Skip to main content
Top
Published in: Journal of Cardiovascular Magnetic Resonance 1/2019

Open Access 01-12-2019 | Stem Cell Transplantation | Research

Late effects of pediatric hematopoietic stem cell transplantation on left ventricular function, aortic stiffness and myocardial tissue characteristics

Authors: Elisabeth H. M. Paiman, Marloes Louwerens, Dorine Bresters, Jos J. M. Westenberg, Qian Tao, Rob J. van der Geest, Arjan C. Lankester, Arno A. W. Roest, Hildo J. Lamb

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2019

Login to get access

Abstract

Background

Pediatric hematopoietic stem cell transplantation (HSCT) recipients are at increased risk of cardiovascular disease later in life. As HSCT survival has significantly improved, with a growing number of HSCT indications, tailored screening strategies for HSCT-related late effects are warranted. Little is known regarding the value of cardiovascular magnetic resonance (CMR) for early identification of high-risk patients after HSCT, before symptomatic cardiovascular disease manifests. This study aimed to assess CMR-derived left ventricular (LV) systolic and diastolic function, aortic stiffness and myocardial tissue characteristics in young adults who received HSCT during childhood.

Methods

Sixteen patients (22.1 ± 1.5 years) treated with HSCT during childhood and 16 healthy controls (22.1 ± 1.8 years) underwent 3 T CMR. LV systolic and diastolic function were measured as LV ejection fraction (LVEF), the ratio of transmitral early and late peak filling rate (E/A), the estimated LV filling pressure (E/Ea) and global longitudinal and circumferential systolic strain and diastolic strain rates, using balanced steady-state free precession cine CMR and 2D velocity-encoded CMR over the mitral valve. Aortic stiffness, myocardial fibrosis and steatosis were assessed with 2D velocity-encoded CMR, native T1 mapping and proton CMR spectroscopy (1H-CMRS), respectively.

Results

In the patient compared to the control group, E/Ea (9.92 ± 3.42 vs. 7.24 ± 2.29, P = 0.004) was higher, LVEF (54 ± 6% vs. 58 ± 5%, P = 0.055) and global longitudinal strain (GLS) ( -20.7 ± 3.5% vs. -22.9 ± 3.0%, P = 0.063) tended to be lower, while aortic pulse wave velocity (4.40 ± 0.26 vs. 4.29 ± 0.29 m/s, P = 0.29), native T1 (1211 ± 36 vs. 1227 ± 28 ms, P = 0.16) and myocardial triglyceride content (0.47 ± 0.18 vs. 0.50 ± 0.13%, P = 0.202) were comparable. There were no differences between patients and controls in E/A (2.76 ± 0.92 vs. 2.97 ± 0.91, P = 0.60) and diastolic strain rates.

Conclusion

In young adults who received HSCT during childhood, LV diastolic function was decreased (higher estimated LV filling pressure) and LV systolic function (LVEF and GLS) tended to be reduced as compared to healthy controls, whereas no concomitant differences were found in aortic stiffness and myocardial tissue characteristics. When using CMR, assessment of LV diastolic function in particular is important for early detection of patients at risk of HSCT-related cardiovascular disease, which may warrant closer surveillance.
Literature
1.
go back to reference Uderzo C, Pillon M, Corti P, Tridello G, Tana F, Zintl F, et al. Impact of cumulative anthracycline dose, preparative regimen and chronic graft-versus-host disease on pulmonary and cardiac function in children 5 years after allogeneic hematopoietic stem cell transplantation: a prospective evaluation on behalf of the EBMT pediatric diseases and late effects working parties. Bone Marrow Transplant. 2007;39(11):667–75.CrossRef Uderzo C, Pillon M, Corti P, Tridello G, Tana F, Zintl F, et al. Impact of cumulative anthracycline dose, preparative regimen and chronic graft-versus-host disease on pulmonary and cardiac function in children 5 years after allogeneic hematopoietic stem cell transplantation: a prospective evaluation on behalf of the EBMT pediatric diseases and late effects working parties. Bone Marrow Transplant. 2007;39(11):667–75.CrossRef
2.
go back to reference Lipshultz SE, Adams MJ, Colan SD, Constine LS, Herman EH, Hsu DT, et al. Long-term cardiovascular toxicity in children, adolescents, and young adults who receive cancer therapy: pathophysiology, course, monitoring, management, prevention, and research directions: a scientific statement from the American Heart Association. Circulation. 2013;128(17):1927–95.CrossRef Lipshultz SE, Adams MJ, Colan SD, Constine LS, Herman EH, Hsu DT, et al. Long-term cardiovascular toxicity in children, adolescents, and young adults who receive cancer therapy: pathophysiology, course, monitoring, management, prevention, and research directions: a scientific statement from the American Heart Association. Circulation. 2013;128(17):1927–95.CrossRef
3.
go back to reference Pulte D, Gondos A, Brenner H. Trends in 5- and 10-year survival after diagnosis with childhood hematologic malignancies in the United States, 1990-2004. J Natl Cancer Inst. 2008;100(18):1301–9.CrossRef Pulte D, Gondos A, Brenner H. Trends in 5- and 10-year survival after diagnosis with childhood hematologic malignancies in the United States, 1990-2004. J Natl Cancer Inst. 2008;100(18):1301–9.CrossRef
4.
go back to reference Chima RS, Daniels RC, Kim MO, Li D, Wheeler DS, Davies SM, et al. Improved outcomes for stem cell transplant recipients requiring pediatric intensive care. Pediatr Crit Care Med. 2012;13(6):e336–42.CrossRef Chima RS, Daniels RC, Kim MO, Li D, Wheeler DS, Davies SM, et al. Improved outcomes for stem cell transplant recipients requiring pediatric intensive care. Pediatr Crit Care Med. 2012;13(6):e336–42.CrossRef
5.
go back to reference Niederwieser D, Baldomero H, Szer J, Gratwohl M, Aljurf M, Atsuta Y, et al. Hematopoietic stem cell transplantation activity worldwide in 2012 and a SWOT analysis of the worldwide network for blood and marrow transplantation group including the global survey. Bone Marrow Transplant. 2016;51(6):778–85.CrossRef Niederwieser D, Baldomero H, Szer J, Gratwohl M, Aljurf M, Atsuta Y, et al. Hematopoietic stem cell transplantation activity worldwide in 2012 and a SWOT analysis of the worldwide network for blood and marrow transplantation group including the global survey. Bone Marrow Transplant. 2016;51(6):778–85.CrossRef
6.
go back to reference Battiwalla M, Tichelli A, Majhail NS. Long-term survivorship after hematopoietic cell transplantation: roadmap for research and care. Biol Blood Marrow Transplant. 2017;23(2):184–92.CrossRef Battiwalla M, Tichelli A, Majhail NS. Long-term survivorship after hematopoietic cell transplantation: roadmap for research and care. Biol Blood Marrow Transplant. 2017;23(2):184–92.CrossRef
7.
go back to reference Battiwalla M, Hashmi S, Majhail N, Pavletic S, Savani BN, Shelburne N. National Institutes of Health hematopoietic cell transplantation late effects initiative: developing recommendations to improve survivorship and long-term outcomes. Biol Blood Marrow Transplant. 2017;23(1):6–9.CrossRef Battiwalla M, Hashmi S, Majhail N, Pavletic S, Savani BN, Shelburne N. National Institutes of Health hematopoietic cell transplantation late effects initiative: developing recommendations to improve survivorship and long-term outcomes. Biol Blood Marrow Transplant. 2017;23(1):6–9.CrossRef
8.
go back to reference Armenian SH, Chemaitilly W, Chen M, Chow EJ, Duncan CN, Jones LW, et al. National Institutes of Health hematopoietic cell transplantation late effects initiative: the cardiovascular disease and associated risk factors working group report. Biol Blood Marrow Transplant. 2017;23(2):201–10.CrossRef Armenian SH, Chemaitilly W, Chen M, Chow EJ, Duncan CN, Jones LW, et al. National Institutes of Health hematopoietic cell transplantation late effects initiative: the cardiovascular disease and associated risk factors working group report. Biol Blood Marrow Transplant. 2017;23(2):201–10.CrossRef
9.
go back to reference Pulsipher MA, Skinner R, McDonald GB, Hingorani S, Armenian SH, Cooke KR, et al. National Cancer Institute, National Heart, lung and blood institute/pediatric blood and marrow transplantation consortium first international consensus conference on late effects after pediatric hematopoietic cell transplantation: the need for pediatric-specific long-term follow-up guidelines. Biol Blood Marrow Transplant. 2012;18(3):334–47.CrossRef Pulsipher MA, Skinner R, McDonald GB, Hingorani S, Armenian SH, Cooke KR, et al. National Cancer Institute, National Heart, lung and blood institute/pediatric blood and marrow transplantation consortium first international consensus conference on late effects after pediatric hematopoietic cell transplantation: the need for pediatric-specific long-term follow-up guidelines. Biol Blood Marrow Transplant. 2012;18(3):334–47.CrossRef
10.
go back to reference Chow EJ, Anderson L, Baker KS, Bhatia S, Guilcher GM, Huang JT, et al. Late effects surveillance recommendations among survivors of childhood hematopoietic cell transplantation: a Children’s oncology group report. Biol Blood Marrow Transplant. 2016;22(5):782–95.CrossRef Chow EJ, Anderson L, Baker KS, Bhatia S, Guilcher GM, Huang JT, et al. Late effects surveillance recommendations among survivors of childhood hematopoietic cell transplantation: a Children’s oncology group report. Biol Blood Marrow Transplant. 2016;22(5):782–95.CrossRef
11.
go back to reference Shankar SM, Marina N, Hudson MM, Hodgson DC, Adams MJ, Landier W, et al. Monitoring for cardiovascular disease in survivors of childhood cancer: report from the cardiovascular disease task force of the Children’s oncology group. Pediatrics. 2008;121(2):e387–96.CrossRef Shankar SM, Marina N, Hudson MM, Hodgson DC, Adams MJ, Landier W, et al. Monitoring for cardiovascular disease in survivors of childhood cancer: report from the cardiovascular disease task force of the Children’s oncology group. Pediatrics. 2008;121(2):e387–96.CrossRef
12.
go back to reference Taskinen M, Saarinen-Pihkala UM, Hovi L, Lipsanen-Nyman M. Impaired glucose tolerance and dyslipidaemia as late effects after bone-marrow transplantation in childhood. Lancet. 2000;356(9234):993–7.CrossRef Taskinen M, Saarinen-Pihkala UM, Hovi L, Lipsanen-Nyman M. Impaired glucose tolerance and dyslipidaemia as late effects after bone-marrow transplantation in childhood. Lancet. 2000;356(9234):993–7.CrossRef
13.
go back to reference McEniery CM, Yasmin HIR, Qasem A, Wilkinson IB, Cockcroft JR, et al. Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity: the Anglo-Cardiff Collaborative Trial (ACCT). J Am Coll Cardiol. 2005;46(9):1753–60.CrossRef McEniery CM, Yasmin HIR, Qasem A, Wilkinson IB, Cockcroft JR, et al. Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity: the Anglo-Cardiff Collaborative Trial (ACCT). J Am Coll Cardiol. 2005;46(9):1753–60.CrossRef
14.
go back to reference Terentes-Printzios D, Vlachopoulos C, Xaplanteris P, Ioakeimidis N, Aznaouridis K, Baou K, et al. Cardiovascular risk factors accelerate progression of vascular aging in the general population: results from the CRAVE study (cardiovascular risk factors affecting vascular age). Hypertension. 2017;70(5):1057–64.CrossRef Terentes-Printzios D, Vlachopoulos C, Xaplanteris P, Ioakeimidis N, Aznaouridis K, Baou K, et al. Cardiovascular risk factors accelerate progression of vascular aging in the general population: results from the CRAVE study (cardiovascular risk factors affecting vascular age). Hypertension. 2017;70(5):1057–64.CrossRef
15.
go back to reference Cheung YF, Chan GC, Ha SY. Arterial stiffness and endothelial function in patients with beta-thalassemia major. Circulation. 2002;106(20):2561–6.CrossRef Cheung YF, Chan GC, Ha SY. Arterial stiffness and endothelial function in patients with beta-thalassemia major. Circulation. 2002;106(20):2561–6.CrossRef
16.
go back to reference Ben-Shlomo Y, Spears M, Boustred C, May M, Anderson SG, Benjamin EJ, et al. Aortic pulse wave velocity improves cardiovascular event prediction: an individual participant meta-analysis of prospective observational data from 17,635 subjects. J Am Coll Cardiol. 2014;63(7):636–46.CrossRef Ben-Shlomo Y, Spears M, Boustred C, May M, Anderson SG, Benjamin EJ, et al. Aortic pulse wave velocity improves cardiovascular event prediction: an individual participant meta-analysis of prospective observational data from 17,635 subjects. J Am Coll Cardiol. 2014;63(7):636–46.CrossRef
17.
go back to reference Puntmann VO, Peker E, Chandrashekhar Y, Nagel E. T1 mapping in characterizing myocardial disease: a comprehensive review. Circ Res. 2016;119(2):277–99.CrossRef Puntmann VO, Peker E, Chandrashekhar Y, Nagel E. T1 mapping in characterizing myocardial disease: a comprehensive review. Circ Res. 2016;119(2):277–99.CrossRef
18.
go back to reference Rayner JJ, Banerjee R, Holloway CJ, Lewis AJM, Peterzan MA, Francis JM, et al. The relative contribution of metabolic and structural abnormalities to diastolic dysfunction in obesity. Int J Obes. 2018;42(3):441-7. Rayner JJ, Banerjee R, Holloway CJ, Lewis AJM, Peterzan MA, Francis JM, et al. The relative contribution of metabolic and structural abnormalities to diastolic dysfunction in obesity. Int J Obes. 2018;42(3):441-7.
19.
go back to reference de Heer P, Bizino MB, Versluis MJ, Webb AG, Lamb HJ. Improved cardiac proton magnetic resonance spectroscopy at 3 T using high permittivity pads. Investig Radiol. 2016;51(2):134–8.CrossRef de Heer P, Bizino MB, Versluis MJ, Webb AG, Lamb HJ. Improved cardiac proton magnetic resonance spectroscopy at 3 T using high permittivity pads. Investig Radiol. 2016;51(2):134–8.CrossRef
20.
go back to reference Grotenhuis HB, Westenberg JJ, Steendijk P, van der Geest RJ, Ottenkamp J, Bax JJ, et al. Validation and reproducibility of aortic pulse wave velocity as assessed with velocity-encoded MRI. J Magn Reson Imaging. 2009;30(3):521–6.CrossRef Grotenhuis HB, Westenberg JJ, Steendijk P, van der Geest RJ, Ottenkamp J, Bax JJ, et al. Validation and reproducibility of aortic pulse wave velocity as assessed with velocity-encoded MRI. J Magn Reson Imaging. 2009;30(3):521–6.CrossRef
21.
go back to reference Brandts A, Bertini M, van Dijk EJ, Delgado V, Marsan NA, van der Geest RJ, et al. Left ventricular diastolic function assessment from three-dimensional three-directional velocity-encoded MRI with retrospective valve tracking. J Magn Reson Imaging. 2011;33(2):312–9.CrossRef Brandts A, Bertini M, van Dijk EJ, Delgado V, Marsan NA, van der Geest RJ, et al. Left ventricular diastolic function assessment from three-dimensional three-directional velocity-encoded MRI with retrospective valve tracking. J Magn Reson Imaging. 2011;33(2):312–9.CrossRef
22.
go back to reference de Heer P, Bizino MB, Lamb HJ, Webb AG. Parameter optimization for reproducible cardiac (1) H-MR spectroscopy at 3 tesla. J Magn Reson Imaging. 2016;44(5):1151–8.CrossRef de Heer P, Bizino MB, Lamb HJ, Webb AG. Parameter optimization for reproducible cardiac (1) H-MR spectroscopy at 3 tesla. J Magn Reson Imaging. 2016;44(5):1151–8.CrossRef
23.
go back to reference Ohyama Y, Teixido-Tura G, Ambale-Venkatesh B, Noda C, Chugh AR, Liu CY, et al. Ten-year longitudinal change in aortic stiffness assessed by cardiac MRI in the second half of the human lifespan: the multi-ethnic study of atherosclerosis. Eur Heart J Cardiovasc Imaging. 2016;17(9):1044–53.CrossRef Ohyama Y, Teixido-Tura G, Ambale-Venkatesh B, Noda C, Chugh AR, Liu CY, et al. Ten-year longitudinal change in aortic stiffness assessed by cardiac MRI in the second half of the human lifespan: the multi-ethnic study of atherosclerosis. Eur Heart J Cardiovasc Imaging. 2016;17(9):1044–53.CrossRef
24.
go back to reference van der Meer RW, Rijzewijk LJ, Diamant M, Hammer S, Schar M, Bax JJ, et al. The ageing male heart: myocardial triglyceride content as independent predictor of diastolic function. Eur Heart J. 2008;29(12):1516–22.CrossRef van der Meer RW, Rijzewijk LJ, Diamant M, Hammer S, Schar M, Bax JJ, et al. The ageing male heart: myocardial triglyceride content as independent predictor of diastolic function. Eur Heart J. 2008;29(12):1516–22.CrossRef
25.
go back to reference Roy C, Slimani A, de Meester C, Amzulescu M, Pasquet A, Vancraeynest D, et al. Age and sex corrected normal reference values of T1, T2 T2* and ECV in healthy subjects at 3T CMR. J Cardiovasc Magn Reson. 2017;19(1):72.CrossRef Roy C, Slimani A, de Meester C, Amzulescu M, Pasquet A, Vancraeynest D, et al. Age and sex corrected normal reference values of T1, T2 T2* and ECV in healthy subjects at 3T CMR. J Cardiovasc Magn Reson. 2017;19(1):72.CrossRef
26.
go back to reference Zile MR, Baicu CF, Gaasch WH. Diastolic heart failure--abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med. 2004;350(19):1953–9.CrossRef Zile MR, Baicu CF, Gaasch WH. Diastolic heart failure--abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med. 2004;350(19):1953–9.CrossRef
27.
go back to reference Tassan-Mangina S, Codorean D, Metivier M, Costa B, Himberlin C, Jouannaud C, et al. Tissue Doppler imaging and conventional echocardiography after anthracycline treatment in adults: early and late alterations of left ventricular function during a prospective study. Eur J Echocardiogr. 2006;7(2):141–6.CrossRef Tassan-Mangina S, Codorean D, Metivier M, Costa B, Himberlin C, Jouannaud C, et al. Tissue Doppler imaging and conventional echocardiography after anthracycline treatment in adults: early and late alterations of left ventricular function during a prospective study. Eur J Echocardiogr. 2006;7(2):141–6.CrossRef
28.
go back to reference Nagy AC, Cserep Z, Tolnay E, Nagykalnai T, Forster T. Early diagnosis of chemotherapy-induced cardiomyopathy: a prospective tissue Doppler imaging study. Pathol Oncol Res. 2008;14(1):69–77.CrossRef Nagy AC, Cserep Z, Tolnay E, Nagykalnai T, Forster T. Early diagnosis of chemotherapy-induced cardiomyopathy: a prospective tissue Doppler imaging study. Pathol Oncol Res. 2008;14(1):69–77.CrossRef
29.
go back to reference Ingels NB Jr. Myocardial fiber architecture and left ventricular function. Technol Health Care. 1997;5(1–2):45–52.PubMed Ingels NB Jr. Myocardial fiber architecture and left ventricular function. Technol Health Care. 1997;5(1–2):45–52.PubMed
30.
go back to reference Dorri F, Niederer PF, Lunkenheimer PP, Anderson RH. The architecture of the left ventricular myocytes relative to left ventricular systolic function. Eur J Cardiothorac Surg. 2010;37(2):384–92.PubMed Dorri F, Niederer PF, Lunkenheimer PP, Anderson RH. The architecture of the left ventricular myocytes relative to left ventricular systolic function. Eur J Cardiothorac Surg. 2010;37(2):384–92.PubMed
31.
go back to reference Ong G, Brezden-Masley C, Dhir V, Deva DP, Chan KKW, Chow CM, et al. Myocardial strain imaging by cardiac magnetic resonance for detection of subclinical myocardial dysfunction in breast cancer patients receiving trastuzumab and chemotherapy. Int J Cardiol. 2018. Ong G, Brezden-Masley C, Dhir V, Deva DP, Chan KKW, Chow CM, et al. Myocardial strain imaging by cardiac magnetic resonance for detection of subclinical myocardial dysfunction in breast cancer patients receiving trastuzumab and chemotherapy. Int J Cardiol. 2018.
32.
go back to reference Lunning MA, Kutty S, Rome ET, Li L, Padiyath A, Loberiza F, et al. Cardiac magnetic resonance imaging for the assessment of the myocardium after doxorubicin-based chemotherapy. Am J Clin Oncol. 2015;38(4):377–81.CrossRef Lunning MA, Kutty S, Rome ET, Li L, Padiyath A, Loberiza F, et al. Cardiac magnetic resonance imaging for the assessment of the myocardium after doxorubicin-based chemotherapy. Am J Clin Oncol. 2015;38(4):377–81.CrossRef
33.
go back to reference Hudsmith LE, Neubauer S. Magnetic resonance spectroscopy in myocardial disease. JACC Cardiovasc Imaging. 2009;2(1):87–96.CrossRef Hudsmith LE, Neubauer S. Magnetic resonance spectroscopy in myocardial disease. JACC Cardiovasc Imaging. 2009;2(1):87–96.CrossRef
34.
go back to reference Keltai K, Cervenak L, Mako V, Doleschall Z, Zsary A, Karadi I. Doxorubicin selectively suppresses mRNA expression and production of endothelin-1 in endothelial cells. Vasc Pharmacol. 2010;53(5–6):209–14.CrossRef Keltai K, Cervenak L, Mako V, Doleschall Z, Zsary A, Karadi I. Doxorubicin selectively suppresses mRNA expression and production of endothelin-1 in endothelial cells. Vasc Pharmacol. 2010;53(5–6):209–14.CrossRef
35.
go back to reference Soucy KG, Attarzadeh DO, Ramachandran R, Soucy PA, Romer LH, Shoukas AA, et al. Single exposure to radiation produces early anti-angiogenic effects in mouse aorta. Radiat Environ Biophys. 2010;49(3):397–404.CrossRef Soucy KG, Attarzadeh DO, Ramachandran R, Soucy PA, Romer LH, Shoukas AA, et al. Single exposure to radiation produces early anti-angiogenic effects in mouse aorta. Radiat Environ Biophys. 2010;49(3):397–404.CrossRef
36.
go back to reference Woywodt A, Scheer J, Hambach L, Buchholz S, Ganser A, Haller H, et al. Circulating endothelial cells as a marker of endothelial damage in allogeneic hematopoietic stem cell transplantation. Blood. 2004;103(9):3603–5.CrossRef Woywodt A, Scheer J, Hambach L, Buchholz S, Ganser A, Haller H, et al. Circulating endothelial cells as a marker of endothelial damage in allogeneic hematopoietic stem cell transplantation. Blood. 2004;103(9):3603–5.CrossRef
37.
go back to reference de Witte T. The role of iron in patients after bone marrow transplantation. Blood Rev. 2008;22(Suppl 2):S22–8.CrossRef de Witte T. The role of iron in patients after bone marrow transplantation. Blood Rev. 2008;22(Suppl 2):S22–8.CrossRef
38.
go back to reference Duffy SJ, Biegelsen ES, Holbrook M, Russell JD, Gokce N, Keaney JF Jr, et al. Iron chelation improves endothelial function in patients with coronary artery disease. Circulation. 2001;103(23):2799–804.CrossRef Duffy SJ, Biegelsen ES, Holbrook M, Russell JD, Gokce N, Keaney JF Jr, et al. Iron chelation improves endothelial function in patients with coronary artery disease. Circulation. 2001;103(23):2799–804.CrossRef
39.
go back to reference Chaosuwannakit N, D'Agostino R Jr, Hamilton CA, Lane KS, Ntim WO, Lawrence J, et al. Aortic stiffness increases upon receipt of anthracycline chemotherapy. J Clin Oncol. 2010;28(1):166–72.CrossRef Chaosuwannakit N, D'Agostino R Jr, Hamilton CA, Lane KS, Ntim WO, Lawrence J, et al. Aortic stiffness increases upon receipt of anthracycline chemotherapy. J Clin Oncol. 2010;28(1):166–72.CrossRef
40.
go back to reference Drafts BC, Twomley KM, D'Agostino R Jr, Lawrence J, Avis N, Ellis LR, et al. Low to moderate dose anthracycline-based chemotherapy is associated with early noninvasive imaging evidence of subclinical cardiovascular disease. JACC Cardiovasc Imaging. 2013;6(8):877–85.CrossRef Drafts BC, Twomley KM, D'Agostino R Jr, Lawrence J, Avis N, Ellis LR, et al. Low to moderate dose anthracycline-based chemotherapy is associated with early noninvasive imaging evidence of subclinical cardiovascular disease. JACC Cardiovasc Imaging. 2013;6(8):877–85.CrossRef
41.
go back to reference Turanlahti MI, Taskinen M, Saarinen-Pihkala U, Jokinen EV. Time-related arterial changes after allogeneic hematopoietic stem cell transplantation in children. Pediatr Res. 2013;73(6):777–82.CrossRef Turanlahti MI, Taskinen M, Saarinen-Pihkala U, Jokinen EV. Time-related arterial changes after allogeneic hematopoietic stem cell transplantation in children. Pediatr Res. 2013;73(6):777–82.CrossRef
42.
go back to reference Grover S, Lou PW, Bradbrook C, Cheong K, Kotasek D, Leong DP, et al. Early and late changes in markers of aortic stiffness with breast cancer therapy. Intern Med J. 2015;45(2):140–7.CrossRef Grover S, Lou PW, Bradbrook C, Cheong K, Kotasek D, Leong DP, et al. Early and late changes in markers of aortic stiffness with breast cancer therapy. Intern Med J. 2015;45(2):140–7.CrossRef
43.
go back to reference Jordan JH, Vasu S, Morgan TM, D'Agostino RB Jr, Melendez GC, Hamilton CA, et al. Anthracycline-associated T1 mapping characteristics are elevated independent of the presence of cardiovascular comorbidities in Cancer survivors. Circ Cardiovasc Imaging. 2016;9(8). Jordan JH, Vasu S, Morgan TM, D'Agostino RB Jr, Melendez GC, Hamilton CA, et al. Anthracycline-associated T1 mapping characteristics are elevated independent of the presence of cardiovascular comorbidities in Cancer survivors. Circ Cardiovasc Imaging. 2016;9(8).
44.
go back to reference Neilan TG, Coelho-Filho OR, Shah RV, Feng JH, Pena-Herrera D, Mandry D, et al. Myocardial extracellular volume by cardiac magnetic resonance imaging in patients treated with anthracycline-based chemotherapy. Am J Cardiol. 2013;111(5):717–22.CrossRef Neilan TG, Coelho-Filho OR, Shah RV, Feng JH, Pena-Herrera D, Mandry D, et al. Myocardial extracellular volume by cardiac magnetic resonance imaging in patients treated with anthracycline-based chemotherapy. Am J Cardiol. 2013;111(5):717–22.CrossRef
45.
go back to reference Toro-Salazar OH, Gillan E, O'Loughlin MT, Burke GS, Ferranti J, Stainsby J, et al. Occult cardiotoxicity in childhood cancer survivors exposed to anthracycline therapy. Circ Cardiovasc Imaging. 2013;6(6):873–80.CrossRef Toro-Salazar OH, Gillan E, O'Loughlin MT, Burke GS, Ferranti J, Stainsby J, et al. Occult cardiotoxicity in childhood cancer survivors exposed to anthracycline therapy. Circ Cardiovasc Imaging. 2013;6(6):873–80.CrossRef
46.
go back to reference Tham EB, Haykowsky MJ, Chow K, Spavor M, Kaneko S, Khoo NS, et al. Diffuse myocardial fibrosis by T1-mapping in children with subclinical anthracycline cardiotoxicity: relationship to exercise capacity, cumulative dose and remodeling. J Cardiovasc Magn Reson. 2013;15:48.CrossRef Tham EB, Haykowsky MJ, Chow K, Spavor M, Kaneko S, Khoo NS, et al. Diffuse myocardial fibrosis by T1-mapping in children with subclinical anthracycline cardiotoxicity: relationship to exercise capacity, cumulative dose and remodeling. J Cardiovasc Magn Reson. 2013;15:48.CrossRef
47.
go back to reference Ylanen K, Poutanen T, Savikurki-Heikkila P, Rinta-Kiikka I, Eerola A, Vettenranta K. Cardiac magnetic resonance imaging in the evaluation of the late effects of anthracyclines among long-term survivors of childhood cancer. J Am Coll Cardiol. 2013;61(14):1539–47.CrossRef Ylanen K, Poutanen T, Savikurki-Heikkila P, Rinta-Kiikka I, Eerola A, Vettenranta K. Cardiac magnetic resonance imaging in the evaluation of the late effects of anthracyclines among long-term survivors of childhood cancer. J Am Coll Cardiol. 2013;61(14):1539–47.CrossRef
48.
go back to reference van der Meer RW, Lamb HJ, Smit JW, de Roos A. MR imaging evaluation of cardiovascular risk in metabolic syndrome. Radiology. 2012;264(1):21–37.CrossRef van der Meer RW, Lamb HJ, Smit JW, de Roos A. MR imaging evaluation of cardiovascular risk in metabolic syndrome. Radiology. 2012;264(1):21–37.CrossRef
49.
go back to reference Cavalcante JL, Lima JA, Redheuil A, Al-Mallah MH. Aortic stiffness: current understanding and future directions. J Am Coll Cardiol. 2011;57(14):1511–22.CrossRef Cavalcante JL, Lima JA, Redheuil A, Al-Mallah MH. Aortic stiffness: current understanding and future directions. J Am Coll Cardiol. 2011;57(14):1511–22.CrossRef
Metadata
Title
Late effects of pediatric hematopoietic stem cell transplantation on left ventricular function, aortic stiffness and myocardial tissue characteristics
Authors
Elisabeth H. M. Paiman
Marloes Louwerens
Dorine Bresters
Jos J. M. Westenberg
Qian Tao
Rob J. van der Geest
Arjan C. Lankester
Arno A. W. Roest
Hildo J. Lamb
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2019
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/s12968-018-0513-4

Other articles of this Issue 1/2019

Journal of Cardiovascular Magnetic Resonance 1/2019 Go to the issue