Echocardiographic measures associated with the presence of left ventricular thrombus in patients with chemotherapy-related cardiac dysfunction
Danai Kitkungvan MD
Division of Cardiovascular Medicine, The University of Texas Health and Science Center at Houston, Houston, TX, USA
Search for more papers by this authorSyed W. Yusuf MBBS
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorRohit Moudgil MD, PhD
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorNicolas Palaskas MD
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorMichele Guindani PhD
Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorSong Juhee PhD
Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorSaamir Hassan MD
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorLiza Sanchez RCS
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorCorresponding Author
Jose Banchs MD
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Correspondence
Jose Banchs, Echocardiography, Medicine, Department of Cardiology, University of Texas - MD Anderson Cancer Center, Houston, TX, USA.
Email: [email protected]
Search for more papers by this authorDanai Kitkungvan MD
Division of Cardiovascular Medicine, The University of Texas Health and Science Center at Houston, Houston, TX, USA
Search for more papers by this authorSyed W. Yusuf MBBS
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorRohit Moudgil MD, PhD
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorNicolas Palaskas MD
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorMichele Guindani PhD
Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorSong Juhee PhD
Department of Biostatistics, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorSaamir Hassan MD
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorLiza Sanchez RCS
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Search for more papers by this authorCorresponding Author
Jose Banchs MD
Department of Cardiology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
Correspondence
Jose Banchs, Echocardiography, Medicine, Department of Cardiology, University of Texas - MD Anderson Cancer Center, Houston, TX, USA.
Email: [email protected]
Search for more papers by this authorAbstract
Background
Previous studies have not evaluated the prevalence and specific risk factors for the development of left ventricular (LV) thrombus in patients with severely reduced left ventricular dysfunction due to chemotherapy-related cardiomyopathy. We sought to evaluate the prevalence and potential markers of LV thrombus in this patient population.
Methods
From January 2009 to December 2013, patients with chemotherapy-related severe LV dysfunction (LV ejection fraction [LVEF] ≤ 30%) identified from MD Anderson Cancer Center database were reviewed. Patient characteristics and echocardiographic parameters were analyzed to determine potential risk factors for LV thrombus.
Results
A total of 121 patients met inclusion criteria (age 54.8 ± 15.2 years; female 63.6%; LVEF 26.3 ± 4%). LV thrombus was present in 9 patients (7.4%). Patients with LV thrombus have significantly lower LVEF compared to those without (18.7 ± 3.8% vs 26.9 ± 3.4%, P < .0001). Prevalence of LV thrombus increased as LVEF decreased and was the highest in patients with LVEF < 20%. By univariate analysis, decreased LVEF, particularly LVEF < 20% (OR 36.30, 95% CI 7.35–179.25, P < .0001) and restrictive LV filling pattern (OR 18.13, 95% CI 4.17–78.89, P = .0001) were associated with presence of LV thrombus.
Conclusion
In patients with severely reduced LV systolic function due to chemotherapy-induced cardiomyopathy, LV thrombus was found in 7.4% of subjects. Severely decreased LVEF (<20%) and restrictive LV filling pattern were associated with the presence of LV thrombus.
REFERENCES
- 1Lip GY, Piotrponikowski P, Andreotti F, et al. Thromboembolism and antithrombotic therapy for heart failure in sinus rhythm: an executive summary of a joint consensus document from the ESC Heart Failure Association and the ESC Working Group on Thrombosis. Thromb Haemost. 2012; 108: 1009–1022.
- 2Yancy CW, Jessup M, Bozkurt B, et al. 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2013; 62: e147–e239.
- 3Loh E, Sutton MS, Wun CC, et al. Ventricular dysfunction and the risk of stroke after myocardial infarction. N Engl J Med. 1997; 336: 251–257.
- 4Sharma ND, McCullough PA, Philbin EF, Weaver WD. Left ventricular thrombus and subsequent thromboembolism in patients with severe systolic dysfunction. Chest. 2000; 117: 314–320.
- 5Yeh ET, Bickford CL. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol. 2009; 53: 2231–2247.
- 6Weinsaft JW, Kim HW, Shah DJ, et al. Detection of left ventricular thrombus by delayed-enhancement cardiovascular magnetic resonance prevalence and markers in patients with systolic dysfunction. J Am Coll Cardiol. 2008; 52: 148–157.
- 7Shacham Y, Leshem-Rubinow E, Ben Assa E, et al. Frequency and correlates of early left ventricular thrombus formation following anterior wall acute myocardial infarction treated with primary percutaneous coronary intervention. Am J Cardiol. 2013; 111: 667–670.
- 8Weinsaft JW, Kim HW, Crowley AL, et al. LV thrombus detection by routine echocardiography: insights into performance characteristics using delayed enhancement CMR. JACC Cardiovasc Imaging. 2011; 4: 702–712.
- 9Cardinale D, Colombo A, Lamantia G, et al. Anthracycline-induced cardiomyopathy: clinical relevance and response to pharmacologic therapy. J Am Coll Cardiol. 2010; 55: 213–220.
- 10Lang RM, Bierig M, Devereux RB, et al. Recommendations for chamber quantification: a report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005; 18: 1440–1463.
- 11Nagueh SF, Appleton CP, Gillebert TC, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr. 2009; 22: 107–133.
- 12Pepi M, Evangelista A, Nihoyannopoulos P, et al. Recommendations for echocardiography use in the diagnosis and management of cardiac sources of embolism: European Association of Echocardiography (EAE) (a registered branch of the ESC). Eur J Echocardiogr. 2010; 11: 461–476.
- 13John S, Gottdiener BM, Susan B, , et al. Prevalence of left ventricular thrombus in dilated cardiomyopathy: the WATCH trial. J Am Coll Cardiol 2003; 41: 202.
- 14Kurisu S, Inoue I, Kawagoe T, et al. Incidence and treatment of left ventricular apical thrombosis in Tako-tsubo cardiomyopathy. Int J Cardiol. 2011; 146: e58–e60.
- 15Mansencal N, Nasr IA, Pilliere R, et al. Usefulness of contrast echocardiography for assessment of left ventricular thrombus after acute myocardial infarction. Am J Cardiol. 2007; 99: 1667–1670.
- 16Weinsaft JW, Kim RJ, Ross M, et al. Contrast-enhanced anatomic imaging as compared to contrast-enhanced tissue characterization for detection of left ventricular thrombus. JACC Cardiovasc Imaging. 2009; 2: 969–979.
- 17Kurt M, Shaikh KA, Peterson L, et al. Impact of contrast echocardiography on evaluation of ventricular function and clinical management in a large prospective cohort. J Am Coll Cardiol. 2009; 53: 802–810.
- 18Mulvagh SL, Rakowski H, Vannan MA, et al. American Society of Echocardiography Consensus statement on the clinical applications of ultrasonic contrast agents in echocardiography. J Am Soc Echocardiogr. 2008; 21: 1179–1201; quiz 1281.
- 19Ascione L, Antonini-Canterin F, Macor F, et al. Relation between early mitral regurgitation and left ventricular thrombus formation after acute myocardial infarction: results of the GISSI-3 echo substudy. Heart. 2002; 88: 131–136.
- 20Kalaria VG, Passannante MR, Shah T, Modi K, Weisse AB. Effect of mitral regurgitation on left ventricular thrombus formation in dilated cardiomyopathy. Am Heart J. 1998; 135: 215–220.
- 21Pinamonti B, Zecchin M, Di Lenarda A, et al. Persistence of restrictive left ventricular filling pattern in dilated cardiomyopathy: an ominous prognostic sign. J Am Coll Cardiol. 1997; 29: 604–612.
- 22Doughty RN, Klein AL, Poppe KK, et al. Independence of restrictive filling pattern and LV ejection fraction with mortality in heart failure: an individual patient meta-analysis. Eur J Heart Fail. 2008; 10: 786–792.
- 23Moller JE, Whalley GA, Dini FL, et al. Independent prognostic importance of a restrictive left ventricular filling pattern after myocardial infarction: an individual patient meta-analysis: meta-Analysis Research Group in Echocardiography acute myocardial infarction. Circulation. 2008; 117: 2591–2598.
- 24Celik S, Baykan M, Erdol C, et al. Doppler-derived mitral deceleration time as an early predictor of left ventricular thrombus after first anterior acute myocardial infarction. Am Heart J. 2000; 140: 772–776.
- 25Yilmaz R, Celik S, Baykan M, et al. Assessment of mitral annular velocities by Doppler tissue imaging in predicting left ventricular thrombus formation after first anterior acute myocardial infarction. J Am Soc Echocardiogr. 2005; 18: 632–637.
- 26Lip GY, Gibbs CR. Does heart failure confer a hypercoagulable state? Virchow's triad revisited. J Am Coll Cardiol. 1999; 33: 1424–1426.
- 27Fischer D, Rossa S, Landmesser U, et al. Endothelial dysfunction in patients with chronic heart failure is independently associated with increased incidence of hospitalization, cardiac transplantation, or death. Eur Heart J. 2005; 26: 65–69.
- 28Gibbs CR, Blann AD, Watson RD, Lip GY. Abnormalities of hemorheological, endothelial, and platelet function in patients with chronic heart failure in sinus rhythm: effects of angiotensin-converting enzyme inhibitor and beta-blocker therapy. Circulation. 2001; 103: 1746–1751.
- 29Lip GY, Chin BS, Blann AD. Cancer and the prothrombotic state. Lancet Oncol. 2002; 3: 27–34.
- 30Young A, Chapman O, Connor C, et al. Thrombosis and cancer. Nat Rev Clin Oncol. 2012; 9: 437–449.
- 31Blann AD, Dunmore S. Arterial and venous thrombosis in cancer patients. Cardiol Res Pract. 2011; 2011: 394740.
- 32Schmitt M, Kuhn W, Harbeck N, Graeff H. Thrombophilic state in breast cancer. Semin Thromb Hemost. 1999; 25: 157–166.
- 33Levine M, Hirsh J, Gent M, et al. Double-blind randomised trial of a very-low-dose warfarin for prevention of thromboembolism in stage IV breast cancer. Lancet. 1994; 343: 886–889.
- 34Wada H, Sase T, Yamaguchi M. Hypercoagulant states in malignant lymphoma. Exp Oncol. 2005; 27: 179–185.
- 35Arima H, Inoue D, Tabata S, et al. Simultaneous thrombosis of the mesenteric artery and vein as a novel clinical manifestation of intravascular large B-cell lymphoma. Acta Haematol. 2014; 132: 108–111.
- 36Del Principe MI, Del Principe D, Venditti A. Thrombosis in adult patients with acute leukemia. Curr Opin Oncol. 2017; 29: 448–454.
- 37Athale UH, Chan AK. Thrombosis in children with acute lymphoblastic leukemia: part I. Epidemiology of thrombosis in children with acute lymphoblastic leukemia. Thromb Res. 2003; 111: 125–131.
- 38Khorana AA, Francis CW, Culakova E, et al. Thromboembolism in hospitalized neutropenic cancer patients. J Clin Oncol. 2006; 24: 484–490.
- 39Khorana AA, Francis CW, Blumberg N, et al. Blood transfusions, thrombosis, and mortality in hospitalized patients with cancer. Arch Intern Med. 2008; 168: 2377–2381.
- 40Boles JC, Williams JC, Hollingsworth RM, et al. Anthracycline treatment of the human monocytic leukemia cell line THP-1 increases phosphatidylserine exposure and tissue factor activity. Thromb Res. 2012; 129: 197–203.
- 41Neilan TG, Coelho-Filho OR, Pena-Herrera D, et al. Left ventricular mass in patients with a cardiomyopathy after treatment with anthracyclines. Am J Cardiol. 2012; 110: 1679–1686.
- 42Meyersohn NM, Pursnani A, Neilan TG. Detection of cardiac toxicity due to cancer treatment: role of cardiac mri. Curr Treat Options Cardiovasc Med. 2015; 17: 396.
- 43Bernaba BN, Chan JB, Lai CK, Fishbein MC. Pathology of late-onset anthracycline cardiomyopathy. Cardiovasc Pathol. 2010; 19: 308–311.
- 44Neilan TG, Coelho-Filho OR, Shah RV, et al. Myocardial extracellular volume by cardiac magnetic resonance imaging in patients treated with anthracycline-based chemotherapy. Am J Cardiol. 2013; 111: 717–722.