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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]
Experimental — accuracy not yet measuredIn the citing paper
“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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“PLT x10(9)/L 38 [7-517] 40 [7-128] 37 [14-517] NS”
Cechova, H., Laššuthová, P., Nováková, L., Beličková, M., Stemberkova, R., Jenčík, J., STANKOVA, M., Hrabakova, P., Pegova, K., ZIZKOVA, H., et al. (2011) · Neoplasma · doi:10.4149/neo_2012_022 · Cited by 28
“Allogeneic SCT is the only treatment modality in MDS, but is available only for selected patients depending mainly on the amount of the bone marrow blasts, comorbidities, suitable donor and other criteria (15, 18).”
BackgroundInfluentialEttou, S. S., Audureau, É., Humbrecht, C., Bénet, B., Jammes, H., Clozel, T., Bardet, V., Lacombe, C., Dreyfus, F., Mayeux, P., et al. (2012) · Leukemia · doi:10.1038/leu.2012.152 · Cited by 28
Azacitidine for the treatment of myelodysplastic syndrome
Cataldo, V. D., Cortes, J. E., & Quintás‐Cardama, A. (2009) · Expert Review of Anticancer Therapy · doi:10.1586/era.09.61 · Cited by 28
Schiffer, S., Rosinke, R., Jost, E., Hehmann-Titt, G., Hühn, M., Melmer, G., Barth, S., & Thepen, T. (2014) · International Journal of Cancer · doi:10.1002/ijc.28786 · Cited by 27
“Palliative treatments for advanced CMML include transfusions and hydroxyurea to reduce the high cell count in peripheral blood,(11) although DNA methyltransferase inhibitors may also be administered to CMML2 patients to delay transformation to AMML and reduce the frequency of transfusions.(12) AMML represents 15–20% o…”
BackgroundDan, C., Chi, J., & Wang, L. (2015) · Annals of Medicine · doi:10.3109/07853890.2015.1009156 · Cited by 27
Prognosis of Myelodysplastic Syndromes
Garcia‐Manero, G. (2010) · Hematology · doi:10.1182/asheducation-2010.1.330 · Cited by 27
Tsujioka, T., Yokoi, A., Itano, Y., Takahashi, K., Ouchida, M., Okamoto, S., Kondo, T., Suemori, S.-I., Tohyama, Y., & Tohyama, K. (2015) · Scientific Reports · doi:10.1038/srep16709 · Cited by 27
Recent advances in the treatment of lower-risk non-del(5q) myelodysplastic syndromes (MDS)
Almeida, A. M., Fenaux, P., List, A. F., Raza, A., Platzbecker, U., & Santini, V. (2016) · Leukemia Research · doi:10.1016/j.leukres.2016.11.008 · Cited by 27
Self-citationPD-1/PD-L1 as a prognostic factor in leukemia
Rezaeeyan, H., Hassani, S., Barati, M., Shahjahani, M., & Saki, N. (2017) · Journal of Hematopathology · doi:10.1007/s12308-017-0293-z · Cited by 27
“In other studies, it was found that the reduction of c-fos (a component of AP-1 factor) follows increased miR34a in MDS [76].”
InfluentialTherapeutic choices after hypomethylating agent resistance for myelodysplastic syndromes
Bravo, G. M., Garcia‐Manero, G., & Jabbour, E. J. (2017) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000400 · Cited by 27
“The hypomethylating agents azacitidine [1] and decitabine [1,2] are the standard of care for patients with MDS.”
BackgroundChronic myelomonocytic leukemia - a review
Thomopoulos, T. P., Bouhla, A., Papageorgiou, S. G., & Pappa, V. (2020) · Expert Review of Hematology · doi:10.1080/17474086.2021.1860004 · Cited by 27
Boovarahan, S. R., & Kurian, G. A. (2021) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22911 · Cited by 27
Epidemiology and Pathogenesis of Myelodysplastic Syndrome
Rotter, L. K., Shimony, S. O., Ling, K., Chen, E., Shallis, R. M., Zeidan, A. M., & Stahl, M. F. (2023) · The Cancer Journal · doi:10.1097/ppo.0000000000000665 · Cited by 27
Azacitidine: A new medication associated with Sweet syndrome
Tintle, S. J., Patel, V. K., Ruskin, A., & Halasz, C. L. (2011) · Journal of the American Academy of Dermatology · doi:10.1016/j.jaad.2010.06.032 · Cited by 27
“To the Editor: The DNA methyltransferase inhibitors azacitidine and decitabine have become the standard of care in the treatment of myelodysplastic syndrome (MDS).(1) A 69-year-old man presented with a fever and a painful vesicular patch at the site of subcutaneous azacitidine injection (Fig 1, A).”
BackgroundWang, R., Gross, C. P., Frick, K. D., Xu, X. J., Long, J. B., Raza, A., Galili, N., Zikria, J., Guan, Y., & Ma, X. (2012) · Leukemia Research · doi:10.1016/j.leukres.2012.07.020 · Cited by 27
“The subtypes were based on ICD-O-3 codes and included (1) 9980: refractory anemia (RA); (2) 9982: RA with ringed sideroblasts (RARS); (3) 9983: RA with excess blasts (RAEB); and (4) 9985: refractory cytopenia with multilineage dysplasia (RCMD).”
MethodScreening for Compounds That Modulate Epigenetic Regulation of the Transcriptome: An Overview
Eglen, R. M., & Reisine, T. (2011) · SLAS DISCOVERY · doi:10.1177/1087057111417871 · Cited by 28
Comparison of 7-day azacitidine and 5-day decitabine for treating myelodysplastic syndrome
Lee, J., Choi, Y., Kim, S.-D., Kim, D.-Y., Lee, K., Lee, K.-H., Lee, W. S., Cho, S.-H., Lee, W. S., & Joo, Y. (2013) · Annals of Hematology · doi:10.1007/s00277-013-1702-8 · Cited by 27
“administer a hypomethylating agent has been made, which drug should be chosen for a particular patient? Two metaanalyses comparing the two hypomethylating agents [5, 12] that included the same four randomised controlled trials (two trials each for azacitidine [2, 25] and decitabine [10, 15]) showed that azacitidine bu…”
BackgroundMethodInfluentialAlternative novel therapies for the treatment of elderly acute myeloid leukemia patients
Isidori, A., Venditti, A., Maurillo, L., Buccisano, F., Loscocco, F., Manduzio, P., Sparaventi, G., Amadori, S., & Visani, G. (2013) · Expert Review of Hematology · doi:10.1586/17474086.2013.858018 · Cited by 27
Zeidan, A. M., Sekeres, M. A., Wang, X., Ali, N. E. A., Garcia‐Manero, G., Steensma, D. P., Roboz, G. J., Barnard, J., Padron, E., Dezern, A. E., et al. (2015) · American Journal of Hematology · doi:10.1002/ajh.24173 · Cited by 27
“It is important to note here that it is currently unknown whether treating patients identified as LR-PSS category 3 risk with HMAs will improve their outcomes compared to conventional care regimens in a similar fashion to what was observed for patients with IPSS HR-MDS in the randomized AZA-001 trial [17].”
ResultSelf-citationPrimary Myelodysplastic Syndromes
Gangat, N., Patnaik, M. M., Begna, K. H., Kourelis, T., Al‐Kali, A., Elliott, M. A., Hogan, W. J., Letendre, L., Litzow, M. R., Knudson, R. A., et al. (2015) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2015.08.022 · Cited by 27
Moudrá, A., Hubáčková, S., Machalová, V., Vančurová, M., Bártek, J., Reiniš, M., Hodný, Z., & Jonasova, A. T. (2016) · OncoImmunology · doi:10.1080/2162402x.2016.1183860 · Cited by 27
Epigenetic landscape of the TERT promoter: a potential biomarker for high risk AML / MDS
Zhao, X., Tian, X., Kajigaya, S., Cantilena, C. R., Strickland, S. A., Savani, B. N., Mohan, S. R., Feng, X., Keyvanfar, K., Dunavin, N., et al. (2016) · British Journal of Haematology · doi:10.1111/bjh.14244 · Cited by 27
“Clinical responses to DNA methyltransferase inhibitors, such as 5-azacytidine (5-Aza), support epigenetic alterations as a fundamental pathophysiology in MDS and subsets of AML (Silverman et al, 2006; Fenaux et al, 2009; Traina et al, 2014).”
Leitch, H. A., Buckstein, R. J., Zhu, N. Y., Nevill, T. J., Yee, K. W. L., Leber, B. F., Keating, M., St‐Hilaire, È., Kumar, R., Delage, R., et al. (2018) · Leukemia Research · doi:10.1016/j.leukres.2018.09.005 · Cited by 27
Myelodysplastic syndrome from theoretical review to clinical application view
Mohammed, A. A. (2018) · Oncology Reviews · doi:10.4081/oncol.2018.397 · Cited by 29
The prognostic and therapeutic potential of HO-1 in leukemia and MDS
Sadeghi, M. R., Fathi, M., Navashenaq, J. G., Mohammadi, H., Yousefi, M., Hojjat‐Farsangi, M., Namdar, A., Akbari, A. A. M., & Jadidi‐Niaragh, F. (2023) · Cell Communication and Signaling · doi:10.1186/s12964-023-01074-8 · Cited by 27
“Another study group investigated the role of HO-1 in resistance to 5-Azacytidine (AZA), a DNA methyltransferase inhibitor used for treating MDS and AML patients [61].”
BackgroundThe evolving landscape in the therapy of acute myeloid leukemia
Peloquin, G. L., Chen, Y., & Fathi, A. T. (2013) · Protein & Cell · doi:10.1007/s13238-013-3057-2 · Cited by 26
McGovern, A. P., Powell, B. E., & Chevassut, T. J. T. (2012) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2012.06.018 · Cited by 27
“The association between epigenetic dysregulation and malignancy has culminated in recent clinical trials of hypomethylating agents (5-azacytidine and 5-aza-20-deoxycytidine) in MDS that show improved hematological responses, delayed leukemogenesis and improved overall survival (Fenaux et al., 2009).”
Combination strategies in myelodysplastic syndromes
Ornstein, M. C., & Sekeres, M. A. (2012) · International Journal of Hematology · doi:10.1007/s12185-011-0987-4 · Cited by 24
Bonifer, C., & Bowen, D. (2010) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399410001377 · Cited by 26
“965-970 149 Fenaux, P. et al. (2009) Efficacy of azacitidine”
BackgroundIn Silico Analysis Guides Selection of BET Inhibitors for Triple-Negative Breast Cancer Treatment
Pérez‐Peña, J., Serrano‐Heras, G., Montero, J. C., Corrales‐Sánchez, V., Pandiella, A., & Ocaña, A. (2016) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-16-0004 · Cited by 26
“In addition, the demethylating agent 5-azacytidine has been approved for the therapy of myelodisplastic syndromes (5).”
BackgroundEpimutational profile of hematologic malignancies as attractive target for new epigenetic therapies
Fratta, E., Montico, B., Rizzo, A., Colizzi, F., Sigalotti, L., & Dolcetti, R. (2016) · Oncotarget · doi:10.18632/oncotarget.10033 · Cited by 26
Splicing factor mutations in the myelodysplastic syndromes: target genes and therapeutic approaches
Armstrong, R. N., Steeples, V., Singh, S., Sanchi, A., Boultwood, J., & Pellagatti, A. (2017) · Advances in Biological Regulation · doi:10.1016/j.jbior.2017.09.008 · Cited by 30
“There are few effective treatments for MDS (Blum, 2016; Chamseddine et al., 2016; Fenaux et al., 2009; List et al., 2006; Steensma, 2015).”
Background
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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