehlmann R, Erben P, Lauseker M, Fabarius A, et al. Early molecular and cytogenetic response is predictive for long-term progression-free and overall survival in chronic myeloid leukemia (CML). Leukemia. 2012;26:2096–102.
doi: 10.1038/leu.2012.85
Hughes TP, Saglio G, Kantarjian HM, Guilhot F, Niederwieser D, Rosti G, et al. Early molecular response predicts outcomes in patients with chronic myeloid leukemia in chronic phase treated with frontline nilotinib or imatinib. Blood. 2014;123:1353–60.
doi: 10.1182/blood-2013-06-510396
Branford S, Yeung DT, Parker WT, Roberts ND, Purins L, Braley JA, et al. Prognosis for patients with CML and >10% BCR-ABL1 after 3 months of imatinib depends on the rate of BCR-ABL1 decline. Blood. 2014;124:511–8.
doi: 10.1182/blood-2014-03-566323
Rousselot P, Huguet F, Rea D, Legros L, Cayuela JM, Maarek O, et al. Imatinib mesylate discontinuation in patients with chronic myelogenous leukemia in complete molecular remission for more than 2 years. Blood. 2007;109:58–60.
doi: 10.1182/blood-2006-03-011239
Mahon FX, Rea D, Guilhot J, Guilhot F, Legros L, Nicolini F, et al. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre stop imatinib (STIM) trial. Lancet Oncol. 2010;11:1029–35.
doi: 10.1016/S1470-2045(10)70233-3
Saussele S, Richter J, Guilhot J, Gruber FX, Hjorth-Hansen H, Almeida A, et al. Discontinuation of treatment in chronic myeloid leukaemia—prospective analysis of molecular recurrence-free survival in the euro-ski trial. Lancet Oncol. 2018;19:747–57.
doi: 10.1016/S1470-2045(18)30192-X
Rousselot P, Charbonnier A, Cony-Makhoul P, Agape P, Nicolini FE, Varet B, et al. Loss of major molecular response as a trigger for restarting tyrosine kinase inhibitor therapy in patients with chronic-phase chronic myelogenous leukemia who have stopped imatinib after durable undetectable disease. J Clin Oncol. 2014;32:424–30.
doi: 10.1200/JCO.2012.48.5797
Hehlmann R, Lauseker M, Saussele S, Pfirrmann M, Krause S, Kolb HJ, et al. Assessment of imatinib as first-line treatment of chronic myeloid leukemia: 10-year survival results of the randomized CML study IV and impact of non-CML determinants. Leukemia. 2017;31:2398–406.
doi: 10.1038/leu.2017.253
Hochhaus A, Saglio G, Hughes TP, Larson RA, Kim DW, Issaragrisil S, et al. Long-term benefits and risks of frontline nilotinib vs imatinib for chronic myeloid leukemia in chronic phase: 5-year update of the randomized ENESTnd trial. Leukemia. 2016;30:1044–54.
doi: 10.1038/leu.2016.5
Cortes JE, Saglio G, Kantarjian HM, Baccarani M, Mayer J, Boqué C, et al. Final 5-year study results of DASISION: the dasatinib versus imatinib study in treatment—Naïve chronic myeloid leukemia patients trial. J Clin Oncol. 2016;34:2333–40.
doi: 10.1200/JCO.2015.64.8899
Hochhaus A, Baccarani M, Silver RT, Schiffer C, Apperley JF, Cervantes F, et al. European LeukemiaNet 2020 recommendations for treating chronic myeloid leukemia. Leukemia. 2020;34:966–84.
doi: 10.1038/s41375-020-0776-2
Mahon FX, Delbrel X, Cony-makhoul P, Faberes C, Boiron JM, Barthe C, et al. Follow-up of complete cytogenetic remission in patients with chronic myeloid leukemia after cessation of interferon alfa. J Clin Oncol. 2001;20:214–20.
doi: 10.1200/JCO.2002.20.1.214
Nicolini FE, Etienne G, Dubruille V, Roy L, Huguet F, Legros L, et al. Nilotinib and pegylated interferon alfa 2a for newly diagnosed chronic phase chronic myeloid leukaemia patients. Results of a multicentric phase II study. Lancet Haematol. 2015;2:e37–e46.
doi: 10.1016/S2352-3026(14)00027-1
Hjorth-Hansen H, Stentoft J, Richter J, Koskenvesa P, Höglund M, Dreimane A, et al. Safety and efficacy of the combination of pegylated interferon-α2b and dasatinib in newly diagnosed chronic-phase chronic myeloid leukemia patients. Leukemia. 2016;30:1853–60.
doi: 10.1038/leu.2016.121
Hochhaus A, Burchert A, Saussele S, Baerlocher GM, Brümmendorf TH, La Rosée P, et al. Nilotinib vs nilotinib plus pegylated interferon α (Peg-IFN) induction and nilotinib or Peg-IFN maintenance therapy for newly diagnosed BCR-ABL1 positive chronic myeloid leukemia patients in chronic phase (TIGER study): the addition of Peg-IFN is associated with higher rates of deep molecular response. Blood. 2019; 134(suppl 1): Abstract 495.
Yeung DT, Shanmuganathan N, Grigg A, Cunningham I, Shortt J, Rowling P, et al. Combination of nilotinib and pegylated interferon Alfa-2B results in high rates of MR4.5 at 24 months—primary analysis of the ALLG CML 11 Pinnacle Study. Blood. 2019; 134(suppl 1): Abstract 2926
Nicolini FE, Etienne G, Huguet F, Guerci-Bresler A, Charbonnier A, Escoffre-Barbe M, et al. The combination of nilotinib + pegylated IFN alpha 2a provides somewhat higher cumulative incidence rates of MR4.5 at M36 versus nilotinib alone in newly diagnosed CP CML patients. Updated results of the petals phase III national study. Blood. 2019;134(suppl 1): Abstract 494.

Auteurs

Francois Guilhot (F)

INSERM CIC 1402, CHU, Poitiers, France. fr.guilhot@wanadoo.fr.

Françoise Rigal-Huguet (F)

Clinical Hematology Department, I.U.C.T.O., CHU, Toulouse, France.

Joëlle Guilhot (J)

INSERM CIC 1402, CHU, Poitiers, France.

Agnès-Paule Guerci-Bresler (AP)

Clinical Hematology Department, CHRU Brabois, Vandoeuvre-les-Nancy, France.

Frédéric Maloisel (F)

Hematology Department, Clinique Sainte Anne, Strasbourg, France.

Delphine Rea (D)

Department of Hematology, Hopital Saint-Louis, APHP, Paris, France.

Valérie Coiteux (V)

Clinical Hematology Department, Hospital Claude Huriez, CHRU, Lille, France.

Martine Gardembas (M)

Department of Hematology, CHU, Angers, France.

Christian Berthou (C)

Department of Hematology, Brest University Hospital, Brest, France.

Anne Vekhoff (A)

Clinical Hematology Department, Hospital St Antoine, APHP. Sorbonne Université, Paris, France.

Eric Jourdan (E)

Hématologie Clinique, Institut de Cancérologie du Gard, CHU de Nîmes, Nîmes, France.

Marc Berger (M)

Hematologie Biologique, CHU Estaing, Clermont Ferrand, France.

Loïc Fouillard (L)

Clinical Hematology, CH Orleans, Orleans, France.

Magda Alexis (M)

Hématologie et Thérapie Cellulaire, Grand Hôpital de l'EST Francilien, Meaux, France.

Laurence Legros (L)

Department of Haematology, Hopital Paul Brousse, AP-HP, INSERM UMRS-MD1197, Villejuif, France.

Philippe Rousselot (P)

Hematology Department, Division of Innovative Therapies, Centre Hospitalier de Versailles, Versailles and Université Paris-Saclay, Inserm, CEA, Center for Immunology of Viral, Auto-immune, Hematological and Bacterial Diseases (IMVA-HB/IDMIT), Fontenay-aux-Roses & Le Kremlin-Bicêtre, France.

Alain Delmer (A)

Clinical Hematology Department, CHU, Reims, France.

Pascal Lenain (P)

Clinical Hematology Department, Centre Henri Becquerel, Rouen, France.

Martine Escoffre Barbe (M)

Clinical Hematology Department, CHU Pontchaillou, Rennes, France.

Emmanuel Gyan (E)

Hematology and Cell Therapy Department, University of Tours, Tours, France.

Claude-Eric Bulabois (CE)

Hematologie Soins Intensifs, CHU Grenoble Alpes, Grenoble, France.

Viviane Dubruille (V)

Clinical Hematology Department, CHU Hotel Dieu, Nantes, France.

Bertrand Joly (B)

Hématologie Clinique, CH Sud Francilien, Corbeil-Essonnes, France.

Bertrand Pollet (B)

Hématologie Clinique, CH Boulogne sur mer, Boulogne sur mer, France.

Pascale Cony-Makhoul (P)

Hematology Department, CH Annecy-Genevois, Epagny Metz-Tessy, Pringy, France.

Hyacinthe Johnson-Ansah (H)

Institut d'Hématologie de Basse Normandie (IHBN), CHU Côte de Nacre, Caen, France.

Melanie Mercier (M)

Service d'Dématologie Médecine Interne Maladies Infectieuses, Centre Hospitalier Bretagne Atlantique Vannes, Vannes, France.

Denis Caillot (D)

Hématologie Clinique, CHU Dijon Bourgogne, Dijon, France.

Aude Charbonnier (A)

Clinical Hematology Department, Institut Paoli Calmettes, Marseille, France.

Jean-Jacques Kiladjian (JJ)

Inserm CIC 1427, Université de Paris, Paris, France.

Jacques Chapiro (J)

Service Hématologie Clinique, Hopitaux Civiles de Colmar, Colmar, France.

Amélie Penot (A)

Service Hématologie et Thérapie Cellulaire, CHU Limoges, Limoges, France.

Véronique Dorvaux (V)

Hématologie Clinique, CHR Metz-Thionville, Metz, France.

Iona Vaida (I)

Hématologie Clinique, Centre Hospitalier René-Dubois, Cergy-Pontoise, France.

Alberto Santagostino (A)

Hématologie Clinique, CH, Troyes, France.

Lydia Roy (L)

Clinical Hematology Department, Hop Henri Mondor, APHP, UPEC, Créteil, France.

Hacene Zerazhi (H)

Service Oncologie Médicale et Hématologie Clinique, Centre Hospitalier Henri Duffaut, Avignon, France.

Eric Deconinck (E)

Service d'Hématologie, CHRU Besançon, Besançon, France.

Herve Maisonneuve (H)

Oncologie Médicale, CHD Vendée, La Roche Sur Yon, France.

Isabelle Plantier (I)

Hématologie Clinique CH Roubaix, Roubaix, France.

Delphine Lebon (D)

Service d'Hématologie Clinique CHU Amiens-Picardie, Amiens-Picardie, France.

Yazid Arkam (Y)

Service d'Hématologie GHR Mulhouse, Mulhouse, France.

Nathalie Cambier (N)

Hématologie Clinique, CH Valenciennes, Valenciennes, France.

Kamel Ghomari (K)

Service d'Hématologie-Oncologie CH Beauvais, Beauvais, France.

Jean-Michel Miclea (JM)

Service Hémato-oncologie CH Chartres, Chartres, France.

Sylvie Glaisner (S)

Service d'Hématologie Institut Curie, St Cloud, France.

Jean-Michel Cayuela (JM)

Service d'Hématologie Moléculaire, Hôpital St Louis, APHP, Paris, France.

Jean-Claude Chomel (JC)

Service Cancérologie Biologique CHU Poitiers, Poitiers, France.

Marc Muller (M)

Laboratoire de Génétique, CHRU Nancy, Nancy, France.

Ludovic Lhermitte (L)

Laboratory of Onco-Hematology, Assistance Publique-Hôpitaux de Paris, Hôpital Necker Enfants-Malades, Paris, France.

Marc Delord (M)

Clinical Research Department, Hôpital André Mignot, Versailles, France.

Claude Preudhomme (C)

Hematology Laboratory, Center for Biologic Pathology, Lille, France.

Gabriel Etienne (G)

Clinical Hematology Department, Institut Bergonié, Bordeaux, France.

François-Xavier Mahon (FX)

Clinical Hematology Department, Institut Bergonié, Bordeaux, France.

Franck-Emmanuel Nicolini (FE)

Hematology Department, INSERM U1052, CRCL, Centre Leon Berard, Lyon, France.

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