Cardiovascular Toxicity of Tyrosine Kinase Inhibitors in Patients with Chronic Myeloid Leukemia

I.L. Davydkin, Kseniya Viktorovna Naumova, A.M. Osadchuk, I.A. Zolotovskaya, O.E. Danilova, T.Yu. Stepanova, O.V. Tereshina, L.V. Limareva, A.S. Shpigel’, T.P. Kuz’mina,

DOI:

https://doi.org/10.21320/2500-2139-2018-11-4-378-387

In the present review the cardiovascular complications in patients with chronic myeloid leukemia (CML) receiving tyrosine kinase inhibitors (TKI) are discussed. It covers current views on pathogenesis of TKI cardiovascular toxicity. The pathophysiology of cardiovascular diseases (CVD) is considered as a part of the so-called pathophysiological continuum, i.e. a complex of processes developing at the molecular and cellular levels before clinical symptoms of the above diseases occur. Cardiovascular toxicity of certain TKIs can contribute to progression of pathophysiological processes in CML patients. The study of mechanisms underlying cardiovascular complications of TKI-based therapy is essential for evaluating the risks of their development in each patient. Identification of CVD predictors during TKI-based therapy can allow to elaborate a scheme for cardiovascular monitoring and safe patient management under consideration of individual risks and to avoid severe life-threatening complications.

  • I.L. Davydkin Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099; SamGMU Research Institute of Hematology, Transfusiology and Intensive Care, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099; НИИ гематологии, трансфузиологии и интенсивной терапии СамГМУ, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • Kseniya Viktorovna Naumova Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • A.M. Osadchuk Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • I.A. Zolotovskaya Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • O.E. Danilova Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • T.Yu. Stepanova Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • O.V. Tereshina Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • L.V. Limareva SamGMU Institute of Experimental Medicine and Biotechnology, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; Институт экспериментальной медицины и биотехнологий СамГМУ, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • A.S. Shpigel’ Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  • T.P. Kuz’mina Samara State Medical University, 89 Chapaevskaya str., Samara, Russian Federation, 443099 ; ФГБОУ ВО «Самарский государственный медицинский университет» Минздрава России, ул. Чапаевская, д. 89, Самара, Российская Федерация, 443099
  1. Elliott P. Pathogenesis of cardiotoxicity induced by anthracyclines. Sem Oncol. 2006;33:2–7. doi: 10.1053/j.seminoncol.2006.04.020. DOI: https://doi.org/10.1053/j.seminoncol.2006.04.020
  2. Tokarska-Schlattner M, Zaugg M, Zuppinger C, et al. New insights into doxorubicin-induced cardiotoxicity: the critical role of cellular energetics. J Mol Cell Cardiol. 2006;41(3):389–405. doi: 10.1016/j.yjmcc.2006.06.009. DOI: https://doi.org/10.1016/j.yjmcc.2006.06.009
  3. Mellor HR, Bell AR, Valentin JP, Roberts RRA. Cardiotoxicity associated with targeting kinase pathways in cancer. Toxicol Sci. 2011;120(1):14–32. doi: 10.1093/toxsci/kfq378. DOI: https://doi.org/10.1093/toxsci/kfq378
  4. Orphanos GS, Ioannidis GN, Ardavanis AG. Cardiotoxicity induced by tyrosine kinase inhibitors. Acta 2009;48(7):964–70. doi: 10.1080/02841860903229124. DOI: https://doi.org/10.1080/02841860903229124
  5. Baccarani M, Deininger MW, Rosti G, et European LeukemiaNet recommendations for the management of chronic myeloid leukemia: 2013. Blood. 2013;122(6):872–84. doi: 10.1182/blood-2013-05-501569. DOI: https://doi.org/10.1182/blood-2013-05-501569
  6. Moslehi JJ, Deininger M. Tyrosine kinase inhibitor-associated cardiovascular toxicity in chronic myeloid leukemia. J Clin Oncol. 2015;33(35):4210–8. doi: 10.1200/jco.2015.62.4718. DOI: https://doi.org/10.1200/JCO.2015.62.4718
  7. Anhel N, Delgado DH, Lipton JH. Cardiovascular toxicities of BCR-ABL tyrosine kinase inhibitors in chronic myeloid leukemia: preventive strategies and cardiovascular surveillance. Vasc Health Risk Manage. 2017;13:293–303. doi: 10.2147/vhrm.s108874. DOI: https://doi.org/10.2147/VHRM.S108874
  8. Rix U, Hantschel O, Durnberger G, et al. Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets. Blood. 2007;110(12):4055–63. doi: 10.1182/blood-2007-07-102061. DOI: https://doi.org/10.1182/blood-2007-07-102061
  9. Туркина А.Г., Челышева Е.Ю. Стратегия терапии хронического миелолейкоза: возможности и перспективы. Терапевтический архив. 2013;85(7):4–9.
  10. [Turkina AG, Chelysheva EYu. Therapeutic strategy for chronic myeloid leukemia: possibilities and prospects. Terapevticheskii arkhiv. 2013;85(7):4–9. (In Russ)]
  11. Laneuville P. When to Stop Tyrosine Kinase Inhibitors for the Treatment of Chronic Myeloid Leukemia. Curr Treat Opt 2018;19(3):15. doi: 10.1007/s11864-018-0532-2. DOI: https://doi.org/10.1007/s11864-018-0532-2
  12. Hughes TP, Ross DM. Moving treatment-free remission into mainstream clinical practice in CML. Blood. 2016;128(1):17–23. doi: 10.1182/blood-2016-01-694265. DOI: https://doi.org/10.1182/blood-2016-01-694265
  13. Etienne G, Guilhot J, Rea D, et al. Long-Term Follow-Up of the French Stop Imatinib (STIM1) Study in Patients With Chronic Myeloid Leukemia. J Clin Oncol. 2017;35(3):298–305. doi: 10.1200/JCO.2016.68.2914. DOI: https://doi.org/10.1200/JCO.2016.68.2914
  14. Rea D, Nicolini FE, Tulliez M, et al. Discontinuation of dasatinib or nilotinib in chronic myeloid leukemia: interim analysis of the STOP 2G-TKI study. Blood. 2016;129(7):846–54. doi: 10.1182/blood-2016-09-742205. DOI: https://doi.org/10.1182/blood-2016-09-742205
  15. Hehlmann R. Research in the heart of hematology: chronic myeloid leukemia 2017. Haematologica. 2017;102(3):418–21. doi: 10.3324/haematol.2016.159848. DOI: https://doi.org/10.3324/haematol.2016.159848
  16. Куликов С.М., Виноградова О.Ю., Челышева Е.Ю. и др. Заболеваемость хроническим миелолейкозом в 6регионах России по данным популяционного исследования 2009–2012 гг. Терапевтический архив. 2014;86(7):24–30.
  17. [Kulikov SM, Vinogradova OYu, Chelysheva EYu, et al. Incidence of chronic myeloid leukemia in 6 regions of Russia according to the data of the 2009–2012 population-based study. Terapevticheskii arkhiv. 2014;86(7):24–30. (In Russ)]
  18. Рабочая группа по онкологическим заболеваниям и сердечно-сосудистой токсичности Европейского общества кардиологов (ЕОК). Меморандум ESC по лечению онкологических заболеваний и сердечно-сосудистой токсичности, разработанный под эгидой комитета по практике ESC Российский кардиологический журнал. 2017;3(143):105–39. doi: 10.15829/1560-4071-2017-3-105-139. DOI: https://doi.org/10.15829/1560-4071-2017-3-105-139
  19. [The Task Force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). 2016 ESC position paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC committee for practice guidelines. Russian Journal of Cardiology. 2017;3(143):105–39. doi: 10.15829/1560-4071-2017-3-105-139. (In Russ)] DOI: https://doi.org/10.15829/1560-4071-2017-3-105-139
  20. Steegmann JL, Baccarani M, Breccia M, et al. European LeukemiaNet recommendations for the management and avoidance of adverse events of treatment in chronic myeloid leukaemia. Leukemia. 2016;30(8):1648–71. doi: 10.1038/leu.2016.104. DOI: https://doi.org/10.1038/leu.2016.104
  21. Kerkela R, Grazette L, Yacobi R, et al. Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med. 2006;12(8):908–16. doi: 10.1038/nm1446. DOI: https://doi.org/10.1038/nm1446
  22. Hochhaus A, Larson RA, Guilhot F, et al. Long-term outcomes of imatinib treatment for chronic myeloid leukemia. N Engl J Med. 2017;376(10):917–27. doi: 10.1056/nejmoa1609324. DOI: https://doi.org/10.1056/NEJMoa1609324
  23. Gambacorti-Passerini С, Cortes JE, Lipton JH, et al. Safety of bosutinib versus imatinib in the phase 3 BELA trial in newly diagnosed chronic phase chronic myeloid leukemia. Am J Hematol. 2014;89(10):947–53. doi: 1002/ajh.23788. DOI: https://doi.org/10.1002/ajh.23788
  24. Cortes JE, Gambacorti-Passerini C, Deininger MW, et al. Bosutinib Versus Imatinib for Newly Diagnosed Chronic Myeloid Leukemia: Results From the Randomized BFORE Trial. J Clin Oncol. 2018;36(3):231–9. doi: 10.1200/jco.2017.74.7162. DOI: https://doi.org/10.1200/JCO.2017.74.7162
  25. Cortes JE, Khoury HJ, Kantarjian H, et al. Long-term evaluation of cardiac and vascular toxicity in patients with Philadelphia chromosome-positive leukemias treated with bosutinib. Am J Hematol. 2016;91(6): 606–16. doi: 10.1002/ajh.24360. DOI: https://doi.org/10.1002/ajh.24360
  26. Montani D, Bergot E, Gunther S, et al. Pulmonary arterial hypertension in patients treated by dasatinib. Circulation. 2012;125(17):2128–37. doi: 10.1161/circulationaha.111.079921. DOI: https://doi.org/10.1161/CIRCULATIONAHA.111.079921
  27. Cortes JE, Saglio G, Kantarjian HM, et al. Final 5-year study results of DASISION: the dasatinib versus imatinib study in treatment-naive chronic myeloid leukemia patients trial. J Clin Oncol. 2016;34(20):2333–40. doi: 10.1200/jco.2015.64.8899. DOI: https://doi.org/10.1200/JCO.2015.64.8899
  28. Shah NP, Rousselot P, Schiffer C, et al. Dasatinib in imatinib-resistant or -intolerant chronic-phase, chronic myeloid leukemia patients: 7-year follow-up of study CA180-034. Am J Hematol. 2016;91(9):869–74. doi: 10.1002/ajh.24423. DOI: https://doi.org/10.1002/ajh.24423
  29. Jeon Y-W, Lee S-E, Kim S-H, et al. Six-Year Follow-Up Of Dasatinib-Related Pulmonary Arterial Hypertension (PAH) For Chronic Myeloid Leukemia In Single Center. Blood. 2013;122(21):4017. DOI: https://doi.org/10.1182/blood.V122.21.4017.4017
  30. Kong JH, Jeon Y-W, Lee S-E, et al. Long-Term Assessment of Dasatinib-Induced Pulmonary Arterial Hypertension in Chronic Myeloid Leukemia. Blood. 2014;124(21):5535. DOI: https://doi.org/10.1182/blood.V124.21.5535.5535
  31. Рабочая группа по диагностике и лечению легочной гипертензии Европейского общества кардиологов (ESC) и Европейского общества пульмонологов (ERS). Рекомендации ESC/ERS по диагностике и лечению легочной гипертензии 2015. Российский кардиологический журнал. 2016;5(133):5–64. doi: 10.15829/1560-4071-2016-5-5-64. DOI: https://doi.org/10.15829/1560-4071-2016-5-5-64
  32. [The Joint Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS). 2015 ESC/ERS guidelines for the diagnosis and treatment of pulmonary hypertension. Russian Journal of Cardiology. 2016;5(133):5–64. doi: 10.15829/1560-4071-2016-5-5-64. (In Russ)] DOI: https://doi.org/10.15829/1560-4071-2016-5-5-64
  33. Aichberger KJ, Herndlhofer S, Schernthaner G-H, et al. Progressive peripheral arterial occlusive disease and other vascular events during nilotinib therapy in CML. Am J Hematol. 2011;86(7):533–9. doi: 10.1002/ajh.22037. DOI: https://doi.org/10.1002/ajh.22037
  34. Le Coutre P, Rea D, Abruzzese E, et al. Severe peripheral arterial disease during nilotinib therapy. J Nat Cancer Inst. 2011;103(17):1347–8. doi: 10.1093/jnci/djr292. DOI: https://doi.org/10.1093/jnci/djr292
  35. Hochhaus A, Saglio G, Hughes TP, 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(5):1044–54. doi: 10.1038/leu.2016.5. DOI: https://doi.org/10.1038/leu.2016.5
  36. Cortes JE, Kantarjian H, Shah NP, et al. Ponatinib in refractory Philadelphia chromosome-positive leukemias. N Engl J Med. 2012;367(22):2075–88. doi: 10.1056/nejmoa1205127. DOI: https://doi.org/10.1056/NEJMoa1205127
  37. Cortes JE, Kim D-W, Pinilla-Ibarz J. Ponatinib efficacy and safety in Philadelphia chromosome–positive leukemia: Final 5-year results of the phase 2 PACE trial. Blood. 2018:blood-2016-09-739086. doi: 10.1182/blood-2016-09-739086. DOI: https://doi.org/10.1182/blood-2016-09-739086
  38. Lipton JH, Chuah C, Guerci-Bresler A, et al. Ponatinib versus imatinib for newly diagnosed chronic myeloid leukaemia: an international, randomised, open-label, phase 3 trial. Lancet Oncol. 2016;17(5):612–21. doi: 10.1016/s1470-2045(16)00080-2. DOI: https://doi.org/10.1016/S1470-2045(16)00080-2
  39. Иклусиг® (инструкция по медицинскому применению). Австралия: Ariad Pharmaceuticals. Доступно по: http://lechimvizraile.ru/articles/iklusig_instruktsiya_po_primeneniyu/ Ссылка активна на 7.06.2018.
  40. [Iclusig® (package insert). Australia: Ariad Pharmaceuticals. Available from: http://lechimvizraile.ru/articles/iklusig_instruktsiya_po_primeneniyu/ (accessed 7.06.2018) (In Russ)]
  41. Dorer DJ, Knickerbocker RK, Baccarani M, et al. Impact of dose intensity of ponatinib on selected adverse events: multivariate analyses from a pooled population of clinical trial patients. Leuk Res. 2016;48:84–91. doi: 10.1016/j.leukres.2016.07.007. DOI: https://doi.org/10.1016/j.leukres.2016.07.007
  42. Dahlen T, Edgren G, Lambe M, et al. Cardiovascular events associated with use of tyrosine kinase inhibitors in chronic myeloid leukemia: a population-based cohort study. Ann Int Med. 2016;165(3):161–6. doi: 10.7326/m15-2306. DOI: https://doi.org/10.7326/M15-2306
  43. Ross DM, Arthur C, Burbury K, et al. Chronic myeloid leukaemia and tyrosine kinase inhibitor therapy: assessment and management of cardiovascular risk factors. Int Med J. 2018;48(Suppl 2):5–13. doi: 10.1111/imj.13716. DOI: https://doi.org/10.1111/imj.13716
  44. Douxfils J, Haguet H, Mullier F, et al. Association Between BCR-ABL Tyrosine Kinase Inhibitors for Chronic Myeloid Leukemia and Cardiovascular Events, Major Molecular Response, and Overall Survival A Systematic Review and Meta-analysis. JAMA Oncol. 2016;2(5):625–32. doi: 10.1001/jamaoncol.2015.5932. DOI: https://doi.org/10.1001/jamaoncol.2015.5932
  45. Haguet H, Douxfils J, Mullier F, et al. Risk of arterial and venous occlusive events in chronic myeloid leukemia patients treated with new generation BCR-ABL tyrosine kinase inhibitors: a systematic review and meta-analysis. Exp Opin Drug Safety. 2017;16(1):5–12. doi: 10.1080/14740338.2017.1261824. DOI: https://doi.org/10.1080/14740338.2017.1261824
  46. Zhang J, Yang PL, Gray NS. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer. 2009;9(1):28–39. doi: 10.1038/nrc2559. DOI: https://doi.org/10.1038/nrc2559
  47. Gschwind A, Fischer OM, Ullrich A. The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat Rev Cancer. 2004;4(5):361–70. doi: 10.1038/nrc1360. DOI: https://doi.org/10.1038/nrc1360
  48. Zuppinger C, Suter TM. Cancer therapy-associated cardiotoxicity and signaling in the myocardium. J Cardiovasc Pharmacol. 2010;56(2):141–6. doi: 10.1097/fjc.0b013e3181e0f89a. DOI: https://doi.org/10.1097/FJC.0b013e3181e0f89a
  49. Зейфман А.А., Челышева Е.Ю., Туркина А.Г., Чилов Г.Г. Роль селективности ингибиторов тирозинкиназ в развитии побочных эффектов при терапии хронического миелолейкоза. Клиническая онкогематология. 2014;7(1):16–27. DOI: https://doi.org/10.21320/2500-2139-2014-7-1-16-27
  50. [Zeyfman AA, Chelysheva YeYu, Turkina AG, Chilov GG. Role of tyrosine-kinase inhibitor selectivity in development of adverse effects during treatment of chronic myeloid leukemia. Klinicheskaya onkogematologiya. 2014;7(1):16–27 (In Russ)]
  51. Bellinger AM, Arteaga CL, Force T, et al. Cardio-oncology. 2015;132(23):2248–58. doi: 10.1161/circulationaha.115.010484. DOI: https://doi.org/10.1161/CIRCULATIONAHA.115.010484
  52. Han MS, Chung KW, Cheon HG, et al. Imatinib mesylate reduces endoplasmic reticulum stress and induces remission of diabetes in db/db mice. 2009;58(2):329–36. doi: 10.2337/db08-0080. DOI: https://doi.org/10.2337/db08-0080
  53. Iurlo A, Orsi E, Cattaneo D, et al. Effects of first- and second-generation tyrosine kinase inhibitor therapy on glucose and lipid metabolism in chronic myeloid leukemia patients: a real clinical problem? Oncotarget. 2015;6(32):33944–51. doi: 10.18632/oncotarget.5580. DOI: https://doi.org/10.18632/oncotarget.5580
  54. Alhawiti N, Burbury KL, Kwa FA, et al. The tyrosine kinase inhibitor, nilotinib potentiates a prothrombotic state. Thromb Res. 2016;145:54–64. doi: 10.1016/j.thromres.2016.07.019. DOI: https://doi.org/10.1016/j.thromres.2016.07.019
  55. Albrecht-Schgoer K, Huber K, Grebien F, et al. Nilotinib exerts direct proatherogenic and anti-angiogenic effects on vascular endothelial cells: a potential explanation for drug-induced vasculopathy in CML. Blood. 2013;122(21):257. DOI: https://doi.org/10.1182/blood.V122.21.257.257
  56. Bair SM, Choueiri TK, Moslehi J. Cardiovascular complications associated with novel angiogenesis inhibitors: emerging evidence and evolving perspectives. Trends Cardiovasc Med. 2013;23(4):104–13. doi: 1016/j.tcm.2012.09.008. DOI: https://doi.org/10.1016/j.tcm.2012.09.008
  57. Садыкова Д.И. Современные подходы к диагностике и лечению легочной гипертензии. Практическая медицина. 2012;7(62):21–6.
  58. [Sadykova DI. Modern approaches to diagnostic and treatment of pulmonary hypertension. Prakticheskaya meditsina. 2012;7(62):21–6. (In Russ)]
  59. Godinas L, Guingabert C, Seferian A, et al. Tyrosine kinase inhibitors in pulmonary arterial hypertension: a double-edge sword? Semin Respir Crit Care Med. 2013;34(5):714–24. doi: 10.1055/s-0033-1356494. DOI: https://doi.org/10.1055/s-0033-1356494
  60. Morello F, Perino A, Hirsch E. Phosphoinositide 3-kinase signaling in the vascular system. Cardiovasc Res. 2009;82(2):261–71. doi: 10.1093/cvr/cvn325. DOI: https://doi.org/10.1093/cvr/cvn325
  61. Yang JC, Haworth L, Sherry RM, et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003;349(5):427–34. doi: 10.1056/nejmoa021491. DOI: https://doi.org/10.1056/NEJMoa021491
  62. Verheul HM, Pinedo HM. Possible molecular mechanisms involved in the toxicity of angiogenesis inhibition. Nat Rev Cancer. 2007;7(6):475–85. doi: 10.1038/nrc2152. DOI: https://doi.org/10.1038/nrc2152
  63. Dhaun N, Goddard J, Webb DJ. The endothelin system and its antagonism in chronic kidney disease. J Am Soc Nephrol. 2006;17(4):943–55. doi: 10.1681/asn.2005121256. DOI: https://doi.org/10.1681/ASN.2005121256
  64. Amiri F, Virdis A, Neves MF, et al. Endothelium-restricted overexpression of human endothelin-1 causes vascular remodeling and endothelial dysfunction. Circulation. 2004;110(15):2233–40. doi: 10.1161/01.cir.0000144462.08345.b9. DOI: https://doi.org/10.1161/01.CIR.0000144462.08345.B9
  65. Lankhorst S, Baelde HJ, Kappers MH, et al. Greater sensitivity of blood pressure than renal toxicity to tyrosine kinase receptor inhibition with sunitinib. Hypertension. 2015;66(3):543–9. doi: 10.1161/hypertensionaha.115.05435. DOI: https://doi.org/10.1161/HYPERTENSIONAHA.115.05435
  66. Kostos L, Burbury K, Srivastava G, Prince HM. Gastrointestinal bleeding in a chronic myeloid leukaemia patient precipitated by dasatinib-induced platelet dysfunction: case report. Platelets. 2015;26(8):809–11. doi: 10.3109/09537104.2015.1049138. DOI: https://doi.org/10.3109/09537104.2015.1049138
  67. Quintas-Cardama A, Kantarjian H, Ravandi F, et al. Bleeding diasthesis in patients with chronic myelogenous leukaemia receiving dasatinib therapy. Cancer. 2009;115(11):2482–90. doi: 10.1002/cncr.24257. DOI: https://doi.org/10.1002/cncr.24257
  68. Quintas-Cardama A, Kantarjian H, O’Brien S, et al. Pleural effusion in patients with chronic myelogenous leukemia treated with dasatinib after imatinib failure. J Clin Oncol. 2007;25(25):3908–14. doi: 10.1200/jco.2007.12.0329. DOI: https://doi.org/10.1200/JCO.2007.12.0329
  69. Poredos P, Jug B. The prevalence of peripheral arterial disease in high risk subject sand coronary or cerebrovascular patients. Angiology. 2007;58(3):309–15. doi: 10.1177/0003319707302494. DOI: https://doi.org/10.1177/0003319707302494
  70. Steg Ph, Bhatt DL, Wilson PWF, et al. One-year cardiovascular event rates in outpatients with atherothrombosis. JAMA. 2007;297(11):1197. doi: 10.1001/jama.297.11.1197. DOI: https://doi.org/10.1001/jama.297.11.1197
  71. Giles FJ, le Coutre PD, Pinilla-Ibarz J, et al. Nilotinib in imatinib-resistant or imatinib-intolerant patients with chronic myeloid leukemia in chronic phase: 48-month follow-up results of a phase II study. Leukemia. 2013;27(1):107–12. doi: 10.1038/leu.2012.181. DOI: https://doi.org/10.1038/leu.2012.181
  72. Agostino NM, Chinchilli VM, Lynch CJ, et al. Effect of the tyrosine kinase inhibitors (sunitinib, sorafenib, dasatinib, and imatinib) on blood glucose levels in diabetic and nondiabeticpatients in general clinical practice. J Oncol Pharm Pract. 2010;17(3):197–202. doi: 10.1177/1078155210378913. DOI: https://doi.org/10.1177/1078155210378913
  73. Lassila M, Allen TJ, Cao Z, et al. Imatinib attenuates diabetes-associated atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24(5):935–42. doi: 10.1161/01.atv.0000124105.39900.db. DOI: https://doi.org/10.1161/01.ATV.0000124105.39900.db
  74. Hoffmann VS, Baccarani M, Hasford J, et al. The EUTOS population based registry: incidence and clinical characteristics of 2904 CML patients in 20 European Countries. 2015;29(6):1336–43. doi: 10.1038/leu.2015.73. DOI: https://doi.org/10.1038/leu.2015.73
  75. Dzau VJ, Antman EM, Black HR, et al. The cardiovascular disease continuum: validated clinical evidence of improved patient outcomes. Part I: pathophysiology and clinical trial evidence risk factors through stable coronary artery disease. Circulation. 2006;114(25):2850–70. doi: 10.1161/circulationaha.106.655688. DOI: https://doi.org/10.1161/CIRCULATIONAHA.106.655688
  76. Daher IN, Daigle TR, Bhatia N, Durand J-B. The Prevention of Cardiovascular Disease In Cancer Survivors. Tex Heart Inst J. 2012;39(2):190–8.
  77. Brown S-A, Nhola L, Herrmann J. Cardiovascular toxicities of small molecule tyrosine kinase inhibitors: an opportunity for systems-based approaches. Clin Pharmacol Ther. 2016;101(1):65–80. doi: 10.1002/cpt.552. DOI: https://doi.org/10.1002/cpt.552
  78. Kim TD, Rea D, Schwarz M, et al. Peripheral artery occlusive disease in chronic phase chronic myeloid leukemia patients treated with nilotinib or imatinib. 2013;27(6):1316–21. doi: 10.1038/leu.2013.70. DOI: https://doi.org/10.1038/leu.2013.70
  79. Cortes JE, Kim D-W, Pinilla-Ibarz J, et al. A phase 2 trial of ponatinib in Philadelphia chromosome-positive leukemias. N Engl J Med. 2013;369(19):1783–96. doi: 10.1056/nejmoa1306494. DOI: https://doi.org/10.1056/NEJMoa1306494
  80. Гусарова Г.А., Туркина А.Г. Артериальные события у больных хроническим миелолейкозом, получающих терапию ингибиторами тирозинкиназ 2-го поколения. Клиническая онкогематология. 2016;9(4):474–84. doi: 10.21320/2500-2139-2016-9-4-474-484. DOI: https://doi.org/10.21320/2500-2139-2016-9-4-474-484
  81. [Gusarova GA, Turkina AG. Arterial Events in Patients with Chronic Myeloid Leukemia Receiving Treatment with Second Generation Tyrosine Kinase Inhibitors. Clinical oncohematology. 2016;9(4):474–84. doi: 10.21320/2500-2139-2016-9-4-474-484. (In Russ)] DOI: https://doi.org/10.21320/2500-2139-2016-9-4-474-484
  82. Li W, Croce K, Steensma DP, et al. Vascular and metabolic implications of novel targeted cancer therapies. J Am Coll Cardiol. 2015;66(10):1160–78. doi: 10.1016/j.jacc.2015.07.025. DOI: https://doi.org/10.1016/j.jacc.2015.07.025
  83. Conroy RM, Pyorala K, Fitzgerald AP, et al. Estimation of ten-year risk of fatal cardiovascular disease in Europe: the SCORE project. Eur Heart J. 2003;24(11):987–1003. doi: 10.1016/s0195-668x(03)00114-3. DOI: https://doi.org/10.1016/S0195-668X(03)00114-3
  84. Gerhard-Herman MD, Gornik HL, Barrett C, et al. 2016 AHA/ACC guideline on the management of patients with lower extremity peripheral artery disease: a report of the American College of Cardiology/American Heart Association Task Force on clinical practice guidelines. J Am Coll Cardiol. 2017;69(11):e71–e126. doi: 10.1016/j.jacc.2016.11.007. DOI: https://doi.org/10.1016/j.jacc.2016.11.007
  85. Овсянникова Е.Г., Попов Е.А., Давыдкин И.Л. и др. Современные аспекты диагностики, прогнозирования и лечения хронического миелолейкоза. Астраханский медицинский журнал. 2015;10(3):27–44.
  86. [Ovsyannikova EG, Popov EA, Davydkin IL, et al. Modern aspects of diagnosis, prognosis and treatment of chronic myeloid leukemia. Astrakhanskii meditsinskii zhurnal. 2015;10(3):27–44. (In Russ)]
  87. Jessup M, Abraham WT, Casey DE, et al. 2009 ACCF/AHA Guidelines for the Diagnosis and Management of heart failure in adults: a report of the American College of cardiology foundation/American heart association task force on practice guidelines: developed in collaboration with the International Society for heart and lung transplantation. Circulation. 2009;119(14):1977–2016. doi: 10.1161/circulationaha.109.192064. DOI: https://doi.org/10.1161/CIRCULATIONAHA.109.192064
  88. Granados-Principal S, Quiles JL, Ramirez-Tortosa CL, et al. New advances in molecular mechanisms and the prevention of adriamycin toxicity by antioxidant nutrients. Food Chem Toxicol. 2010;48(6):1425–38. doi: 10.1016/j.fct.2010.04.007. DOI: https://doi.org/10.1016/j.fct.2010.04.007
  89. Wouters KA, Kremer LC, Miller TL, et al. Protecting against anthracycline-induced myocardial damage: a review of the most promising strategies. Br J Haematol. 2005;131(5):561–78. doi: 10.1111/j.1365-2141.2005.05759.x. DOI: https://doi.org/10.1111/j.1365-2141.2005.05759.x
  90. Mohamed HE, El-Swefy SE, Hagar HH. The protective effect of glutathione administration on Adriamycin-induced acute cardiac toxicity in rats. Pharmacol Res. 2000;42(2):115–21. doi: 10.1006/phrs.1999.0630. DOI: https://doi.org/10.1006/phrs.1999.0630
  91. van Leeuwen RWF, van Gelder T, Mathijssen RHJ, Jansman FGA. Drug–drug interactions with tyrosine-kinase inhibitors: a clinical perspective. Lancet Oncol. 2014;15(8):e315–e26. doi: 10.1016/s1470-2045(13)70579-5. DOI: https://doi.org/10.1016/S1470-2045(13)70579-5
  92. Haouala A, Widmer N, Duchosal MA, et al. Drug interactions with the tyrosine kinase inhibitors imatinib, dasatinib, and nilotinib. Blood. 2011;117(8):e75–e87. doi: 10.1182/blood-2010-07-294330. DOI: https://doi.org/10.1182/blood-2010-07-294330
  93. Туркина А.Г., Зарицкий А.Ю., Шуваев В.А. и др. Клинические рекомендации по диагностике и лечению хронического миелолейкоза. Клиническая онкогематология. 2017;10(3):294–316. doi: 10.21320/2500-2139-2017-10-3-294-316. DOI: https://doi.org/10.21320/2500-2139-2017-10-3-294-316
  94. [Turkina AG, Zaritskii AYu, Shuvaev VA, et al. Clinical Recommendations for the Diagnosis and Treatment of Chronic Myeloid Leukemia. Clinical oncohematology. 2017;10(3):294–316. doi: 10.21320/2500-2139-2017-10-3-294-316. (In Russ)] DOI: https://doi.org/10.21320/2500-2139-2017-10-3-294-316
  95. Poch MM, Sibai H, Deotare U, Lipton JH. Ponatinib in the therapy of chronic myeloid leukemia. Exp Rev Hematol. 2016;9(10):923–32. doi: 10.1080/17474086.2016.1232163. DOI: https://doi.org/10.1080/17474086.2016.1232163
  96. Breccia M, Pregno P, Spallarossa P, et al. Identification, prevention and management of cardiovascular risk in chronic myeloid leukaemia patients candidate to ponatinib: an expert opinion. Ann Hematol. 2016;96(4):549–58. doi: 10.1007/s00277-016-2820-x. DOI: https://doi.org/10.1007/s00277-016-2820-x

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Published

01.10.2018

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COMPLICATIONS OF CHEMOTHERAPY

How to Cite

Davydkin I.L., Naumova K.V., Osadchuk A.M., et al. Cardiovascular Toxicity of Tyrosine Kinase Inhibitors in Patients with Chronic Myeloid Leukemia. Clinical Oncohematology. Basic Research and Clinical Practice. 2018;11(4):378–387. doi:10.21320/2500-2139-2018-11-4-378-387.

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