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Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study
Open accessAbstract
Background Drug treatments for patients with high-risk myelodysplastic syndromes provide no survival advantage. In this trial, we aimed to assess the effect of azacitidine on overall survival compared with the three commonest conventional care regimens.Methods In a phase III, international, multicentre, controlled, parallel-group, open-label trial, patients with higher-risk myelodysplastic syndromes were randomly assigned one-to-one to receive azacitidine (75 mg/m(2) per day for 7 days every 28 days) or conventional care (best supportive care, low-dose cytarabine, or intensive chemotherapy as selected by investigators before randomisation). Patients were stratified by French-American-British and international prognostic scoring system classifications; randomisation was done with a block size of four. The primary endpoint was overall survival. Efficacy analyses were by intention to treat for all patients assigned to receive treatment. This study is registered with ClinicalTrials.gov, number NCT00071799.Findings Between Feb 13, 2004, and Aug 7, 2006, 358 patients were randomly assigned to receive azacitidine (n=179) or conventional care regimens (n=179). Four patients in the azacitidine and 14 in the conventional care groups received no study drugs but were included in the intention-to-treat efficacy analysis. After a median follow-up of 21.1 months (IQR 15.1-26.9), median overall survival was 24.5 months (9.9-not reached) for the azacitidine group versus 15.0 months (5.6-24.1) for the conventional care group (hazard ratio 0.58; 95% CI 0.43-0.77; stratified log-rank p=0.0001). At last follow-up, 82 patients in the azacitidine group had died compared with 113 in the conventional care group. At 2 years, on the basis of Kaplan-Meier estimates, 50.8% (95% CI 42.1-58.8) of patients in the azacitidine group were alive compared with 26.2% (18.7-34.3) in the conventional care group (p<0.0001). Peripheral cytopenias were the most common grade 3-4 adverse events for all treatments.Interpretation Treatment with azacitidine increases overall survival in patients with higher-risk myelodysplastic syndromes relative to conventional care.
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“Hypomethylating agents (HMAs), such as azacitidine and decitabine, yield statistically similar complete remission (CR) rates of approximately 15%-20% in patients with either TP53-mutant or wild-type MDS.12-14”
From Eprenetapopt (APR-246) and Azacitidine in TP53 -Mutant Myelodysplastic Syndromes (2021) · cites this paper as [14]
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“Adverse events were similar to those reported for azacitidine or eprenetapopt monotherapy, with the most common grade ≥ 3 adverse events being febrile neutropenia (33%), leukopenia (29%), and neutropenia (29%).”
From Eprenetapopt (APR-246) and Azacitidine in TP53 -Mutant Myelodysplastic Syndromes (2021) · cites this paper as [14]
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“Whilst response rates of up to 60% to azacytidine have been reported in MDS 125,129 ,”
From The roles of DNA, RNA and histone methylation in ageing and cancer (2019) · cites this paper as [129]
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“Azacitidine Celgene approved[92,93]”
Gene-Specific Targeting of DNA Methylation in the Mammalian Genome
Urbano, A., Smith, J., Weeks, R. J., & Chatterjee, A. (2019) · Cancers · doi:10.3390/cancers11101515 · Cited by 67
“DNA methyltransferase inhibitors (DNMTi) are the mainstay drugs for therapies, mainly used in the treatment of myelodysplastic syndrome and acute myeloid leukemia [60,61].”
BackgroundOhtani, H., Ørskov, A. D., Helbo, A. S., Gillberg, L., Liu, M., Zhou, W., Ungerstedt, J. S., Hellström‐Lindberg, E., Sun, W., Liang, G., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-1696 · Cited by 67
“Yet only about half of the patients respond to the treatment, and most patients become resistant over time (1, 2).”
BackgroundSingle-cell gene regulatory network prediction by explainable AI
Keyl, P., Bischoff, P., Dernbach, G., Bockmayr, M. L., Fritz, R., Horst, D. A., Blüthgen, N., Montavon, G., Müller, K., & Klauschen, F. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac1212 · Cited by 72
Mishra, A., Corrales‐Yepez, M., Ali, N. E. A., Kharfan‐Dabaja, M. A., Padron, E., Zhang, L., Epling‐Burnette, P. K., Pinilla-Ibarz, J. A., Lancet, J. E., List, A. F., et al. (2013) · American Journal of Hematology · doi:10.1002/ajh.23454 · Cited by 71
“in which there is recognized survival advantage for patients with higher risk MDS [7].”
BackgroundSelf-citationDinmohamed, A. G., Visser, O. J., van Norden, Y., Huijgens, P. C., Sonneveld, P., van de Loosdrecht, A. A., & Jongen‐Lavrencic, M. (2014) · European Journal of Cancer · doi:10.1016/j.ejca.2013.12.002 · Cited by 68
“azacitidine [18] and decitabine [19].”
Opportunity Cost of Funding Drugs for Rare Diseases
Coyle, D., Cheung, M. C., & Evans, G. A. (2014) · Medical Decision Making · doi:10.1177/0272989x14539731 · Cited by 66
Quintás‐Cardama, A., Daver, N. G., Kim, H., Dinardo, C. D., Jabbour, E. J., Kadia, T. M., Borthakur, G. M., Pierce, S. A., Shan, J., Cárdenas-Turanzas, M., et al. (2014) · Clinical Lymphoma Myeloma & Leukemia · doi:10.1016/j.clml.2014.03.001 · Cited by 66
“, hypomethylating agents) have been shown to prolong the survival of patients with de novo MDS.(38) The importance of the present”
BackgroundAzacitidine: A Review in Myelodysplastic Syndromes and Acute Myeloid Leukaemia
Scott, L. J. (2016) · Drugs · doi:10.1007/s40265-016-0585-0 · Cited by 66
“Key exclusion criteria included prior treatment with azacitidine, a diagnosis of therapy-induced MDS and planned allogeneic HSCT [31].”
BackgroundMethodResultInfluentialWanner, N., & Bechtel‐Walz, W. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2588-x · Cited by 66
“…being used in cancer treatment, such as the correction of CpG methylation through the administration of de-methylating agents or the targeting of histonemodifying enzymes (Dawson and Kouzarides 2012; Fenaux et al. 2009; Jones 2012), will be transferred into clinical usage in patients with CKD.”
Daher-Reyes, G. S., Merchán, B., & Yee, K. W. L. (2019) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2019.1667331 · Cited by 66
“Toxicities were comparable between the 2 dose groups [Table 3] and comparable to other HMAs [11,13].”
ResultEpigenetic regulation of mmp-9 gene expression
Labrie, M., & St‐Pierre, Y. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1214-z · Cited by 65
“Cervical carcinoma SiHa, Caski Timp-2 : [130] 5-Aza-20deoxycytidine Colon cancer RKO, SW48, SW480, HT29 Timp-3 : [131]”
Müller‐Thomas, C., Rudelius, M., Rondak, I., Haferlach, T., Schanz, J., Huberle, C., Schmidt, B., Blaser, R., Kremer, M., Peschel, C., et al. (2014) · Haematologica · doi:10.3324/haematol.2014.104760 · Cited by 67
“5-Aza cycles Median (range) 4 (1-29) 5 (1-22) 0.”
Therapeutic Choice in Older Patients with Acute Myeloid Leukemia: A Matter of Fitness
Palmieri, R., Paterno, G., Bellis, E. D., Mercante, L., Buzzatti, E., Esposito, F., Principe, M. I. D., Maurillo, L., Buccisano, F., & Venditti, A. (2020) · Cancers · doi:10.3390/cancers12010120 · Cited by 66
“Being randomized in the AZA arm was also associated with fewer total days of hospital staying [43].”
BackgroundDecitabine in the treatment of myelodysplastic syndromes
Santos, F. P., Kantarjian, H. M., Garcia‐Manero, G., Issa, J. J., & Ravandi, F. (2009) · Expert Review of Anticancer Therapy · doi:10.1586/era.09.164 · Cited by 66
Boumber, Y., Kantarjian, H. M., Jorgensen, J. L., Wen, S., Faderl, S. H., Castoro, R. J., Autry, J., García-Manero, G., Borthakur, G. M., Jabbour, E., et al. (2012) · Leukemia · doi:10.1038/leu.2012.153 · Cited by 64
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Self-citationHeidenreich, S., Ziagkos, D., de Wreede, L. C., van Biezen, A., Finke, J., Platzbecker, U., Niederwieser, D. W., Einsele, H., Bethge, W. A., Schleuning, M., et al. (2016) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2016.09.027 · Cited by 64
“In this situation, demethylating agents as azacitidine or decitabine provide a survival benefit [11-15].”
BackgroundPancreatic Cancer Heterogeneity Can Be Explained Beyond the Genome
Juiz, N. A., Iovanna, J., & Dusetti, N. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00246 · Cited by 63
The Translational Status of Cancer Liquid Biopsies
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NPM1 ‐mutated acute myeloid leukemia: New pathogenetic and therapeutic insights and open questions
Falini, B. (2023) · American Journal of Hematology · doi:10.1002/ajh.26989 · Cited by 70
Cashen, A. F., Juckett, M. B., Jumonville, A. J., Litzow, M. R., Flynn, P. J., Eckardt, J. R., LaPlant, B. R., Laumann, K. M., Erlichman, C., & DiPersio, J. F. (2011) · Annals of Hematology · doi:10.1007/s00277-011-1240-1 · Cited by 63
“The use of HDAC inhibitors in MDS has been approached with enthusiasm, given the preclinical evidence that HDAC inhibitors promote differentiation in malignant myeloid cell lines [1] and the fact that hypomethylating agents, which also act via epigenetic mechanisms, have established efficacy in MDS [13, 14].”
BackgroundHypomethylating agent combination strategies in myelodysplastic syndromes: hopes and shortcomings
Ball, B. J., Zeidan, A. M., Gore, S. D., & Prébet, T. (2016) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428194.2016.1228927 · Cited by 64
“[17] Evidence supporting use of decitabine in high risk MDS comes from a randomized phase III trial, which showed an overall response rate of 30% and a trend toward a longer median time to AML or death (12.1 months vs. 7.8 months P =0.16 by the log-rank test) when compared to conventional care.”
InfluentialSelf-citationSchroeder, T. A., Rautenberg, C., Haas, R. R., Germing, U., & Kobbe, G. (2017) · International Journal of Hematology · doi:10.1007/s12185-017-2364-4 · Cited by 63
Zeidan, A. M., Stahl, M. F., DeVeaux, M., Giri, S., Huntington, S. F., Podoltsev, N. A., Wang, R., Ma, X., Davidoff, A. J., & Gore, S. D. (2018) · Blood Cancer Journal · doi:10.1038/s41408-018-0081-8 · Cited by 62
Self-citationChien, K. S., Kim, K., Nogueras‐González, G. M., Borthakur, G. M., Naqvi, K., Daver, N. G., Bravo, G. M., Cortes, J. E., Dinardo, C. D., Jabbour, E. J., et al. (2021) · British Journal of Haematology · doi:10.1111/bjh.17689 · Cited by 62
“Age, years/gender 71 M 80 M 65 M 83 M 72 M IPSS INT-1 INT-1 INT-1 High INT-2 Prior HMA cycles, n 15 9 29 6 11 Best response HI-P CR mCR HI-P mCR Laboratory values at baseline and best response* WBC, 910(9)/l 1 1 1 2 3 5 3 8 4 3 3 4 1 6 1 4 0 6 0 6 ANC, 910(9)/l 0 76 0 47 1 26 2 13 2 33 1 81 0 70 0 73 0 19 0 05 Haemogl…”
Laille, E. J., Shi, T., Garcia‐Manero, G., Cogle, C. R., Gore, S. D., Hetzer, J., Kumar, K., Skikne, B., & MacBeth, K. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135520 · Cited by 62
Self-citationCould valproic acid be an effective anticancer agent? The evidence so far
Brodie, S. A., & Brandes, J. C. (2014) · Expert Review of Anticancer Therapy · doi:10.1586/14737140.2014.940329 · Cited by 62
“patients with poor-risk myelodysplasia was proof of concept for a major role of epigenetic therapies in cancer [6].”
BackgroundPotter, V. T., Iacobelli, S., van Biezen, A., Maertens, J., Bourhis, J.-H., Passweg, J. R., Yakoub‐Agha, I., Tabrizi, R., Bay, J., Chevallier, P., et al. (2016) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2016.05.026 · Cited by 62
“The demonstration of the utility of azacitidine (AZA) and other hypomethylating (HMA) agents for the treatment of higher risk MDS in recent years [1,2] has provided an alternative approach to pretransplantation induction therapy.”
BackgroundSelf-citationTobiasson, M., Abdulkadir, H., Lennartsson, A., Katayama, S., Marabita, F., Paepe, A. D., Karimi, M., Krjutškov, K., Einarsdóttir, E., Grövdal, M., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.15807 · Cited by 64
“Azacitidine (Aza) is a cytosine analog and an inhibitor of DNA methyl transferase (DNMT) licensed in Europe as first-line treatment for higher-risk myelodysplastic syndromes, in the US for all types of MDS and frequently used also in other myeloid malignancies, such as acute myeloid [8, 9] Treatment has been confident…”
BackgroundZeidan, A. M., Boss, I., Beach, C. L., Copeland, W. B., Thompson, E., Fox, B. A., Hasle, V. E., Ogasawara, K., Cavenagh, J., Silverman, L. R., et al. (2022) · Blood Advances · doi:10.1182/bloodadvances.2021005487 · Cited by 61
Self-citationTargeting the epigenome for treatment of cancer
Geutjes, E.-J., Bajpe, P. K., & Bernards, R. (2011) · Oncogene · doi:10.1038/onc.2011.552 · Cited by 62
“(2005) Azacitidine Celgene AML P3 (2) (Fenaux et al., 2009; Fenaux et al., 2010) Azacitidine Celgene MF, MM, prostate cancer, lung cancer P2 (4) (Sonpavde et al.”
BackgroundPleyer, L., Stauder, R., Burgstaller, S., Schreder, M., Tinchon, C., Pfeilstöcker, M., Steinkirchner, S., Melchardt, T., Mitrovic, M., Girschikofsky, M., et al. (2013) · Journal of Hematology & Oncology · doi:10.1186/1756-8722-6-32 · Cited by 61
“Azacitidine was not always second line therapy in chemotherapy refractory patients, but t-AML indicates treatment related AML; AML-RCA, AML with recurrent cytogenetic abnormalities; AML-MRF, AML with MDS related features; MPN, myeloproliferative neoplasia; MLD, multilineage dysplasia; MRC, MDS-related cytogenetics; AM…”
BackgroundResultInfluentialHypoxia, Epithelial-Mesenchymal Transition, and TET-Mediated Epigenetic Changes
Kao, S.-H., Wu, K., & Lee, W. (2016) · Journal of Clinical Medicine · doi:10.3390/jcm5020024 · Cited by 64
“, hypermethylation of tumor suppressor genes in cancers, can be corrected by hypomethylating agents, such as 5-azacitidine and decitabine [92,93], and their applicability has already been tested in clinical studies.”
Recent advances in the understanding and treatment of acute myeloid leukemia
Watts, J. M., & Nimer, S. D. (2018) · F1000Research · doi:10.12688/f1000research.14116.1 · Cited by 61
Clinical update on hypomethylating agents
Duchmann, M., & Itzykson, R. (2019) · International Journal of Hematology · doi:10.1007/s12185-019-02651-9 · Cited by 60
The role of vitamin C in epigenetic cancer therapy
Mikkelsen, S. U., Gillberg, L., Lykkesfeldt, J., & Grønbæk, K. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.03.017 · Cited by 62
Germing, U., Kobbe, G., Haas, R. R., & Gattermann, N. (2013) · Deutsches Ärzteblatt international · doi:10.3238/arztebl.2013.0783 · Cited by 67
Self-citation
Metadata
- Authors
- Fenaux, P., Mufti, G. J., Hellstrom-Lindberg, E., Santini, V., Finelli, C., Giagounidis, A., Schoch, R., Gattermann, N., Sanz, G., List, A., Gore, S. D., Seymour, J. F., Bennett, J. M., Byrd, J., Backstrom, J., Zimmerman, L., McKenzie, D., Beach, C., & Silverman, L. R.
- Affiliations
- Université Sorbonne Paris Nord (FR)
- King's College Hospital (GB)
- Azienda Ospedaliero-Universitaria Careggi (IT)
- University Hospital Schleswig-Holstein (DE)
- Düsseldorf University Hospital (DE)
- Hospital Universitari i Politècnic La Fe (ES)
- Moffitt Cancer Center (US)
- Johns Hopkins University (US)
- Karolinska University Hospital (SE)
- University of Rochester Medicine (US)
- The Ohio State University (US)
- Celgene (United States) (US)
- Icahn School of Medicine at Mount Sinai (US)
- Corresponding author
- Fenaux, Pierre
- ORCID
- Venue
- The Lancet Oncology
- Publisher
- Elsevier BV
- Published
- 2009-03
- Volume
- 10
- Issue
- 3
- Pages
- 223-232
- ISSN
- 1470-2045 (ISSN-L)
- PMC
- PMC4086808
- OpenAlex
- W2118771330
- Cited by
- 2,663
- References
- 45
- Citations by year
- 2026: 80 · 2025: 99 · 2024: 103 · 2023: 153 · 2022: 149 · 2021: 182 · 2020: 148 · 2019: 149 · 2018: 132 · 2017: 164 · 2016: 178 · 2015: 173 · 2014: 201 · 2013: 182 · 2012: 178
- FWCI
- 124.66
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Lancet Oncology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Florence Research (University of Florence) (submittedVersion)
- IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Celgene
- National Cancer Institute (K24CA111717)
- Topics
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Keywords
- azacitidine, myelodysplastic syndrome, high-risk myelodysplastic syndrome, overall survival, low-dose cytarabine, intensive chemotherapy, best supportive care, hypomethylating agents, treatment efficacy comparison, hematologic malignancies
- MeSH terms
- Adult, Aged, Aged, 80 and over, Antimetabolites, Antineoplastic, Azacitidine, Female, Humans, Male, Middle Aged, Myelodysplastic Syndromes, Proportional Hazards Models
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