Yıl: 2023 Cilt: 40 Sayı: 2 Sayfa Aralığı: 92 - 100 Metin Dili: İngilizce DOI: 10.4274/tjh.galenos.2023.2022.0437 İndeks Tarihi: 01-06-2023

Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data

Öz:
Objective: This study was undertaken to evaluate the long-term clinical efficacy of epoetin alfa and darbepoetin alfa in patients with myelodysplastic syndrome (MDS) in a real-life setting. Materials and Methods: A total of 204 patients with low-risk or intermediate-1-risk MDS who received epoetin alfa or darbepoetin alfa were included. Hemoglobin levels and transfusion needs were recorded before treatment and at 12 months, 24 months, 36 months, and 48 months of treatment. Results: At the 36-month (p=0.025) and 48-month (p=0.022) visits, epoetin alfa yielded significantly higher hemoglobin levels compared to darbepoetin alfa. Transfusion needs were also significantly lower with epoetin alfa compared to darbepoetin alfa at 24 months (p=0.012) and in the low-risk group compared to the intermediate-risk group at 24 months (p=0.018), 36 months (p=0.025), and 48 months (p<0.001). Treatment response rates at the 24-month, 36-month, and 48-month visits in the epoetin alfa (43.0%, 33.6%, and 27.1%), darbepoetin alfa (29.9%, 22.7%, and 16.5%), low-risk (39.3%, 30.0%, and 26.0%), and intermediate-risk (29.6%, 24.1%, and 11.1%) groups were lower than those obtained at 12 months, and the values differed significantly for the 36-month and 48-month visits with values ranging from p<0.05 to p<0.001. Conclusion: This real-life long-term ESA extension study investigated the clinical efficacy of epoetin alfa and darbepoetin alfa for up to 48 months, revealing that treatment efficacy reached a plateau starting from the 24th month of therapy with a continuing decrease in treatment response rates regardless of treatment type, risk status, or gender. Nonetheless, significantly higher hemoglobin levels and marked improvement in transfusion needs were evident in epoetintreated patients compared to darbepoetin-treated patients and in the low-risk group compared to the intermediate-risk group.
Anahtar Kelime:

Eritropoezi Stimüle Edici Ajanların Düşük Riskli veya Orta-1 Riskli Myelodisplastik Sendromlu Hastalarda Uzun Dönem Tedavi Etkinliğinin Değerlendirilmesi: Çok Merkezli Gerçek Yaşam Verisi

Öz:
Amaç: Myelodisplastik sendromlu (MDS) hastalarda epoetin alfa ve darbepoetin alfa tedavisinin gerçek yaşam ortamında uzun-dönem klinik etkinliğini değerlendirmek. Gereç ve Yöntemler: Bu çalışmaya düşük veya orta-1 risk grubu MDS tanısı ile epoetin alfa veya darbepoetin alfa tedavisi almış 204 hasta dahil edildi. Hemoglobin düzeyleri ve transfüzyon gereksinimi, tedaviden önce ve tedavinin 12., 24., 36. ve 48. aylarında değerlendirildi. Bulgular: Epoetin alfa, darbepoetin alfa ile kıyaslandığında, 36. ay (p=0,025) ve 48. aylarda (p=0,022) anlamlı şekilde daha yüksek hemoglobin düzeylerini sağladı. Transfüzyon gereksinimi 24. ayda (p=0,012) epoetin alfa grubunda darbepoetin alfa grubuna göre, 24. ay (p=0,018), 36. ay (p=0,025) ve 48. aylarda (p<0,001) ise düşük risk grubunda orta risk grubuna göre anlamlı şekilde daha düşük olarak bulundu. Tedavi yanıt oranları 24. ay, 36. ay ve 48. aylarda epoetin alfa (%43,0, %33,6 ve %27,1), darbepoetin alfa (%29,9, %22,7 ve %16,5), düşük risk (%39,3, %30,0 ve %26,0) ve orta risk (%29,6, %24,1 ve %11,1) gruplarında 12. ay yanıt oranlarına göre daha düşük olup, 36. ve 48. aylarda bu değişim istatistiksel olarak anlamlı idi (p<0,05 ile <0,001 arası). Sonuç: Epoetin alfa ve darbepoetin alfanın 48 aylık klinik etkililiğinin değerlendirildiği bu gerçek-yaşam uzun-dönem ESA çalışmasında, tedavi etkililiğinin tedavinin 24. ayından başlayarak plato evresine eriştiği ve devamında tedavi yanıt oranlarında, tedavi tipi, risk durumu veya cinsiyetten bağımsız olarak süregiden bir düşüşün gerçekleştiği saptandı. Bununla birlikte, epoetin tedavisi alan grupta darbepoetin ile tedavi edilen gruba göre ve düşük risk grubu hastalarda orta risk grubu hastalara göre, hemoglobin düzeyleri anlamlı şekilde daha yüksek olup, transfüzyon gereksiniminde de belirgin azalma olduğu tespit edildi.
Anahtar Kelime:

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık
  • 1. Park S, Greenberg P, Yucel A, Farmer C, O’Neill F, De Oliveira Brandao C, Fenaux P. Clinical effectiveness and safety of erythropoietin-stimulating agents for the treatment of low- and intermediate-1-risk myelodysplastic syndrome: a systematic literature review. Br J Haematol 2019;184:134-160.
  • 2. Malcovati L, Hellström-Lindberg E, Bowen D, Adès L, Cermak J, Del Cañizo C, Della Porta MG, Fenaux P, Gattermann N, Germing U, Jansen JH, Mittelman M, Mufti G, Platzbecker U, Sanz GF, Selleslag D, Skov-Holm M, Stauder R, Symeonidis A, van de Loosdrecht AA, de Witte T, Cazzola M; European LeukemiaNet. Diagnosis and treatment of primary myelodysplastic syndromes in adults: recommendations from the European LeukemiaNet. Blood 2013;122:2943-2964.
  • 3. Fenaux P, Haase D, Sanz GF, Santini V, Buske C; ESMO Guidelines Working Group. Myelodysplastic syndromes: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2014;25(Suppl 3):57-69.
  • 4. Killick SB, Carter C, Culligan D, Dalley C, Das-Gupta E, Drummond M, Enright H, Jones GL, Kell J, Mills J, Mufti G, Parker J, Raj K, Sternberg A, Vyas P, Bowen D; British Committee for Standards in Haematology. Guidelines for the diagnosis and management of adult myelodysplastic syndromes. Br J Haematol 2014;164:503-525.
  • 5. Park S, Kelaidi C, Sapena R, Vassilieff D, Beyne-Rauzy O, Coiteux V, Vey N, Ravoet C, Cheze S, Rose C, Legros L, Stamatoullas A, Escoffre-Barbe M, Guerci A, Chaury MP, Fenaux P, Dreyfus F. Early introduction of ESA in low risk MDS patients may delay the need for RBC transfusion: a retrospective analysis on 112 patients. Leuk Res 2010;34:1430-1436.
  • 6. Park S, Kelaidi C, Sapena R, Vassilieff D, Beyne-Rauzy O, Coiteux V, Vey N, Ravoet C, Cheze S, Rose C, Legros L, Stamatoullas A, Escoffre-Barbe M, Guerci A, Chaury MP, Fenaux P, Dreyfus F. Predictive factors of response and survival in myelodysplastic syndrome treated with erythropoietin and G-CSF: the GFM experience. Blood 2008;111:574-582.
  • 7. Duong VH, Baer MR, Hendrick F, Weiss SR, Sato M, Zeidan AM, Gore SD, Davidoff AJ. Variations in erythropoiesis-stimulating agent administration in transfusion-dependent myelodysplastic syndromes impact response. Leuk Res 2015;39:586-591.
  • 8. Greenberg PL, Attar E, Bennett JM, Bloomfield CD, Borate U, De Castro CM, Deeg HJ, Frankfurt O, Gaensler K, Garcia-Manero G, Gore SD, Head D, Komrokji R, Maness LJ, Millenson M, O’Donnell MR, Shami PJ, Stein BL, Stone RM, Thompson JE, Westervelt P, Wheeler B, Shead DA, Naganuma M. Myelodysplastic syndromes: clinical practice guidelines in oncology. J Natl Compr Canc Netw 2013;11:838-874.
  • 9. Negrin RS, Stein R, Doherty K, Cornwell J, Vardiman J, Krantz S, Greenberg PL. Maintenance treatment of the anemia of myelodysplastic syndromes with recombinant human granulocyte colony-stimulating factor and erythropoietin: evidence for in vivo synergy. Blood 1996;87:4076-4081.
  • 10. Moura ATG, Duarte FB, Barbosa MC, Santos TEJD, Lemes RPG. Prolonged response to recombinant human erythropoietin treatment in patients with myelodysplastic syndrome at a single referral centre in Brazil. Clinics (Sao Paulo) 2019;74:e771.
  • 11. Carraway HE, Saygin C. Therapy for lower-risk MDS. Hematology Am Soc Hematol Educ Program. 2020;2020:426-433.
  • 12. Ak MA, Sahip B, Geduk A, Ucar MA, Kale H, Hacibekiroglu T, Polat MG, Kalpakci Y, Bolaman AZ, Guvenc B, Ertop S. The clinical efficacy of epoetin alfa and darbepoetin alfa in patients with low-risk or intermediate-1-risk myelodysplastic syndrome: retrospective multi-center real-life study. Indian J Hematol Blood Transfus 2022;38:299-308.
  • 13. Greenberg P, Cox C, LeBeau MM, Fenaux P, Morel P, Sanz G, Sanz M, Vallespi T, Hamblin T, Oscier D, Ohyashiki K, Toyama K, Aul C, Mufti G, Bennett J. International scoring system for evaluating prognosis in myelodysplastic syndromes. Blood 1997;89:2079-2088.
  • 14. Tefferi A, Barosi G, Mesa RA, Cervantes F, Deeg HJ, Reilly JT, Verstovsek S, Dupriez B, Silver RT, Odenike O, Cortes J, Wadleigh M, Solberg LA Jr, Camoriano JK, Gisslinger H, Noel P, Thiele J, Vardiman JW, Hoffman R, Cross NC, Gilliland DG, Kantarjian H; IWG for Myelofibrosis Research and Treatment (IWG-MRT). International Working Group (IWG) consensus criteria for treatment response in myelofibrosis with myeloid metaplasia, for the IWG for Myelofibrosis Research and Treatment (IWG-MRT). Blood 2006;108:1497-1503.
  • 15. Jädersten M, Malcovati L, Dybedal I, Della Porta MG, Invernizzi R, Montgomery SM, Pascutto C, Porwit A, Cazzola M, Hellström-Lindberg E. Erythropoietin and granulocyte-colony stimulating factor treatment associated with improved survival in myelodysplastic syndrome. J Clin Oncol 2008;26:3607-3613.
  • 16. Ross SD, Allen IE, Probst CA, Sercus B, Crean SM, Ranganathan G. Efficacy and safety of erythropoiesis-stimulating proteins in myelodysplastic syndrome: a systematic review and meta-analysis. Oncologist 2007;12:1264-1273.
  • 17. Kelaidi C, Beyne-Rauzy O, Braun T, Sapena R, Cougoul P, Adès L, Pillard F, Lamberto C, Charniot JC, Guerci A, Choufi B, Stamatoullas A, Slama B, De Renzis B, Ame S, Damaj G, Boyer F, Chaury MP, Legros L, Cheze S, Testu A, Gyan E, Béné MC, Rose C, Dreyfus F, Fenaux P. High response rate and improved exercise capacity and quality of life with a new regimen of darbepoetin alfa with or without filgrastim in lower-risk myelodysplastic syndromes: a phase II study by the GFM. Ann Hematol 2013;92:621-631.
  • 18. Fenaux P, Santini V, Spiriti MAA, Giagounidis A, Schlag R, Radinoff A, Gercheva-Kyuchukova L, Anagnostopoulos A, Oliva EN, Symeonidis A, Berger MH, Götze KS, Potamianou A, Haralampiev H, Wapenaar R, Milionis I, Platzbecker U. A phase 3 randomized, placebo-controlled study assessing the efficacy and safety of epoetin-α in anemic patients with low-risk MDS. Leukemia 2018;32:2648-2658.
  • 19. Spiriti MA, Latagliata R, Niscola P, Cortelezzi A, Francesconi M, Ferrari D, Volpe E, Clavio M, Grossi A, Reyes MT, Musto P, Mitra ME, Azzarà A, Pagnini D, D'Arena G, Spadano A, Balleari E, Pecorari P, Capochiani E, De Biasi E, Perego D, Monarca B, Pisani F, Scaramella G, Petti MC. Impact of a new dosing regimen of epoetin alfa on quality of life and anemia in patients with low-risk myelodysplastic syndrome. Ann Hematol 2005;84:167-176.
  • 20. Greenberg PL, Sun Z, Miller KB, Bennett JM, Tallman MS, Dewald G, Paietta E, van der Jagt R, Houston J, Thomas ML, Cella D, Rowe JM. Treatment of myelodysplastic syndrome patients with erythropoietin with or without granulocyte colony-stimulating factor: results of a prospective randomized phase 3 trial by the Eastern Cooperative Oncology Group (E1996). Blood 2009;114:2393-2400.
  • 21. Musto P, Villani O, Martorelli MC, Pietrantuono G, Guariglia R, Mansueto G, D’Auria F, Grieco V, Bianchino G, Sparano A, Zonno A, Lerose R, Sanpaolo G, Falcone A. Response to recombinant erythropoietin alpha, without the adjunct of granulocyte-colony stimulating factor, is associated with a longer survival in patients with transfusion-dependent myelodysplastic syndromes. Leuk Res 2010;34:981-985.
  • 22. Gotlib J, Lavori P, Quesada S, Stein RS, Shahnia S, Greenberg PL. A phase II intra-patient dose-escalation trial of weight-based darbepoetin alfa with or without granulocyte-colony stimulating factor in myelodysplastic syndromes. Am J Hematol 2009;84:15-20.
  • 23. Mannone L, Gardin C, Quarre MC, Bernard JF, Vassilieff D, Ades L, Park S, Vaultier S, Hamza F, Beyne-Rauzy MO, Cheze S, Giraudier S, Agape P, Legros L, Voillat L, Dreyfus F, Fenaux P; Groupe Francais des Myelodysplasies. High-dose darbepoetin alpha in the treatment of anaemia of lower risk myelodysplastic syndrome results of a phase II study. Br J Haematol 2006;133:513-519.
  • 24. Oliva EN, Nobile F, Alimena G, Specchia G, Danova M, Rovati B, Ronco F, Impera S, Risitano A, Alati C, Breccia M, Carmosino I, Vincelli I, Latagliata R. Darbepoetin alfa for the treatment of anemia associated with myelodysplastic syndromes: efficacy and quality of life. Leuk Lymphoma 2010;51:1007-1014.
  • 25. Sekeres MA, Schoonen WM, Kantarjian H, List A, Fryzek J, Paquette R, Maciejewski JP. Characteristics of US patients with myelodysplastic syndromes: results of six cross-sectional physician surveys. J Natl Cancer Inst 2008;100:1542-1551.
  • 26. Pierri I, Balleari E, Olcese E, Passalia C, Calvia A, Clavio M, Varaldo R, Miglino M, Ballerini F, Canepa L, Ghiggi C, Vignolo L, Ghiso A, Ghio R, Gobbi M. High dose of r-EPO (40,000 IU) once a week is highly effective in a selected cohort of MDS patients with basal EPO level < 250mu/mi, IPSS score ≤ 1.5 and low transfusional need [abstract]. Leuk Res 2007;31:S140.
  • 27. Mele G, Musto C, Matera R, Vigliotti ML, Tartarone A, Romano G, Coccaro MR, Di Renzo N. High-dose of epoetin alfa in patients with low-risk myelodysplastic syndromes (MDS): a single institution experience. Blood 2004;104:260B.
  • 28. Park S, Hamel JF, Toma A, Kelaidi C, Thépot S, Campelo MD, Santini V, Sekeres MA, Balleari E, Kaivers J, Sapena R, Götze K, Müller-Thomas C, Beyne-Rauzy O, Stamatoullas A, Kotsianidis I, Komrokji R, Steensma DP, Fensterl J, Roboz GJ, Bernal T, Ramos F, Calabuig M, Guerci-Bresler A, Bordessoule D, Cony- Makhoul P, Cheze S, Wattel E, Rose C, Vey N, Gioia D, Ferrero D, Gaidano G, Cametti G, Pane F, Sanna A, Germing U, Sanz GF, Dreyfus F, Fenaux P. Outcome of lower-risk patients with myelodysplastic syndromes without 5q deletion after failure of erythropoiesis-stimulating agents. J Clin Oncol 2017;35:1591-1597.
  • 29. Park S, Fenaux P, Greenberg P, Mehta B, Callaghan F, Kim C, Tomita D, Xu H. Efficacy and safety of darbepoetin alpha in patients with myelodysplastic syndromes: a systematic review and meta-analysis. Br J Haematol 2016;174:730-747.
  • 30. Gascón P, Krendyukov A, Mathieson N, Aapro M. Epoetin alfa for the treatment of myelodysplastic syndrome-related anemia: a review of clinical data, clinical guidelines, and treatment protocols. Leuk Res 2019;81:35-42.
  • 31. Moyo V, Lefebvre P, Duh MS, Yektashenas B, Mundle S. Erythropoiesisstimulating agents in the treatment of anemia in myelodysplastic syndromes: a meta-analysis. Ann Hematol 2008;87:527-536.
  • 32. Velloso EDRP, Magalhães SMM, Chauffaille MLLF, Buzzini R, Bernardo WM. Part 3: Myelodysplastic syndromes—Treatment of low-risk patients without the 5q deletion. Hematol Transfus Cell Ther 2018;40:267-273.
  • 33. Harnan S, Ren S, Gomersall T, Everson-Hock ES, Sutton A, Dhanasiri S, Kulasekararaj A. Association between transfusion status and overall survival in patients with myelodysplastic syndromes: a systematic literature review and meta-analysis. Acta Haematol 2016;136:23-42.
  • 34. Symeonidis A, Zikos P, Galanopoulos A, Kotsianidis I, Kouraklis A, Protopapa M, Psyllaki M, Lambropoulou V, Aktypi A, Bakarakos P, TSatalas C. Response to treatment with erythropoietin in patients with MDS highly predicts low risk of evolution to AML and longer survival. Leuk Res 2011;35:S127-128.
  • 35. Platzbecker U, Symeonidis A, Oliva EN, Goede JS, Delforge M, Mayer J, Slama B, Badre S, Gasal E, Mehta B, Franklin J. A phase 3 randomized placebo-controlled trial of darbepoetin alfa in patients with anemia and lower-risk myelodysplastic syndromes. Leukemia 2017;31:1944-1950.
  • 36. Santini V. Clinical use of erythropoietic stimulating agents in myelodysplastic syndromes. Oncologist 2011;16(Suppl 3):35-42.
  • 37. Hellström-Lindberg E, Malcovati L. Supportive care, growth factors, and new therapies in myelodysplastic syndromes. Blood Rev 2008;22:75-91.
  • 38. Terpos E, Mougiou A, Kouraklis A, Chatzivassili A, Michalis E, Giannakoulas N, Manioudaki E, Lazaridou A, Bakaloudi V, Protopappa M, Liapi D, Grouzi E, Parharidou A, Symeonidis A, Kokkini G, Laoutaris NP, Vaipoulos G, Anagnostopoulos NI, Christakis JI, Meletis J, Bourantas KL, Zoumbos NC, Yataganas X, Viniou NA; Greek MDS Study Group. Prolonged administration of erythropoietin increases erythroid response rate in myelodysplastic syndromes: a phase II trial in 281 patients. Br J Haematol 2002;118:174- 180.
  • 39. Hellström-Lindberg E, Ahlgren T, Beguin Y, Carlsson M, Carneskog J, Dahl IM, Dybedal I, Grimfors G, Kanter-Lewensohn L, Linder O, Luthman M, Löfvenberg E, Nilsson-Ehle H, Samuelsson J, Tangen JM, Winqvist I, Oberg G, Osterborg A, Ost A. Treatment of anemia in myelodysplastic syndromes with granulocyte colony-stimulating factor plus erythropoietin: results from a randomized phase II study and long-term follow-up of 71 patients. Blood 1998;92:68-75.
  • 40. Buckstein R, Balleari E, Wells R, Santini V, Sanna A, Salvetti C, Crisà E, Allione B, Danise P, Finelli C, Clavio M, Poloni A, Salvi F, Cilloni D, Oliva EN, Musto P, Houston B, Zhu N, Geddes M, Leitch H, Leber B, Sabloff M, Nevill TJ, Yee KW, Storring JM, Francis J, Maurillo L, Latagliata R, Spiriti MAA, Andriani A, Piccioni AL, Fianchi L, Fenu S, Gumenyuk S, Buccisano F. ITACA: A new validated international erythropoietic stimulating agent-response score that further refines the predictive power of previous scoring systems. Am J Hematol 2017;92:1037-1046.
  • 41. Houston BL, Jayakar J, Wells RA, Lenis M, Zhang L, Zhu N, Leitch HA, Nevill TJ, Yee KWL, Leber B, Sabloff M, St-Hilaire E, Kumar R, Geddes M, Shamy A, Storring JM, Keating MM, Elemary M, Delage R, Mamedov A, Buckstein R. A predictive model of response to erythropoietin stimulating agents in myelodysplastic syndrome: from the Canadian MDS patient registry. Ann Hematol 2017;96:2025-2029.
  • 42. Platzbecker U, Fenaux P, Adès L, Giagounidis A, Santini V, van de Loosdrecht AA, Bowen D, de Witte T, Garcia-Manero G, Hellström-Lindberg E, Germing U, Stauder R, Malcovati L, Sekeres MA, Steensma DP, Gloaguen S. Proposals for revised IWG 2018 hematological response criteria in patients with MDS included in clinical trials. Blood 2019;133:1020-1030.
  • 43. Trincavelli ML, Da Pozzo E, Ciampi O, Cuboni S, Daniele S, Abbracchio MP, Martini C. Regulation of erythropoietin receptor activity in endothelial cells by different erythropoietin (EPO) derivatives: an in vitro study. Int J Mol Sci 2013;14:2258-2281.
  • 44. Choi MJ, Yee J. Erythropoiesis-stimulating agents and cancer: myth or truth. Adv Chronic Kidney Dis 2019;26:221-224.
  • 45. Hedley BD, Allan AL, Xenocostas A. The role of erythropoietin and erythropoiesis-stimulating agents in tumor progression. Clin Cancer Res 2011;17:6373-6380.
APA ASLANER AK M, gedük a, Açar İ, Polat M, Sunu C, bolaman a, Hacibekiroglu T, Guvenc B, ERTOP S (2023). Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. , 92 - 100. 10.4274/tjh.galenos.2023.2022.0437
Chicago ASLANER AK Müzeyyen,gedük ayfer,Açar İbrahim halil,Polat Merve Gökçen,Sunu Cenk,bolaman ali zahit,Hacibekiroglu Tuba,Guvenc Birol,ERTOP SEHMUS Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. (2023): 92 - 100. 10.4274/tjh.galenos.2023.2022.0437
MLA ASLANER AK Müzeyyen,gedük ayfer,Açar İbrahim halil,Polat Merve Gökçen,Sunu Cenk,bolaman ali zahit,Hacibekiroglu Tuba,Guvenc Birol,ERTOP SEHMUS Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. , 2023, ss.92 - 100. 10.4274/tjh.galenos.2023.2022.0437
AMA ASLANER AK M,gedük a,Açar İ,Polat M,Sunu C,bolaman a,Hacibekiroglu T,Guvenc B,ERTOP S Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. . 2023; 92 - 100. 10.4274/tjh.galenos.2023.2022.0437
Vancouver ASLANER AK M,gedük a,Açar İ,Polat M,Sunu C,bolaman a,Hacibekiroglu T,Guvenc B,ERTOP S Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. . 2023; 92 - 100. 10.4274/tjh.galenos.2023.2022.0437
IEEE ASLANER AK M,gedük a,Açar İ,Polat M,Sunu C,bolaman a,Hacibekiroglu T,Guvenc B,ERTOP S "Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data." , ss.92 - 100, 2023. 10.4274/tjh.galenos.2023.2022.0437
ISNAD ASLANER AK, Müzeyyen vd. "Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data". (2023), 92-100. https://doi.org/10.4274/tjh.galenos.2023.2022.0437
APA ASLANER AK M, gedük a, Açar İ, Polat M, Sunu C, bolaman a, Hacibekiroglu T, Guvenc B, ERTOP S (2023). Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. Turkish Journal of Hematology, 40(2), 92 - 100. 10.4274/tjh.galenos.2023.2022.0437
Chicago ASLANER AK Müzeyyen,gedük ayfer,Açar İbrahim halil,Polat Merve Gökçen,Sunu Cenk,bolaman ali zahit,Hacibekiroglu Tuba,Guvenc Birol,ERTOP SEHMUS Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. Turkish Journal of Hematology 40, no.2 (2023): 92 - 100. 10.4274/tjh.galenos.2023.2022.0437
MLA ASLANER AK Müzeyyen,gedük ayfer,Açar İbrahim halil,Polat Merve Gökçen,Sunu Cenk,bolaman ali zahit,Hacibekiroglu Tuba,Guvenc Birol,ERTOP SEHMUS Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. Turkish Journal of Hematology, vol.40, no.2, 2023, ss.92 - 100. 10.4274/tjh.galenos.2023.2022.0437
AMA ASLANER AK M,gedük a,Açar İ,Polat M,Sunu C,bolaman a,Hacibekiroglu T,Guvenc B,ERTOP S Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. Turkish Journal of Hematology. 2023; 40(2): 92 - 100. 10.4274/tjh.galenos.2023.2022.0437
Vancouver ASLANER AK M,gedük a,Açar İ,Polat M,Sunu C,bolaman a,Hacibekiroglu T,Guvenc B,ERTOP S Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data. Turkish Journal of Hematology. 2023; 40(2): 92 - 100. 10.4274/tjh.galenos.2023.2022.0437
IEEE ASLANER AK M,gedük a,Açar İ,Polat M,Sunu C,bolaman a,Hacibekiroglu T,Guvenc B,ERTOP S "Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data." Turkish Journal of Hematology, 40, ss.92 - 100, 2023. 10.4274/tjh.galenos.2023.2022.0437
ISNAD ASLANER AK, Müzeyyen vd. "Long-Term Efficacy of Erythropoiesis-Stimulating Agents in Patients with Low-Risk or Intermediate-1-Risk Myelodysplastic Syndrome: Multicenter Real-Life Data". Turkish Journal of Hematology 40/2 (2023), 92-100. https://doi.org/10.4274/tjh.galenos.2023.2022.0437