Cardiovascular mortality among chronic myeloid leukemia patients in the pre-tyrosine kinase inhibitor (TKI) and TKI eras: a surveillance, epidemiology and end results (SEER) analysis

References

• Kumar V, Garg M, Chaudhary N, et al. An observational study on risk of secondary cancers in chronic myeloid leukemia patients in the TKI era in the United States. PeerJ. 2018;6:e4342.
   PubMed Web of Science ®Google Scholar
• Saglio G, Le Coutre P, Cortes J, et al. Evaluation of cardiovascular ischemic event rates in dasatinib-treated patients using standardized incidence ratios. Ann Hematol. 2017;96(8):1303–1313.
   PubMed Web of Science ®Google Scholar
• Miranda MB, Lauseker M, Kraus MP, et al. Secondary malignancies in chronic myeloid leukemia patients after imatinib-based treatment: long-term observation in CML Study IV. Leukemia. 2016;30(6):1255–1262.
   PubMed Web of Science ®Google Scholar
• Sasaki K, Strom SS, O'Brien S, et al. Relative survival in patients with chronic-phase chronic myeloid leukaemia in the tyrosine-kinase inhibitor era: analysis of patient data from six prospective clinical trials. Lancet Haematol. 2015;2(5):e186–e193.
   PubMed Web of Science ®Google Scholar
• Hehlmann R, Heimpel H, Hasford J, et al. Randomized comparison of interferon-alpha with busulfan and hydroxyurea in chronic myelogenous leukemia. The German CML Study Group. Blood. 1994;84(12):4064–4077.
   PubMed Web of Science ®Google Scholar
• Gunnarsson N, Stenke L, Hoglund M, et al. Second malignancies following treatment of chronic myeloid leukaemia in the tyrosine kinase inhibitor era. Br J Haematol. 2015;169(5):683–688.
   PubMed Web of Science ®Google Scholar
• Hehlmann R, Heimpel H, Kolb HJ, et al. The German CML study, comparison of busulfan vs. hydroxyurea vs. interferon alpha and establishment of prognostic score 1. Leuk Lymphoma. 1993;11 (Suppl 1):159–168.
   PubMedGoogle Scholar
• Medeiros BC, Possick J, Fradley M. Cardiovascular, pulmonary, and metabolic toxicities complicating tyrosine kinase inhibitor therapy in chronic myeloid leukemia: strategies for monitoring, detecting, and managing. Blood Rev. 2018;32(4):289–299.
   PubMed Web of Science ®Google Scholar
• Lang K, McGarry LJ, Huang H, et al. Mortality and vascular events among elderly patients with chronic myeloid leukemia: a retrospective analysis of linked SEER-medicare data. Clin Lymphoma Myeloma Leuk. 2016;16(5):275.e1–285.e1.
   Web of Science ®Google Scholar
• Pophali PA, Patnaik MM. The role of new tyrosine kinase inhibitors in chronic myeloid leukemia. Cancer J. 2016;22(1):40–50.
   PubMed Web of Science ®Google Scholar
• Damrongwatanasuk R, Fradley MG. Cardiovascular complications of targeted therapies for chronic myeloid leukemia. Curr Treat Options Cardiovasc Med. 2017;19(4):24
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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):1044–1054.
   PubMed Web of Science ®Google Scholar
• 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 Intern Med. 2016;165:161–166.
   PubMed Web of Science ®Google Scholar
• Chai-Adisaksopha C, Lam W, Hillis C. Major arterial events in patients with chronic myeloid leukemia treated with tyrosine kinase inhibitors: a meta-analysis. Leuk Lymphoma. 2016;57(6):1300–1310.
   PubMed Web of Science ®Google Scholar
• Kloth JS, Pagani A, Verboom MC, et al. Incidence and relevance of QTc-interval prolongation caused by tyrosine kinase inhibitors. Br J Cancer. 2015;112(6):1011–1016.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Shah DR, Shah RR, Morganroth J. Tyrosine kinase inhibitors: their on-target toxicities as potential indicators of efficacy. Drug Saf. 2013;36(6):413–426.
   PubMed Web of Science ®Google Scholar
• Hughes TP, Mahon F-X, Kim D-W, et al. Peripheral arterial occlusive disease (PAOD) in patients (Pts) receiving dasatinib: experience across multiple clinical trials. Blood. 2013;122:1489–1489.
   Web of Science ®Google Scholar
• Pinilla-Ibarz J, Sweet K, Emole J, et al. Long-term BCR-ABL1 tyrosine kinase inhibitor therapy in chronic myeloid leukemia. Anticancer Res. 2015;35(12):6355–6364.
   PubMed Web of Science ®Google Scholar
• Rosti G, Martinelli G, Baccarani M. In reply to 'Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med. 2007;13(1):15–15.
   PubMedGoogle Scholar
• Hatfield A, Owen S, Pilot PR. In reply to 'Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med. 2007;13(1):13–13. author reply 15-16.
   PubMed Web of Science ®Google Scholar
• Gambacorti C, Tornaghi L, Franceschino A, et al. In reply to 'Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med. 2007;13(1):13–14.
   PubMedGoogle Scholar
• Atallah E, Kantarjian H, Cortes J. In reply to 'Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med. 2007;13(1):14–14.
   PubMedGoogle Scholar
• Estabragh ZR, Knight K, Watmough SJ, et al. A prospective evaluation of cardiac function in patients with chronic myeloid leukaemia treated with imatinib. Leuk Res. 2011;35(1):49–51.
   PubMed Web of Science ®Google Scholar
• Ribeiro AL, Marcolino MS, Bittencourt HN, et al. An evaluation of the cardiotoxicity of imatinib mesylate. Leuk Res. 2008;32(12):1809–1814.
   PubMed Web of Science ®Google Scholar
• Marcolino MS, Ribeiro AL, Clementino NC, et al. The use of imatinib mesylate has no adverse effects on the heart function. Results of a pilot study in patients with chronic myeloid leukemia. Leuk Res. 2011;35(3):317–322.
   PubMed Web of Science ®Google Scholar
• Marcolino MS, Boersma E, Clementino NC, et al. The duration of the use of imatinib mesylate is only weakly related to elevated BNP levels in chronic myeloid leukaemia patients. Hematol Oncol. 2011;29(3):124–130.
   PubMed Web of Science ®Google Scholar
• Kerkela R, Grazette L, Yacobi R, et al. Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med. 2006;12:908–916.
   PubMed Web of Science ®Google Scholar
• Giles FJ, Mauro MJ, Hong F, et al. Rates of peripheral arterial occlusive disease in patients with chronic myeloid leukemia in the chronic phase treated with imatinib, nilotinib, or non-tyrosine kinase therapy: a retrospective cohort analysis. Leukemia. 2013;27(6):1310–1315.
   PubMed Web of Science ®Google Scholar
• Cortes JE, Kantarjian H, Shah NP, et al. Ponatinib in refractory Philadelphia chromosome-positive leukemias. N Engl J Med. 2012;367(22):2075–2088.
   PubMed Web of Science ®Google Scholar
• 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):1648–1671.
   PubMed Web of Science ®Google Scholar
• Mayer K, Gielen GH, Willinek W, et al. Fatal progressive cerebral ischemia in CML under third-line treatment with ponatinib. Leukemia. 2014;28(4):976–977.
   PubMed Web of Science ®Google Scholar
• Breccia M, Muscaritoli M, Gentilini F, et al. Impaired fasting glucose level as metabolic side effect of nilotinib in non-diabetic chronic myeloid leukemia patients resistant to imatinib. Leuk Res. 2007;31(12):1770–1772.
   PubMed Web of Science ®Google Scholar
• Nicolini FE, Turkina A, Shen ZX, et al. Expanding Nilotinib Access in Clinical Trials (ENACT): an open-label, multicenter study of oral nilotinib in adult patients with imatinib-resistant or imatinib-intolerant Philadelphia chromosome-positive chronic myeloid leukemia in the chronic phase. Cancer. 2012;118(1):118–126.
   PubMed Web of Science ®Google Scholar
• Le Coutre P, Giles FJ, Hochhaus A, et al. Analysis of glucose profiles in imatinib-resistant or intolerant chronic myelogenous leukemia (CML) patients (pts) treated with nilotinib: lack of correlation between glucose levels and nilotinib efficacy. Blood. 2007;110(11):4588–4588.
   PubMed Web of Science ®Google Scholar
• Saglio G, Larson RA, Hughes TP, et al. Efficacy and safety of nilotinib in chronic phase (CP) chronic myeloid leukemia (CML) patients (Pts) with type 2 diabetes in the ENESTnd trial. Blood. 2010;116(21):3430–3430.
   Google Scholar
• Delphine R, Gautier J-f, Breccia M, et al. Incidence of hyperglycemia by 3 years in patients (Pts) with newly diagnosed chronic myeloid leukemia in chronic phase (CML-CP) treated with nilotinib (NIL) or imatinib (IM) in ENESTnd. Blood. 2012;120(21):1686–1686.
   Web of Science ®Google Scholar
• Cortes JE, Kim D-W, Pinilla-Ibarz J, et al. Long-term follow-up of ponatinib efficacy and safety in the phase 2 PACE trial. Blood. 2014;124(21):3135–3135.
   Web of Science ®Google Scholar
• Larson RA, Le Coutre PD, Reiffers J, et al. Comparison of nilotinib and imatinib in patients (pts) with newly diagnosed chronic myeloid leukemia in chronic phase (CML-CP): ENESTnd beyond one year. J Clin Oncol. 2010;28(15_suppl):6501–6501.
   Web of Science ®Google Scholar
• Jain P, Kantarjian H, Jabbour E, et al. Ponatinib as first-line treatment for patients with chronic myeloid leukaemia in chronic phase: a phase 2 study. Lancet Haematol. 2015;2(9):e376–e383.
   PubMed Web of Science ®Google Scholar
• Pfirrmann M, Baccarani M, Saussele S, et al. Prognosis of long-term survival considering disease-specific death in patients with chronic myeloid leukemia. Leukemia. 2016;30(1):48–56.
   PubMed Web of Science ®Google Scholar
• Brunner AM, Campigotto F, Sadrzadeh H, et al. Trends in all-cause mortality among patients with chronic myeloid leukemia: a surveillance, epidemiology, and end results database analysis. Cancer. 2013;119(14):2620–2629.
   PubMed Web of Science ®Google Scholar
• National Cancer Institute (NCI), Surveillance, Epidemiology, and End Results (SEER) Program, SEER*Stat Database: SEER 18 Regs Research Data, Nov 2017 Sub (1973–2014) <Katrina/Rita Population Adjustment> - Linked To County Attributes - Total U.S., 1969––2016 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, released April 2018, based on the November 2017 submission. Available from: https://seer.cancer.gov/data-software/documentation/seerstat/nov2017/.
   Google Scholar
• Xie Y, Davies SM, Xiang Y, et al. Trends in leukemia incidence and survival in the United States (1973–1998). Cancer. 2003;97(9):2229–2235.
   PubMed Web of Science ®Google Scholar
• Louvet C, Szot GL, Lang J, et al. Tyrosine kinase inhibitors reverse type 1 diabetes in nonobese diabetic mice. Proc Natl Acad Sci USA. 2008;105(48):18895–18900.
   PubMed Web of Science ®Google Scholar
• Schermuly RT, Dony E, Ghofrani HA, et al. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest. 2005;115(10):2811–2821.
   PubMed Web of Science ®Google Scholar
• Lassila M, Allen TJ, Cao Z, et al. Imatinib attenuates diabetes-associated atherosclerosis. ATVB. 2004;24(5):935–942.
   Google Scholar
• Druker BJ, Guilhot F, O'Brien SG, et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med. 2006;355(23):2408–2417.
   PubMed Web of Science ®Google Scholar
• Atallah E, Durand J-B, Kantarjian H, et al. Congestive heart failure is a rare event in patients receiving imatinib therapy. Blood. 2007;110(4):1233–1237.
   PubMed Web of Science ®Google Scholar
• Austin PC, Fine JP. Practical recommendations for reporting Fine-Gray model analyses for competing risk data. Stat Med. 2017;36(27):4391–4400.
   PubMed Web of Science ®Google Scholar
• Andersen PK, Keiding N. Interpretability and importance of functionals in competing risks and multistate models. Stat Med. 2012;31(11–12):1074–1088.
   PubMed Web of Science ®Google Scholar
• Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov. ) SEER*Stat Database: Incidence - SEER 13 Regs excluding AK Research Data, Nov 2018 Sub (1992–2016) for SMRs - Linked To County Attributes - Total U.S., 1969–2017 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, released April 2019, based on the November 2018 submission.
   Google Scholar
• Moslehi JJ, Deininger M. Tyrosine kinase inhibitor-associated cardiovascular toxicity in chronic myeloid leukemia. J Clin Oncol. 2015;33(35):4210–4218.
   PubMed Web of Science ®Google Scholar
• Sidney S, Quesenberry CP, Jr., Jaffe MG, et al. Recent trends in cardiovascular mortality in the United States and public health goals. JAMA Cardiol. 2016;1(5):594–599.
   PubMed Web of Science ®Google Scholar
• Senkus E, Jassem J. Cardiovascular effects of systemic cancer treatment. Cancer Treat Rev. 2011;37(4):300–311.
   PubMed Web of Science ®Google Scholar
• Yeh ET. Cardiotoxicity induced by chemotherapy and antibody therapy. Annu Rev Med. 2006;57(1):485–498.
   PubMedGoogle Scholar
• Slordal L, Spigset O. Heart failure induced by non-cardiac drugs. Drug Saf. 2006;29:567–586.
   PubMed Web of Science ®Google Scholar
• Floyd JD, Nguyen DT, Lobins RL, et al. Cardiotoxicity of cancer therapy. J Clin Oncol. 2005;23(30):7685–7696.
   PubMed Web of Science ®Google Scholar
• Yeh ET, Tong AT, Lenihan DJ, et al. Cardiovascular complications of cancer therapy: diagnosis, pathogenesis, and management. Circulation. 2004;109(25):3122–3131.
   PubMed Web of Science ®Google Scholar
• Kuwata A, Ohashi M, Sugiyama M, et al. A case of reversible dilated cardiomyopathy after alpha-interferon therapy in a patient with renal cell carcinoma. Am J Med Sci. 2002;324(6):331–334.
   PubMed Web of Science ®Google Scholar
• Kobayashi T, Sato Y, Hasegawa Y, et al. Multiple myeloma complicated by congestive heart failure following first administration of recombinant alpha-interferon. Intern Med. 1992;31(7):936–940.
   PubMed Web of Science ®Google Scholar
• Sonnenblick M, Rosenmann D, Rosin A. Reversible cardiomyopathy induced by interferon. BMJ. 1990;300(6733):1174–1175.
   PubMedGoogle Scholar
• Deyton LR, Walker RE, Kovacs JA, et al. Reversible cardiac dysfunction associated with interferon alfa therapy in AIDS patients with Kaposi's sarcoma. N Engl J Med. 1989;321(18):1246–1249.
   PubMed Web of Science ®Google Scholar
• Vial T, Descotes J. Immune-mediated side-effects of cytokines in humans. Toxicology. 1995;105(1):31–57.
   PubMed Web of Science ®Google Scholar
• Guerci AP, Guerci B, Levy-Marchal C, et al. Onset of insulin-dependent diabetes mellitus after interferon-alfa therapy for hairy cell leukaemia. Lancet. 1994;343(8906):1167–1168.
   PubMed Web of Science ®Google Scholar
• Fabris P, Betterle C, Floreani A, et al. Development of type 1 diabetes mellitus during interferon alfa therapy for chronic HCV hepatitis. Lancet. 1992;340(8818):548.
   PubMed Web of Science ®Google Scholar
• Koivisto VA. Interferon alfa and development of type 1 diabetes mellitus. Lancet. 1992;340(8829):1236.
   PubMed Web of Science ®Google Scholar
• Epidemiology CNCfHSOoAa. Health, United States, 2017 – Data Finder. 2018.
   Google Scholar
• Steinberg BA, Bhatt DL, Mehta S, et al. Nine-year trends in achievement of risk factor goals in the US and European outpatients with cardiovascular disease. Am Heart J. 2008;156(4):719–727.
   PubMed Web of Science ®Google Scholar
• Mann D, Reynolds K, Smith D, et al. Trends in statin use and low-density lipoprotein cholesterol levels among US adults: impact of the 2001 National Cholesterol Education Program guidelines. Ann Pharmacother. 2008;42(9):1208–1215.
   PubMed Web of Science ®Google Scholar
• Coutinho AD, Makenbaeva D, Farrelly E, et al. Elevated cardiovascular disease risk in patients with chronic myelogenous leukemia seen in community-based oncology practices in the United States. Clin Lymphoma Myeloma Leuk. 2017;17(10):676–683.
   PubMed Web of Science ®Google Scholar
• Breccia M, Molica M, Zacheo I, et al. Application of systematic coronary risk evaluation chart to identify chronic myeloid leukemia patients at risk of cardiovascular diseases during nilotinib treatment. Ann Hematol. 2015;94(3):393–397.
   PubMed Web of Science ®Google Scholar
• Jabbour E, Makenbaeva D, Lingohr-Smith M, et al. Use of real-world claim databases to assess prevalence of comorbid conditions relevant to the treatment of chronic myelogenous leukemia based on national comprehensive network treatment guidelines. Clin Lymphoma Myeloma Leuk. 2015;15(12):797–802.
   PubMed Web of Science ®Google Scholar
• Abdel-Rahman O. Risk of cardiac death among cancer survivors in the United States: a SEER database analysis. Expert Rev Anticancer Ther. 2017;17(9):873–878.
   PubMed Web of Science ®Google Scholar