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Arterial Thrombosis in Patients with Cancer

  • Cardio-oncology (M Fradley, Section Editor)
  • Published:
Current Treatment Options in Cardiovascular Medicine Aims and scope Submit manuscript

Abstract

Purpose of review

Cancer is a common cause of morbidity and mortality in the USA. While the association between venous thrombosis and malignancy is well established, arterial thrombosis has more recently been recognized as a serious complication of cancer and certain chemotherapeutic agents. This review aims to summarize the most recent literature regarding the incidence and risk factors for cancer-related arterial thrombosis, understand the pathophysiologic mechanisms of thrombosis, and highlight the specific diagnostic and treatment considerations relevant to cancer patients.

Recent findings

Based on a recent study looking at the Surveillance, Epidemiology, and End Results (SEER) database, the incidence of arterial thromboembolic events (ATEs) in patients with cancer at 6 months is 4.7%; the presence of an ATE is predictive of worse outcomes. Certain drugs such as platinum-based agents, vascular endothelial growth factor inhibitors, tyrosine kinase inhibitors, and taxanes have been associated with high rates of ATEs. Increased platelet reactivity appears crucial to development of arterial thrombosis in cancer patients.

Summary

Cancer patients have an increased risk of arterial thrombosis that is likely due to both a cancer-associated procoagulant state as well as the adverse effects of certain chemotherapeutic agents. Treatment of arterial thromboembolism in cancer patients typically requires a multidisciplinary approach in part due to high rates of thrombocytopenia and stent thrombosis in the setting of percutaneous interventions. More studies are needed to investigate optimal prophylaxis, surveillance strategies, and treatments of cancer-related arterial thromboembolic disease.

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References and Recommended Reading

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Prevention C for DC and. Deaths and mortality. 2017. Available at: https://www.cdc.gov/nchs/fastats/deaths.htm. Accessed October 12, 2017.

  2. Institute NC. Cancer statistics. Available at: https://www.cancer.gov/about-cancer/understanding/statistics. Accessed January 1, 2017.

  3. American Cancer Society, Cancer Treatment & Survivorship: Facts &Figures, 2016-2017. https://www.cancer.org/content/dam/cancerorg/research/cancer-facts-and-statistics/cancer-treatment-and-survivorship-factsand-figures/cancer-treatment-and-survivorship-facts-and-figures-2016-2017.pdf. Accessed 16 Mar 2018.

  4. Khorana AA, Francis CW, Culakova E, Kuderer NMLG. Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy. J Thromb Haemost. 2007;5:632–4.

    Article  CAS  PubMed  Google Scholar 

  5. Blann AD DS. Arterial and venous thrombosis in cancer patients. Cardiol Res Pr 2011:394740.

  6. Khorana AA, Francis CW, Blumberg N, Culakova E, Refaai MA, Lyman GH. Blood transfusions, thrombosis, and mortality in hospitalized patients with cancer. Arch Intern Med. 2008;168:2377–81.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Khorana AA, Francis CW, Culakova E, Fisher RI, Kuderer NMLG. Thromboembolism in hospitalized neutropenic cancer patients. J Clin Oncol. 2006;24:484–90.

    Article  PubMed  Google Scholar 

  8. •• Navi BB, Reiner AS, Kamel H, Iadecola C, Okin PM, Elkind MSV, et al. Risk of arterial thromboembolism in patients with cancer. J Am Coll Cardiol. 2017;70:926–38. The authors describe the incidence of arterial thromboembolic events in cancer patients included in the SEER database. Incidence with respect to time from diagnosis, the type of cancer, and the cancer stage is also reported

    Article  PubMed  Google Scholar 

  9. Abbott JD, Ahmed HN, Vlachos HA, Selzer FWD. Comparison of outcome in patients with ST-elevation versus non-ST-elevation acute myocardial infarction treated with percutaneous coronary intervention (from the National Heart, Lung, and Blood Institute dynamic registry). Am J Cardiol. 2007;100:190–5.

    Article  PubMed  Google Scholar 

  10. Wang F, Gulati R, Lennon RJ, Lewis BR, Park J, Sandhu GS, et al. Cancer history portends worse acute and long-term noncardiac (but not cardiac) mortality after primary percutaneous coronary intervention for acute ST-segment elevation myocardial infarction. Mayo Clin Proc. 2016;91:1680–92.

    Article  PubMed  Google Scholar 

  11. Navi BB, Singer S, Merkler AE, Cheng NT, Stone JB, Kamel H, et al. Recurrent thromboembolic events after ischemic stroke in patients with cancer. Neurology. 2014;83:26–33.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Gross CM, Posch MG, Geier C, Olthoff H, Krämer J, Dechend R, et al. Subacute coronary stent thrombosis in cancer patients. J Am Coll Cardiol. 2008;51:1232–3.

    Article  PubMed  Google Scholar 

  13. Moore RA, Adel N, Riedel E, Bhutani M, Feldman DR, Tabbara NE, et al. High incidence of thromboembolic events in patients treated with cisplatin-based chemotherapy: a large retrospective analysis. J Clin Oncol. 2011;29:3466–73.

    Article  CAS  PubMed  Google Scholar 

  14. Barceló R, Muñoz AL-VG. Prospective evaluation of major vascular events in patients with nonsmall cell lung carcinoma treated with cisplatin and gemcitabine. Cancer. 2005;104:1110–1.

    Article  PubMed  Google Scholar 

  15. Weijl NI, Rutten MF, Zwinderman AH, Keizer HJ, Nooy MA, Rosendaal FR, et al. Thromboembolic events during chemotherapy for germ cell cancer: a cohort study and review of the literature. J Clin Oncol. 2000;18:2169–78.

    Article  CAS  PubMed  Google Scholar 

  16. Sugrue, MM, Yi, J, Purdie, D, Dong, W, Grothey, A, Kozloff M. Serious arterial thromboembolic events (sATE) in patients (pts) with metastatic colorectal cancer (mCRC) treated with bevacizumab (BV): results from the BRiTE registry. J Clin Oncol.

  17. Schutz FA, Je Y, Azzi GR, Nguyen PLCT. Bevacizumab increases the risk of arterial ischemia: a large study in cancer patients with a focus on different subgroup outcomes. Ann Oncol. 2011;22:14040–1412.

    Article  Google Scholar 

  18. Ranpura V, Hapani S, Chuang JWS. Risk of cardiac ischemia and arterial thromboembolic events with the angiogenesis inhibitor bevacizumab in cancer patients: a meta-analysis of randomized controlled trials. Acta Oncol. 2010;49:287–97.

    Article  CAS  PubMed  Google Scholar 

  19. Tebbutt NC, Murphy F, Zannino D, Wilson K, Cummins MM, Abdi E, et al. Risk of arterial thromboembolic events in patients with advanced colorectal cancer receiving bevacizumab. Ann Oncol. 2011;22:1834–8.

    Article  CAS  PubMed  Google Scholar 

  20. Scappaticci FA, Skillings JR, Holden SN, Gerber HP, Miller K, Kabbinavar F, et al. Arterial thromboembolic events in patients with metastatic carcinoma treated with chemotherapy and bevacizumab. J Natl Cancer Inst. 2007;99:1232–9.

    Article  PubMed  Google Scholar 

  21. Choueiri TK, Schutz FA, Je Y, Rosenberg JEBJ. Risk of arterial thromboembolic events with sunitinib and sorafenib: a systematic review and meta-analysis of clinical trials. J Clin Oncol. 2010;28:2280–5.

    Article  CAS  PubMed  Google Scholar 

  22. Herrmann J, Yang EH, Iliescu CA, Cilingiroglu M, Charitakis K, Hakeem A, et al. Vascular toxicities of cancer therapies: the old and the new—an evolving avenue. Circulation. 2016;133:1272–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Plana JC, Chair MG, Barac A, Ewer MS, Ky B, Scherrer-Crosbie M, et al. Expert consensus for multimodality imaging evaluation of adult patients during and after cancer therapy: a report from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2014;27:911–39.

    Article  PubMed  Google Scholar 

  24. McCormack P. Pazopanib: a review of its use in the management of advanced renal cell carcinoma. Drugs. 2014;74:1111–25.

    Article  CAS  PubMed  Google Scholar 

  25. Frampton J. Pazopanib: a review in advanced renal cell carcinoma. Target Oncol. 2017;12:543–54.

    Article  PubMed  Google Scholar 

  26. FDA. Ponatinib. Available at: https://www.accessdata.fda.gov/drugsatfda_docs/label/2014/203469s009lbl.pdf.

  27. Doll DC, List AF, Greco FA, Hainsworth JD, Hande KRJD. Acute vascular ischemic events after cisplatin-based combination chemotherapy for germ-cell tumors of the testis. Ann Intern Med. 1986;105:48–51.

    Article  CAS  PubMed  Google Scholar 

  28. Haugnes HS, Wethal T, Aass N, Dahl O, Klepp O, Langberg CW, et al. Cardiovascular risk factors and morbidity in long-term survivors of testicular cancer: a 20-year follow-up study. J Clin Oncol. 2010;28:4649–57.

    Article  PubMed  Google Scholar 

  29. Li W, Cornell FR, Lenihan D, Slosky D, Jagasia M, Piazza G, et al. Cardiovascular complications of novel multiple myeloma treatments. Circulation. 2016;133:908–12.

    Article  PubMed  Google Scholar 

  30. Chen XL, Lei YH, Liu CF, Yang QF, Zuo PY, Liu CY, et al. Angiogenesis inhibitor bevacizumab increases the risk of ischemic heart disease associated with chemotherapy: a meta-analysis. PLoS One. 2013;8:e66721.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Chu TF, Rupnick MA, Kerkela R, Dallabrida SM, Zurakowski D, Nguyen L, et al. Cardiotoxicity associated with tyrosine kinase inhibitor sunitinib. Lancet. 2007;370:2011–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebels M, et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med. 2007;356:125–34.

    Article  CAS  PubMed  Google Scholar 

  33. Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Staehler M, et al. Sorafenib for treatment of renal cell carcinoma: final efficacy and safety results of the phase III treatment approaches in renal cancer global evaluation trial. J Clin Oncol. 2009;27:3312–8.

    Article  CAS  PubMed  Google Scholar 

  34. Cortes JE, Kim DW, Pinilla-Ibarz J, le Coutre P, Paquette R, Chuah C, et al. A phase 2 trial of ponatinib in Philadelphia chromosome-positive leukemias. N Engl J Med. 2013;369:1783–96.

    Article  CAS  PubMed  Google Scholar 

  35. Cutsem E, Hoff PM, Blum JL, Van Abt MOB. Incidence of cardiotoxicity with the oral fluoropyrimidine capecitabine is typical of that reported with 5-fluorouracil. Ann Oncol. 2002;13:484–5.

    Article  PubMed  Google Scholar 

  36. Yeh ETBC. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol. 2009;53:2231–47.

    Article  CAS  PubMed  Google Scholar 

  37. Jensen SASJ. Risk factors and prevention of cardiotoxicity induced by 5-fluorouracil or capecitabine. Cancer Chemother Pharmacol. 2006;58:487–93.

    Article  CAS  PubMed  Google Scholar 

  38. Kosmas C, Kallistratos MS, Kopterides P, Syrios J, Skopelitis H, Mylonakis N, et al. Cardiotoxicity of fluoropyrimidines in different schedules of administration: a prospective study. J Cancer Res Clin Oncol. 2008;134:75–82.

    Article  CAS  PubMed  Google Scholar 

  39. Labianca R, Beretta G, Clerici M, Fraschini PLG. Cardiac toxicity of 5-fluorouracil: a study on 1083 patients. Tumori. 1982;68:505–10.

    Article  CAS  PubMed  Google Scholar 

  40. Walko CMLC. Capecitabine: a review. Clin Ther. 2005;27:23–44.

    Article  CAS  PubMed  Google Scholar 

  41. Meyer CC, Calis KA, Burke LB, Walawander CAGT. Symptomatic cardiotoxicity associated with 5-fluorouracil. Pharmacotherapy. 1997;17:729–36.

    CAS  PubMed  Google Scholar 

  42. de Forni M, Malet-Martino MC, Jaillais P, Shubinski RE, Bachaud JM, Lemaire L, et al. Cardiotoxicity of high-dose continuous infusion fluorouracil: a prospective clinical study. J Clin Oncol. 1992;10:1795–801.

    Article  PubMed  Google Scholar 

  43. Polk A, Vaage-Nilsen M, Vistisen KND. Cardiotoxicity in cancer patients treated with 5-fluorouracil or capecitabine: a systematic review of incidence, manifestations and predisposing factors. Cancer Treat Rev. 2013;39:974–84.

    Article  CAS  PubMed  Google Scholar 

  44. Shah K, Gupta S, Ghosh J, Bajpai JMA. Acute non-ST elevation myocardial infarction following paclitaxel administration for ovarian carcinoma: a case report and review of literature. J Cancer Res Ther. 2012;8:442–4.

    Article  PubMed  Google Scholar 

  45. Berardi R, Caramanti M, Savini A, Chiorrini S, Pierantoni C, Onofri A, et al. State of the art for cardiotoxicity due to chemotherapy and to targeted therapies: a literature review. Crit Rev Oncol Hematol. 2013;88:75–86.

    Article  PubMed  Google Scholar 

  46. Rowinsky EK, McGuire WP, Guarnieri T, Fisherman JS, Christian MCDR. Cardiac disturbances during the administration of taxol. J Clin Oncol. 1991;9:1704–12.

    Article  CAS  PubMed  Google Scholar 

  47. Amir E, Seruga B, Niraula S, Carlsson LOA. Toxicity of adjuvant endocrine therapy in postmenopausal breast cancer patients: a systematic review and meta-analysis. J Natl Cancer Inst. 2011;103:1299–309.

    Article  CAS  PubMed  Google Scholar 

  48. Herrmann J. Tyrosine kinase inhibitors and vascular toxicity: impetus for a classification system? Curr Oncol Rep. 2016;18:33.

    Article  PubMed  Google Scholar 

  49. Coutre P, Rea D, Abruzzese E, Dombret H, Trawinska MM, Herndlhofer S, et al. Severe peripheral arterial disease during nilotinib therapy. J Natl Cancer Inst. 2011;103:1347–8.

    Article  PubMed  Google Scholar 

  50. Larson RA, Hochhaus A, Hughes TP, Clark RE, Etienne G, Kim DW, et al. Nilotinib vs imatinib in patients with newly diagnosed Philadelphia chromosome-positive chronic myeloid leukemia in chronic phase: ENESTnd 3-year follow-up. Leukemia. 2012;26:2197–203.

    Article  CAS  PubMed  Google Scholar 

  51. Aichberger KJ, Herndlhofer S, Schernthaner GH, Schillinger M, Mitterbauer-Hohendanner G, Sillaber CVP. Progressive peripheral arterial occlusive disease and other vascular events during nilotinib therapy in CML. Am J Hematol. 2011;86:533–9.

    Article  CAS  PubMed  Google Scholar 

  52. Libourel EJ, Sonneveld P, van der Holt B, de Maat MPLF. High incidence of arterial thrombosis in young patients treated for multiple myeloma: results of a prospective cohort study. Blood. 2010;116:22–6.

    Article  CAS  PubMed  Google Scholar 

  53. Alkindi S, Dennison DPA. Arterial and venous thrombotic complications with thalidomide in multiple myeloma. Arch Med Res. 2008;39:257–8.

    Article  PubMed  Google Scholar 

  54. Saphner T, Tormey DCGR. Venous and arterial thrombosis in patients who received adjuvant therapy for breast cancer. J Clin Oncol. 1991;9:286–94.

    Article  CAS  PubMed  Google Scholar 

  55. Gov.uk, Drug Safety Update. Lenalidomide: risk of thrombosis and thromboembolism. https://www.gov.uk/drug-safety-update/lenalidomide-risk-ofthrombosis-and-thromboembolism. Accessed 16 Mar 2018.

  56. Rumbaut RE, Thiagarajan P. Platelet-vessel wall interactions inHemostasis and thrombosis. Chapter 6: arterial, venous, and microvascular hemostasis/thrombosis. San Rafael: Morgan & Claypool Life Sciences; 2010 https://www.ncbi.nlm.nih.gov/books/NBK53450. Accessed 16 Mar 2018.

  57. Lowe G. Common risk factors for both arterial and venous thrombosis. Br J Haematol. 2008;140:488–95.

    Article  PubMed  Google Scholar 

  58. Previtali E, Bucciarelli P, Passamonti SM, Martinelli I. Risk factors for venous and arterial thrombosis. Blood Transfus. 2011;9:120–38.

    PubMed  PubMed Central  Google Scholar 

  59. Goto I, Okamoto R, Sawai T, Takasaki A, Takeuchi T, Matsuo H, et al. A case of aortic thrombosis and embolism preceding the progression of early esophageal cancer. J Cardiol Cases. 2013;7:e123–5.

    Article  Google Scholar 

  60. Vavlukis M, Kotlar I, Chaparoska E, Antova EKS. Diffuse arterial thrombosis as a first manifestation of occult malignancy. Case Rep Med. 2016;2016:1658392.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Rigdon E. Trousseau’s syndrome and acute arterial thrombosis. Cardiovasc Surg. 2000;8:214–8.

    Article  CAS  PubMed  Google Scholar 

  62. Li W, Garcia D, Cornell RF, Gailani D, Laubach J, Maglio ME, et al. Cardiovascular and thrombotic complications of novel multiple myeloma therapies: a review. JAMA Oncol. 2017;3:980–8.

    Article  PubMed  Google Scholar 

  63. Kristinsson SY, Pfeiffer RM, Björkholm M, Goldin LR, Schulman S, Blimark C, et al. Arterial and venous thrombosis in monoclonal gammopathy of undetermined significance and multiple myeloma: a population-based study. Blood. 2010;115:4991–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Paris F, Fuks Z, Kang A, Capodieci P, Juan G, Ehleiter D, et al. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science. 2001;293(80):293–7.

    Article  CAS  PubMed  Google Scholar 

  65. Brosius FC 3rd, Waller BFRW. Radiation heart disease. Analysis of 16 young (aged 15 to 33 years) necropsy patients who received over 3,500 rads to the heart. Am J Med. 1981;70:519–30.

    Article  PubMed  Google Scholar 

  66. • Iliescu CA, Grines CL, Herrmann J, Yang EH, Cilingiroglu M, Charitakis K, et al. SCAI expert consensus statement: evaluation, management, and special considerations of cardio-oncology patients in the cardiac catheterization laboratory (endorsed by the Cardiological Society of India, and sociedad Latino Americana de Cardiologıa interve). Catheter Cardiovasc Interv. 2016;87:E202–23. This article describes the current expert consensus regarding management of cancer patients requiring evaluation in the catheterization laboratory. Cancer associated complications such as thrombocytopenia require special attention when treating arterial thromboembolic disease

    Article  PubMed  Google Scholar 

  67. Mulrooney DA, Nunnery SE, Armstrong GT, Ness KK, Srivastava D, Donovan FD, et al. Coronary artery disease detected by coronary computed tomography angiography in adult survivors of childhood Hodgkin lymphoma. Cancer. 2014;120:3536–44.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Brønnum D, et al. Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med. 2013;368:987–98.

    Article  CAS  PubMed  Google Scholar 

  69. Heinmöller E, Weinel RJ, Heidtmann HH, Salge U, Seitz R, Schmitz I, et al. Studies on tumor-cell-induced platelet aggregation in human lung cancer cell lines. J Cancer Res Clin Oncol. 1996;122:735–44.

    Article  PubMed  Google Scholar 

  70. Dorresteijn LD, Kappelle AC, Boogerd W, Klokman WJ, Balm AJ, Keus RB, et al. Increased risk of ischemic stroke after radiotherapy on the neck in patients younger than 60 years. J Clin Oncol. 2002;20:282–8.

    Article  PubMed  Google Scholar 

  71. Plummer C, Henderson RD, O’Sullivan JDRS. Ischemic stroke and transient ischemic attack after head and neck radiotherapy: a review. Stroke. 2011;42:2410–8.

    Article  PubMed  Google Scholar 

  72. Mezouar S, Frère C, Darbousset R, Mege D, Crescence L, Dignat-George F, et al. Role of platelets in cancer and cancer-associated thrombosis: experimental and clinical evidences. Thromb Res. 2016;139:65–76.

    Article  CAS  PubMed  Google Scholar 

  73. Pavo N, Raderer M, Hülsmann M, Neuhold S, Adlbrecht C, Strunk G, et al. Cardiovascular biomarkers in patients with cancer and their association with all-cause mortality. Heart. 2015;101:1874–80.

    Article  CAS  PubMed  Google Scholar 

  74. Herrmann JLA. The endothelium: dysfunction and beyond. J Nucl Cardiol. 2001;8:197–206.

    Article  CAS  PubMed  Google Scholar 

  75. Herrmann JLA. The endothelium—the cardiovascular health barometer. Herz. 2008;33:343–53.

    Article  PubMed  Google Scholar 

  76. Seizer PMA. Platelets and matrix metalloproteinases. Thromb Haemost. 2013;110:903–9.

    Article  CAS  PubMed  Google Scholar 

  77. Gremmel T, Perkmann T, Seidinger D, Koppensteiner R, Panzer S, Kopp CWSS. Differential impact of inflammation on six laboratory assays measuring residual arachidonic acid-inducible platelet reactivity during dual antiplatelet therapy. J Atheroscler Thromb. 2013;20:630–45.

    Article  CAS  PubMed  Google Scholar 

  78. Alonso-Escolano D, Strongin AY, Chung AW, Deryugina EIRM. Membrane type-1 matrix metalloproteinase stimulates tumour cell-induced platelet aggregation: role of receptor glycoproteins. Br J Pharmacol. 2004;141:241–52.

    Article  CAS  PubMed  Google Scholar 

  79. Bauer AT, Suckau J, Frank K, Desch A, Goertz L, Wagner AH, et al. von Willebrand factor fibers promote cancer-associated platelet aggregation in malignant melanoma of mice and humans. Blood. 2015;125:3153–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Wang JG, Geddings JE, Aleman MM, et al. Tumor-derived tissue factor activates coagulation and enhances thrombosis in a mouse xenograft model of human pancreatic cancer. Blood 2012;7:119(23):5543–52. https://doi.org/10.1182/blood-2012-01-402156.

  81. Soultati A, Mountzios G, Avgerinou C, Papaxoinis G, Pectasides D, Dimopoulos MAPC. Endothelial vascular toxicity from chemotherapeutic agents: preclinical evidence and clinical implications. Cancer Treat Rev. 2012;38:473–83.

    Article  CAS  PubMed  Google Scholar 

  82. Winnik S, Lohmann C, Siciliani G, von Lukowicz T, Kuschnerus K, Kraenkel N, et al. Systemic VEGF inhibition accelerates experimental atherosclerosis and disrupts endothelial homeostasis—implications for cardiovascular safety. Int J Cardiol. 2013;168:2453–61.

    Article  PubMed  Google Scholar 

  83. Pandey AK, Singhi EK, Arroyo JP, Ikizler TA, Gould ER, Brown J, et al. Mechanisms of VEGF (vascular endothelial growth factor) inhibitor-associated hypertension and vascular disease. Hypertension. 2018;71:e1–8.

    Article  CAS  PubMed  Google Scholar 

  84. Moslehi JJDM. Tyrosine kinase inhibitor-associated cardiovascular toxicity in chronic myeloid leukemia. J Clin Oncol. 2015;33:4210–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Hadzijusufovic E, Albrecht-Schgoer K, Huber K, Hoermann G, Grebien F, Eisenwort G, et al. Nilotinib-induced vasculopathy: identification of vascular endothelial cells as a primary target site. Leukemia. 2017;31:2388–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Kristian Thygesen, Joseph S. Alpert, Allan S. Jaffe, Maarten L. Simoons, Bernard R. Chaitman HDW, infarction and the WG on behalf of the JETF for the UD of M. Third universal definition of myocardial infarction. Circulation 2012;126:2020–2035.

  87. Elting LS, Rubenstein EB, Martin CG, Kurtin D, Rodriguez S, Laiho E, et al. Incidence, cost, and outcomes of bleeding and chemotherapy dose modification among solid tumor patients with chemotherapy-induced thrombocytopenia. J Clin Oncol. 2001;19:1137–46.

    Article  CAS  PubMed  Google Scholar 

  88. Hakim DA, Dangas GD, Caixeta A, Nikolsky E, Lansky AJ, Moses JW, et al. Impact of baseline thrombocytopenia on the early and late outcomes after ST-elevation myocardial infarction treated with primary angioplasty: analysis from the harmonizing outcomes with revascularization and stents in acute myocardial infarction (HORIZONS). Am Heart J. 2011;161:391–6.

    Article  PubMed  Google Scholar 

  89. McCarthy CP, Steg GBD. The management of antiplatelet therapy in acute coronary syndrome patients with thrombocytopenia: a clinical conundrum. Eur Heart J. 2017;38:3488–92.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Giza DE, Lopez-Mattei J, Vejpongsa P, Munoz E, Iliescu G, Kitkungvan D, et al. Stress-induced cardiomyopathy in cancer patients. Am J Cardiol. 2017;120:2284–8.

    Article  PubMed  Google Scholar 

  91. Padfield GJ, Newby DEMN. Understanding the role of endothelial progenitor cells in percutaneous coronary intervention. J Am Coll Cardiol. 2010;55:1553–65.

    Article  PubMed  Google Scholar 

  92. Douglas G, Van Kampen E, Hale AB, McNeill E, Patel J, Crabtree MJ, et al. Endothelial cell repopulation after stenting determines in-stent neointima formation: effects of bare-metal vs. drug-eluting stents and genetic endothelial cell modification. Eur Heart J. 2013;34:3378–88.

    Article  CAS  PubMed  Google Scholar 

  93. Lev EI, Leshem-Lev D, Mager A, Vaknin-Assa H, Harel N, Zimra Y, et al. Circulating endothelial progenitor cell levels and function in patients who experienced late coronary stent thrombosis. Eur Heart J. 2010;31:2625–32.

    Article  CAS  PubMed  Google Scholar 

  94. Ramcharan KS, Lip GY, Stonelake PSBA. Effect of standard chemotherapy and antiangiogenic therapy on plasma markers and endothelial cells in colorectal cancer. Br J Cancer. 2014;111:1742–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Walter DH, Cejna M, Diaz-Sandoval L, Willis S, Kirkwood L, Stratford PW, et al. Local gene transfer of phVEGF-2 plasmid by gene-eluting stents: an alternative strategy for inhibition of restenosis. Circulation. 2004;110:36–45.

    Article  CAS  PubMed  Google Scholar 

  96. Guillem-Llobat P, Dovizio M, Bruno A, Ricciotti E, Cufino V, Sacco A, et al. Aspirin prevents colorectal cancer metastasis in mice by splitting the crosstalk between platelets and tumor cells. Oncotarget. 2016;7:32462–77.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Cooke NM, Spillane CD, Sheils O, O’Leary JKD. Aspirin and P2Y12 inhibition attenuate platelet-induced ovarian cancer cell invasion. BMC Cancer. 2015;627

  98. Gebremeskel S, LeVatte T, Liwski RS, Johnston BBM. The reversible P2Y12 inhibitor ticagrelor inhibits metastasis and improves survival in mouse models of cancer. Int J Cancer. 2015;136:234–40.

    Article  CAS  PubMed  Google Scholar 

  99. Dhillon PK, Kenfield SA, Stampfer MJ, Giovannucci ELCJ. Aspirin use after a prostate cancer diagnosis and cancer survival in a prospective cohort. Cancer Prev Res. 2012;5:1223–8.

    Article  CAS  Google Scholar 

  100. Cardwell CR, Kunzmann AT, Cantwell MM, Hughes C, Baron JA, Powe DGML. Low-dose aspirin use after diagnosis of colorectal cancer does not increase survival: a case-control analysis of a population-based cohort. Gastroenterology. 2014;146:700–8.

    Article  CAS  PubMed  Google Scholar 

  101. Ye XF, Wang J, Shi WTHJ. Relationship between aspirin use after diagnosis of colorectal cancer and patient survival: a meta-analysis of observational studies. Br J Cancer. 2014;111:2172–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Palumbo A, Cavo M, Bringhen S, Zamagni E, Romano A, Patriarca F, et al. Aspirin, warfarin, or enoxaparin thromboprophylaxis in patients with multiple myeloma treated with thalidomide: a phase III, open-label, randomized trial. J Clin Oncol. 2011;29:986–93.

    Article  CAS  PubMed  Google Scholar 

  103. Landolfi R, Marchioli R, Kutti J, Gisslinger H, Tognoni G. Patrono C BTEC on L-DA in PVI. Efficacy and safety of low-dose aspirin in polycythemia vera. N Engl J Med. 2004;350:114–24.

    Article  CAS  PubMed  Google Scholar 

  104. Khemasuwan D, Divietro ML, Tangdhanakanond K, Pomerantz SCEG. Statins decrease the occurrence of venous thromboembolism in patients with cancer. Am J Med. 2010;123:60–5.

    Article  CAS  PubMed  Google Scholar 

  105. Detrano R, Guerci AD, Carr JJ, Bild DE, Burke G, Folsom AR, et al. Coronary calcium as a predictor of coronary events in four racial or ethnic groups. N Engl J Med. 2008;358:1336–45.

    Article  CAS  PubMed  Google Scholar 

  106. A phase 2 pilot study of apixaban for the prevention of thromboembolic events in patients with advanced (metastatic) cancer. Available at: https://clinicaltrials.gov/ct2/show/NCT00320255. Last Accessed February 10, 2018.

  107. Biomarkers related to thrombosis in patients with newly diagnosed multiple myeloma receiving chemotherapy. Available at: https://clinicaltrials.gov/ct2/show/NCT01132833. Last Accessed February 10, 2018.

  108. Anti-platelet and statin therapy to prevent cancer-associated thrombosis. https://clinicaltrials.gov/ct2/show/NCT02285738. Last Accessed February 10, 2018.

  109. Apixaban for the prevention of venous thromboembolism in cancer patients (AVERT). https://clinicaltrials.gov/ct2/show/NCT02048865. Last Accessed February 10, 2018.

  110. Enoxaparin Versus Aspirin in Patients with Cancer and Stroke. https://clinicaltrials.gov/ct2/show/NCT01763606. Accessed 16 Mar 2018.

  111. Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C, et al. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med. 2017;377:1119–31.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Eric H. Yang MD.

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Mirela Tuzovic, Cezar Iliescu, Kostas Marmagkiolis, Boback Ziaeian, and Eric H. Yang each declare no potential conflicts of interest.

Joerg Herrmann was a participant in the 2014 Ponatinib in CML Cardio-Oncology Advisory Board meeting organized by ARIAD Pharmaceuticals and the 2015 Advisory Board meeting of the Institute for Cardio-Oncology sponsored by Bristol-Myers Squibb.

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This article does not contain any studies with human or animal subjects performed by any of the authors.

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This article is part of the Topical Collection on Cardio-oncology

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Tuzovic, M., Herrmann, J., Iliescu, C. et al. Arterial Thrombosis in Patients with Cancer. Curr Treat Options Cardio Med 20, 40 (2018). https://doi.org/10.1007/s11936-018-0635-x

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