Skip to main content
Top
Published in: Journal of Cardiovascular Magnetic Resonance 1/2017

Open Access 01-12-2017 | Research

Prognostic utility of differential tissue characterization of cardiac neoplasm and thrombus via late gadolinium enhancement cardiovascular magnetic resonance among patients with advanced systemic cancer

Authors: Angel T. Chan, Andrew J. Plodkowski, Shawn C. Pun, Yuliya Lakhman, Darragh F. Halpenny, Jiwon Kim, Samantha R. Goldburg, Mathew J. Matasar, Chaya S. Moskowitz, Dipti Gupta, Richard Steingart, Jonathan W. Weinsaft

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2017

Login to get access

Abstract

Background

Late gadolinium enhancement (LGE-) cardiovascular magnetic resonance (CMR) is well-validated for cardiac mass (CMASS) tissue characterization to differentiate neoplasm (CNEO) from thrombus (CTHR): Prognostic implications of CMASS subtypes among systemic cancer patients are unknown.

Methods

CMASS + patients and controls (CMASS -) matched for cancer diagnosis and stage underwent a standardized CMR protocol, including LGE-CMR (IR-GRE) for tissue characterization and balanced steady state free precession cine-CMR (SSFP) for cardiac structure/function. CMASS subtypes (CNEO, CTHR) were respectively defined by presence or absence of enhancement on LGE-CMR; lesions were quantified for tissue properties (contrast-to-noise ratio (CNR); signal-to-noise ratio (SNR) and size. Clinical follow-up was performed to evaluate prognosis in relation to CMASS etiology.

Results

The study population comprised 126 patients with systemic neoplasms referred for CMR, of whom 50% (n = 63) had CMASS + (CNEO = 32%, CTHR = 18%). Cancer etiology differed between CNEO (sarcoma = 20%, lung = 18%) and CTHR (lymphoma = 30%, GI = 26%); cardiac function (left ventricular ejection fraction: 63 ± 9 vs. 62 ± 10%; p = 0.51∣ right ventricular ejection fraction: 53 ± 9 vs. 54 ± 8%; p = 0.47) and geometric indices were similar (all p = NS). LGE-CMR tissue properties assessed by CNR (13.1 ± 13.0 vs. 1.6 ± 1.0; p < 0.001) and SNR (29.7 ± 20.4 vs. 15.0 ± 11.4, p = 0.003) were higher for CNEO, consistent with visually-assigned diagnostic categories. CTHR were more likely to localize to the right atrium (78% vs. 25%, p < 0.001); nearly all (17/18) were associated with central catheters. Lesion size (17.3 ± 23.8 vs. 2.0 ± 1.5 cm2; p < 0.001) was greater with CNEO vs. CTHR, as was systemic disease burden (cancer-involved organs: 3.6 ± 2.0 vs. 2.3 ± 2.1; p = 0.02). Mortality during a median follow-up of 2.5 years was markedly higher among patients with CNEO compared to those with CTHR (HR = 3.13 [CI 1.54–6.39], p = 0.002); prognosis was similar when patients were stratified by lesion size assessed via area (HR = 0.99 per cm2 [CI 0.98–1.01], p = 0.40) or maximal diameter (HR = 0.98 per cm [CI 0.91–1.06], p = 0.61). CTHR conferred similar mortality risk compared to cancer-matched controls without cardiac involvement (p = 0.64) whereas mortality associated with CNEO was slightly higher albeit non-significant (p = 0.12).

Conclusions

Among a broad cancer cohort with cardiac masses, CNEO defined by LGE-CMR tissue characterization conferred markedly poorer prognosis than CTHR, whereas anatomic assessment via cine-CMR did not stratify mortality risk. Both CNEO and CTHR are associated with similar prognosis compared to CMASS - controls matched for cancer type and disease extent.
Literature
2.
go back to reference Lam KY, Dickens P, Chan AC. Tumors of the heart. A 20-year experience with a review of 12,485 consecutive autopsies. Arch Pathol Lab Med. 1993;117(10):1027–31.PubMed Lam KY, Dickens P, Chan AC. Tumors of the heart. A 20-year experience with a review of 12,485 consecutive autopsies. Arch Pathol Lab Med. 1993;117(10):1027–31.PubMed
3.
go back to reference Pun SC, Plodkowski A, Matasar MJ, Lakhman Y, Halpenny DF, Gupta D, Moskowitz C, Kim J, Steingart R, Weinsaft JW. Pattern and prognostic implications of cardiac metastases among patients with advanced systemic cancer assessed with cardiac magnetic resonance imaging. J Am Heart Assoc. 2016;5(5):e003368.CrossRefPubMedPubMedCentral Pun SC, Plodkowski A, Matasar MJ, Lakhman Y, Halpenny DF, Gupta D, Moskowitz C, Kim J, Steingart R, Weinsaft JW. Pattern and prognostic implications of cardiac metastases among patients with advanced systemic cancer assessed with cardiac magnetic resonance imaging. J Am Heart Assoc. 2016;5(5):e003368.CrossRefPubMedPubMedCentral
4.
go back to reference Lee AYY, Levine MN, Butler G, Webb C, Costantini L, Gu C, Julian JA. Incidence, risk factors, and outcomes of catheter-related thrombosis in adult patients with cancer. J Clin Oncol. 2006;24(9):1404–8.CrossRefPubMed Lee AYY, Levine MN, Butler G, Webb C, Costantini L, Gu C, Julian JA. Incidence, risk factors, and outcomes of catheter-related thrombosis in adult patients with cancer. J Clin Oncol. 2006;24(9):1404–8.CrossRefPubMed
5.
go back to reference Luciani A, Clement O, Halimi P, Goudot D, Portier F, Bassot V, Luciani J-A, Avan P, Frija G, Bonfils P. Catheter-related upper extremity deep venous thrombosis in cancer patients: a prospective study based on Doppler US. Radiology. 2001;220(3):655–60.CrossRefPubMed Luciani A, Clement O, Halimi P, Goudot D, Portier F, Bassot V, Luciani J-A, Avan P, Frija G, Bonfils P. Catheter-related upper extremity deep venous thrombosis in cancer patients: a prospective study based on Doppler US. Radiology. 2001;220(3):655–60.CrossRefPubMed
6.
go back to reference Weinsaft JW, Kim HW, Crowley AL, Klem I, Shenoy C, Van Assche L, Brosnan R, Shah DJ, Velazquez EJ, Parker M, et al. LV thrombus detection by routine echocardiography: insights into performance characteristics using delayed enhancement CMR. JACC Cardiovascular imaging. 2011;4(7):702–12.CrossRefPubMedPubMedCentral Weinsaft JW, Kim HW, Crowley AL, Klem I, Shenoy C, Van Assche L, Brosnan R, Shah DJ, Velazquez EJ, Parker M, et al. LV thrombus detection by routine echocardiography: insights into performance characteristics using delayed enhancement CMR. JACC Cardiovascular imaging. 2011;4(7):702–12.CrossRefPubMedPubMedCentral
7.
go back to reference Weinsaft JW, Kim HW, Shah DJ, Klem I, Crowley AL, Brosnan R, James OG, Patel MR, Heitner J, Parker M, et al. Detection of left ventricular thrombus by delayed-enhancement cardiovascular magnetic ResonancePrevalence and markers in patients with systolic dysfunction. J Am Coll Cardiol. 2008;52(2):148–57.CrossRefPubMed Weinsaft JW, Kim HW, Shah DJ, Klem I, Crowley AL, Brosnan R, James OG, Patel MR, Heitner J, Parker M, et al. Detection of left ventricular thrombus by delayed-enhancement cardiovascular magnetic ResonancePrevalence and markers in patients with systolic dysfunction. J Am Coll Cardiol. 2008;52(2):148–57.CrossRefPubMed
8.
go back to reference Weinsaft JW, Kim RJ, Ross M, Krauser D, Manoushagian S, LaBounty TM, Cham MD, Min JK, Healy K, Wang Y, et al. Contrast-enhanced anatomic imaging as compared to contrast-enhanced tissue characterization for detection of left ventricular thrombus. JACC Cardiovascular imaging. 2009;2(8):969–79.CrossRefPubMedPubMedCentral Weinsaft JW, Kim RJ, Ross M, Krauser D, Manoushagian S, LaBounty TM, Cham MD, Min JK, Healy K, Wang Y, et al. Contrast-enhanced anatomic imaging as compared to contrast-enhanced tissue characterization for detection of left ventricular thrombus. JACC Cardiovascular imaging. 2009;2(8):969–79.CrossRefPubMedPubMedCentral
9.
go back to reference Srichai MB, Junor C, Rodriguez LL, Stillman AE, Grimm RA, Lieber ML, Weaver JA, Smedira NG, White RD. Clinical, imaging, and pathological characteristics of left ventricular thrombus: a comparison of contrast-enhanced magnetic resonance imaging, transthoracic echocardiography, and transesophageal echocardiography with surgical or pathological validation. Am Heart J. 2006;152(1):75–84.CrossRefPubMed Srichai MB, Junor C, Rodriguez LL, Stillman AE, Grimm RA, Lieber ML, Weaver JA, Smedira NG, White RD. Clinical, imaging, and pathological characteristics of left ventricular thrombus: a comparison of contrast-enhanced magnetic resonance imaging, transthoracic echocardiography, and transesophageal echocardiography with surgical or pathological validation. Am Heart J. 2006;152(1):75–84.CrossRefPubMed
10.
go back to reference Gerdan L, Segedin B, Veninga T, Schild SE, Rades D. Number of involved extracranial organs predicts survival in patients with brain metastasis from small cell lung cancer. Anticancer Res. 2013;33(9):3887–9.PubMed Gerdan L, Segedin B, Veninga T, Schild SE, Rades D. Number of involved extracranial organs predicts survival in patients with brain metastasis from small cell lung cancer. Anticancer Res. 2013;33(9):3887–9.PubMed
11.
go back to reference Hendriks LE, Derks JL, Postmus PE, Damhuis RA, Houben RM, Troost EG, Hochstenbag MM, Smit EF, Dingemans AM. Single organ metastatic disease and local disease status, prognostic factors for overall survival in stage IV non-small cell lung cancer: results from a population-based study. European journal of cancer (Oxford, England : 1990). 2015;51(17):2534–44.CrossRef Hendriks LE, Derks JL, Postmus PE, Damhuis RA, Houben RM, Troost EG, Hochstenbag MM, Smit EF, Dingemans AM. Single organ metastatic disease and local disease status, prognostic factors for overall survival in stage IV non-small cell lung cancer: results from a population-based study. European journal of cancer (Oxford, England : 1990). 2015;51(17):2534–44.CrossRef
12.
go back to reference Nakazawa K, Kurishima K, Tamura T, Kagohashi K, Ishikawa H, Satoh H, Hizawa N. Specific organ metastases and survival in small cell lung cancer. Oncol Lett. 2012;4(4):617–20.PubMedPubMedCentral Nakazawa K, Kurishima K, Tamura T, Kagohashi K, Ishikawa H, Satoh H, Hizawa N. Specific organ metastases and survival in small cell lung cancer. Oncol Lett. 2012;4(4):617–20.PubMedPubMedCentral
13.
go back to reference Kirkpatrick JN, Wong T, Bednarz JE, Spencer KT, Sugeng L, Ward RP, DeCara JM, Weinert L, Krausz T, Lang RM. Differential diagnosis of cardiac masses using contrast echocardiographic perfusion imaging. J Am Coll Cardiol. 2004;43(8):1412–9.CrossRefPubMed Kirkpatrick JN, Wong T, Bednarz JE, Spencer KT, Sugeng L, Ward RP, DeCara JM, Weinert L, Krausz T, Lang RM. Differential diagnosis of cardiac masses using contrast echocardiographic perfusion imaging. J Am Coll Cardiol. 2004;43(8):1412–9.CrossRefPubMed
14.
15.
go back to reference Kim KJ, Li B, Winer J, Armanini M, Gillett N, Phillips HS, Ferrara N. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature. 1993;362(6423):841–4.CrossRefPubMed Kim KJ, Li B, Winer J, Armanini M, Gillett N, Phillips HS, Ferrara N. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature. 1993;362(6423):841–4.CrossRefPubMed
16.
go back to reference O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997;88(2):277–85.CrossRefPubMed O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997;88(2):277–85.CrossRefPubMed
17.
go back to reference Gabata T, Matsui O, Kadoya M, Yoshikawa J, Ueda K, Kawamori Y, Takashima T, Nonomura A. Delayed MR imaging of the liver: correlation of delayed enhancement of hepatic tumors and pathologic appearance. Abdom Imaging. 1998;23(3):309–13.CrossRefPubMed Gabata T, Matsui O, Kadoya M, Yoshikawa J, Ueda K, Kawamori Y, Takashima T, Nonomura A. Delayed MR imaging of the liver: correlation of delayed enhancement of hepatic tumors and pathologic appearance. Abdom Imaging. 1998;23(3):309–13.CrossRefPubMed
18.
go back to reference Shimizu S, Eguchi Y, Kamiike W, Itoh Y, Hasegawa J, Yamabe K, Otsuki Y, Matsuda H, Tsujimoto Y. Induction of apoptosis as well as necrosis by hypoxia and predominant prevention of apoptosis by Bcl-2 and Bcl-XL. Cancer Res. 1996;56(9):2161–6.PubMed Shimizu S, Eguchi Y, Kamiike W, Itoh Y, Hasegawa J, Yamabe K, Otsuki Y, Matsuda H, Tsujimoto Y. Induction of apoptosis as well as necrosis by hypoxia and predominant prevention of apoptosis by Bcl-2 and Bcl-XL. Cancer Res. 1996;56(9):2161–6.PubMed
19.
go back to reference Tomes L, Emberley E, Niu Y, Troup S, Pastorek J, Strange K, Harris A, Watson PH. Necrosis and hypoxia in invasive breast carcinoma. Breast Cancer Res Treat. 2003;81(1):61–9.CrossRefPubMed Tomes L, Emberley E, Niu Y, Troup S, Pastorek J, Strange K, Harris A, Watson PH. Necrosis and hypoxia in invasive breast carcinoma. Breast Cancer Res Treat. 2003;81(1):61–9.CrossRefPubMed
20.
go back to reference Poss J, Desch S, Eitel C, de Waha S, Thiele H, Eitel I. Left ventricular thrombus formation after ST-segment-elevation myocardial infarction: insights from a cardiac magnetic resonance multicenter study. Circ Cardiovasc Imaging. 2015;8(10):e003417.PubMed Poss J, Desch S, Eitel C, de Waha S, Thiele H, Eitel I. Left ventricular thrombus formation after ST-segment-elevation myocardial infarction: insights from a cardiac magnetic resonance multicenter study. Circ Cardiovasc Imaging. 2015;8(10):e003417.PubMed
Metadata
Title
Prognostic utility of differential tissue characterization of cardiac neoplasm and thrombus via late gadolinium enhancement cardiovascular magnetic resonance among patients with advanced systemic cancer
Authors
Angel T. Chan
Andrew J. Plodkowski
Shawn C. Pun
Yuliya Lakhman
Darragh F. Halpenny
Jiwon Kim
Samantha R. Goldburg
Mathew J. Matasar
Chaya S. Moskowitz
Dipti Gupta
Richard Steingart
Jonathan W. Weinsaft
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2017
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/s12968-017-0390-2

Other articles of this Issue 1/2017

Journal of Cardiovascular Magnetic Resonance 1/2017 Go to the issue