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

Open Access 01-12-2017 | Research

Histological validation of cardiovascular magnetic resonance T1 mapping markers of myocardial fibrosis in paediatric heart transplant recipients

Authors: Seiko Ide, Eugenie Riesenkampff, David A. Chiasson, Anne I. Dipchand, Paul F. Kantor, Rajiv R. Chaturvedi, Shi-Joon Yoo, Lars Grosse-Wortmann

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

Login to get access

Abstract

Background

Adverse fibrotic remodeling is detrimental to myocardial health and a reliable method for monitoring the development of fibrotic remodeling may be desirable during the follow-up of patients after heart transplantation (HTx). Quantification of diffuse myocardial fibrosis with cardiovascular magnetic resonance (CMR) has been increasingly applied and validated histologically in adult patients with heart disease. However, comparisons of CMR findings with histological fibrosis burden in children are lacking. This study aimed to compare native T1 times and extracellular volume fraction (ECV) derived from CMR with the degree of collagen on endomyocardial biopsy (EmBx), and to investigate the association between myocardial fibrosis and clinical as well as functional markers in children after HTx.

Methods

EmBx and CMR were performed on the same day. All specimens were stained with picrosirius red. The collagen volume fraction (CVF) was calculated as ratio of stained collagen area to total myocardial area on EmBx. Native T1 values and ECV were measured by CMR on a mid-ventricular short axis slice, using a modified look-locker inversion recovery approach.

Results

Twenty patients (9.9 ± 6.2 years of age; 9 girls) after HTx were prospectively enrolled, at a median of 1.3 years (0.02–12.6 years) post HTx, and compared to 24 controls (13.9 ± 2.6 years of age; 12 girls). The mean histological CVF was 10.0 ± 3.4%. Septal native T1 times and ECV were higher in HTx patients compared to controls (1008 ± 32 ms vs 979 ± 24 ms, p < 0.005 and 0.30 ± 0.03 vs 0.22 ± 0.03, p < 0.0001, respectively). CVF showed a moderate correlation with native T1 (r = 0.53, p < 0.05) as well as ECV (r = 0.46, p < 0.05). Native T1 time, but not ECV and CVF, correlated with ischemia time (r = 0.46, p < 0.05).

Conclusions

CMR-derived fibrosis markers correlate with histological degree of fibrosis on EmBx in children after HTx. Further, native T1 times are associated with longer ischemia times.
Appendix
Available only for authorised users
Literature
1.
go back to reference Dipchand AI, Kirk R, Mahle WT, Tresler MA, Naftel DC, Pahl E, et al. Ten yr of pediatric heart transplantation: a report from the pediatric heart transplant study. Pediatr Transplant. 2013;17:99–111.CrossRefPubMed Dipchand AI, Kirk R, Mahle WT, Tresler MA, Naftel DC, Pahl E, et al. Ten yr of pediatric heart transplantation: a report from the pediatric heart transplant study. Pediatr Transplant. 2013;17:99–111.CrossRefPubMed
2.
go back to reference Dipchand AI, Rossano JW, Edwards LB, Kucheryavaya AY, Benden C, Goldfarb S, et al. The registry of the international society for heart and lung transplantation: eighteenth official pediatric heart transplantation report—2015; focus theme: early graft failure. J Hear Lung Transplant. 2015;34:1233–43.CrossRef Dipchand AI, Rossano JW, Edwards LB, Kucheryavaya AY, Benden C, Goldfarb S, et al. The registry of the international society for heart and lung transplantation: eighteenth official pediatric heart transplantation report—2015; focus theme: early graft failure. J Hear Lung Transplant. 2015;34:1233–43.CrossRef
3.
go back to reference Hiemann N, Wellnhofer E, Lehmkuhl H, Knosalla C, Hetzer R, Meyer R. Everolimus prevents endomyocardial remodeling after heart transplantation. Transplantation. 2011;92:1165–72.CrossRefPubMed Hiemann N, Wellnhofer E, Lehmkuhl H, Knosalla C, Hetzer R, Meyer R. Everolimus prevents endomyocardial remodeling after heart transplantation. Transplantation. 2011;92:1165–72.CrossRefPubMed
4.
go back to reference Yamani MH, Haji SA, Starling RC, Tuzcu EM, Ratliff NB, Cook DJ, et al. Myocardial ischemic-fibrotic injury after human heart transplantation is associated with increased progression of vasculopathy, decreased cellular rejection and poor long-term outcome. J Am Coll Cardiol. 2002;39:970–7.CrossRefPubMed Yamani MH, Haji SA, Starling RC, Tuzcu EM, Ratliff NB, Cook DJ, et al. Myocardial ischemic-fibrotic injury after human heart transplantation is associated with increased progression of vasculopathy, decreased cellular rejection and poor long-term outcome. J Am Coll Cardiol. 2002;39:970–7.CrossRefPubMed
5.
go back to reference Pichler M, Rainer PP, Schauer S, Hoefler G. Cardiac fibrosis in human transplanted hearts is mainly driven by cells of intracardiac origin. J Am Coll Cardiol. 2012;59:1008–16.CrossRefPubMed Pichler M, Rainer PP, Schauer S, Hoefler G. Cardiac fibrosis in human transplanted hearts is mainly driven by cells of intracardiac origin. J Am Coll Cardiol. 2012;59:1008–16.CrossRefPubMed
6.
go back to reference Perens G, Li F, Meier S, Kaur R, Alejos J, Fishbein M. Clinico-pathologic findings in end-stage pediatric heart transplant grafts. Pediatr Transplant. 2009;13:887–91.CrossRefPubMed Perens G, Li F, Meier S, Kaur R, Alejos J, Fishbein M. Clinico-pathologic findings in end-stage pediatric heart transplant grafts. Pediatr Transplant. 2009;13:887–91.CrossRefPubMed
7.
go back to reference Skowronski EW, Epstein M, Ota D, Hoagland PM, Gordon JB, Adamson RM, et al. Right and left ventricular function after cardiac transplantation. Changes during and after rejection. Circulation. 1991;84:2409–17.CrossRefPubMed Skowronski EW, Epstein M, Ota D, Hoagland PM, Gordon JB, Adamson RM, et al. Right and left ventricular function after cardiac transplantation. Changes during and after rejection. Circulation. 1991;84:2409–17.CrossRefPubMed
8.
go back to reference Mann DL, Bristow MR. Mechanisms and models in heart failure: the biomechanical model and beyond. Circulation. 2005;111:2837–49.CrossRefPubMed Mann DL, Bristow MR. Mechanisms and models in heart failure: the biomechanical model and beyond. Circulation. 2005;111:2837–49.CrossRefPubMed
9.
go back to reference Berk B, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Investigation. 2007;117:568–75.CrossRef Berk B, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Investigation. 2007;117:568–75.CrossRef
10.
go back to reference Kobashigawa JA, Itagaki BK, Razi RR, Patel JK, Chai W, Kawano MA, et al. Correlation between myocardial fibrosis and restrictive cardiac physiology in patients undergoing retransplantation. Clin Transplant. 2013;27:679–84.CrossRef Kobashigawa JA, Itagaki BK, Razi RR, Patel JK, Chai W, Kawano MA, et al. Correlation between myocardial fibrosis and restrictive cardiac physiology in patients undergoing retransplantation. Clin Transplant. 2013;27:679–84.CrossRef
11.
go back to reference Butler CR, Kumar A, Toma M, Thompson R, Chow K, Isaac D, et al. Late gadolinium enhancement in cardiac transplant patients is associated with adverse ventricular functional parameters and clinical outcomes. Can J Cardiol. 2013;29:1076–83.CrossRefPubMed Butler CR, Kumar A, Toma M, Thompson R, Chow K, Isaac D, et al. Late gadolinium enhancement in cardiac transplant patients is associated with adverse ventricular functional parameters and clinical outcomes. Can J Cardiol. 2013;29:1076–83.CrossRefPubMed
12.
go back to reference Kozak M, Redington A, Yoo S-J, Seed M, Greiser A, Grosse-Wortmann L. Diffuse myocardial fibrosis following tetralogy of Fallot repair: a T1 mapping cardiac magnetic resonance study. Pediatr Radiol. 2014;44:403–9.CrossRefPubMed Kozak M, Redington A, Yoo S-J, Seed M, Greiser A, Grosse-Wortmann L. Diffuse myocardial fibrosis following tetralogy of Fallot repair: a T1 mapping cardiac magnetic resonance study. Pediatr Radiol. 2014;44:403–9.CrossRefPubMed
13.
go back to reference Dusenbery SM, Jerosch-Herold M, Rickers C, Colan SD, Geva T, Newburger JW, et al. Myocardial extracellular remodeling is associated with ventricular diastolic dysfunction in children and young adults with congenital aortic stenosis. J Am Coll Cardiol. 2014;63:1778–85.CrossRefPubMed Dusenbery SM, Jerosch-Herold M, Rickers C, Colan SD, Geva T, Newburger JW, et al. Myocardial extracellular remodeling is associated with ventricular diastolic dysfunction in children and young adults with congenital aortic stenosis. J Am Coll Cardiol. 2014;63:1778–85.CrossRefPubMed
14.
go back to reference Moon JC, Messroghli DR, Kellman P, Piechnik SK, Robson MD, Ugander M, et al. Myocardial T1 mapping and extracellular volume quantification: a Society for Cardiovascular Magnetic Resonance (SCMR) and CMR Working Group of the European Society of Cardiology consensus statement. J Cardiovasc Magn Reson. 2013;15:92.CrossRefPubMedPubMedCentral Moon JC, Messroghli DR, Kellman P, Piechnik SK, Robson MD, Ugander M, et al. Myocardial T1 mapping and extracellular volume quantification: a Society for Cardiovascular Magnetic Resonance (SCMR) and CMR Working Group of the European Society of Cardiology consensus statement. J Cardiovasc Magn Reson. 2013;15:92.CrossRefPubMedPubMedCentral
15.
go back to reference Flacke SJ, Fischer SE, Lorenz CH. Measurement of the gadopentetate dimeglumine partition coefficient in human myocardium in vivo: normal distribution and elevation in acute and chronic infarction. Radiology. 2001;218:703–10.CrossRefPubMed Flacke SJ, Fischer SE, Lorenz CH. Measurement of the gadopentetate dimeglumine partition coefficient in human myocardium in vivo: normal distribution and elevation in acute and chronic infarction. Radiology. 2001;218:703–10.CrossRefPubMed
16.
go back to reference Flett AS, Hayward MP, Ashworth MT, Hansen MS, Taylor AM, Elliott PM, et al. Equilibrium contrast cardiovascular magnetic resonance for the measurement of diffuse myocardial fibrosis: preliminary validation in humans. Circulation. 2010;122:138–44.CrossRefPubMed Flett AS, Hayward MP, Ashworth MT, Hansen MS, Taylor AM, Elliott PM, et al. Equilibrium contrast cardiovascular magnetic resonance for the measurement of diffuse myocardial fibrosis: preliminary validation in humans. Circulation. 2010;122:138–44.CrossRefPubMed
17.
go back to reference Riesenkampff E, Chen CK, Kantor PF, Greenway S, Chaturvedi RR, Yoo SJ, et al. Diffuse myocardial fibrosis in children after heart transplantations: a magnetic resonance T1 mapping study. Transplantation. 2015;99:2656–62.CrossRefPubMed Riesenkampff E, Chen CK, Kantor PF, Greenway S, Chaturvedi RR, Yoo SJ, et al. Diffuse myocardial fibrosis in children after heart transplantations: a magnetic resonance T1 mapping study. Transplantation. 2015;99:2656–62.CrossRefPubMed
18.
go back to reference Miller CA, Sarma J, Naish JH, Yonan N, Williams SG, Shaw SM, et al. Multiparametric cardiovascular magnetic resonance assessment of cardiac allograft vasculopathy. J Am Coll Cardiol. 2014;63:799–808.CrossRefPubMed Miller CA, Sarma J, Naish JH, Yonan N, Williams SG, Shaw SM, et al. Multiparametric cardiovascular magnetic resonance assessment of cardiac allograft vasculopathy. J Am Coll Cardiol. 2014;63:799–808.CrossRefPubMed
19.
go back to reference Ellims AH, Shaw JA, Stub D, Iles LM, Hare JL, Slavin GS, et al. Diffuse myocardial fibrosis evaluated by post-contrast T1 mapping correlates with left ventricular stiffness. J Am Coll Cardiol. 2014;63:1112–8.CrossRefPubMed Ellims AH, Shaw JA, Stub D, Iles LM, Hare JL, Slavin GS, et al. Diffuse myocardial fibrosis evaluated by post-contrast T1 mapping correlates with left ventricular stiffness. J Am Coll Cardiol. 2014;63:1112–8.CrossRefPubMed
20.
go back to reference Coelho-Filho OR, Shah R, Lavagnoli CF, Barros JC, Neilan TG, Murthy VL, et al. Myocardial tissue remodeling after orthotopic heart transplantation: a pilot cardiac magnetic resonance study. Int J Cardiovasc Imaging. 2016. doi:10.1007/s10554-016-0937-6. Coelho-Filho OR, Shah R, Lavagnoli CF, Barros JC, Neilan TG, Murthy VL, et al. Myocardial tissue remodeling after orthotopic heart transplantation: a pilot cardiac magnetic resonance study. Int J Cardiovasc Imaging. 2016. doi:10.​1007/​s10554-016-0937-6.
21.
go back to reference Bull S, White SK, Piechnik SK, Flett AS, Ferreira VM, Loudon M, et al. Human non-contrast T1 values and correlation with histology in diffuse fibrosis. Heart. 2013;99:932–7.CrossRefPubMedPubMedCentral Bull S, White SK, Piechnik SK, Flett AS, Ferreira VM, Loudon M, et al. Human non-contrast T1 values and correlation with histology in diffuse fibrosis. Heart. 2013;99:932–7.CrossRefPubMedPubMedCentral
22.
go back to reference Sibley CT, Noureldin RA, Gai N, Nacif MS, Liu S, Turkbey EB, et al. T1 mapping in cardiomyopathy at cardiac MR: comparison with endomyocardial biopsy. Radiology. 2012;265:724–32.CrossRefPubMedPubMedCentral Sibley CT, Noureldin RA, Gai N, Nacif MS, Liu S, Turkbey EB, et al. T1 mapping in cardiomyopathy at cardiac MR: comparison with endomyocardial biopsy. Radiology. 2012;265:724–32.CrossRefPubMedPubMedCentral
23.
go back to reference de Meester de Ravenstein C, Bouzin C, Lazam S, Boulif J, Amzulescu M, Melchior J, et al. Histological validation of measurement of diffuse interstitial myocardial fibrosis by myocardial extravascular volume fraction from Modified Look-Locker imaging (MOLLI) T1 mapping at 3 T. J Cardiovasc Magn Reson. 2015;17:1–11.CrossRef de Meester de Ravenstein C, Bouzin C, Lazam S, Boulif J, Amzulescu M, Melchior J, et al. Histological validation of measurement of diffuse interstitial myocardial fibrosis by myocardial extravascular volume fraction from Modified Look-Locker imaging (MOLLI) T1 mapping at 3 T. J Cardiovasc Magn Reson. 2015;17:1–11.CrossRef
24.
go back to reference Miller CA, Naish JH, Bishop P, Coutts G, Clark D, Zhao S, et al. Comprehensive validation of cardiovascular magnetic resonance techniques for the assessment of myocardial extracellular volume. Circ Cardiovasc Imaging. 2013;6:373–83.CrossRefPubMed Miller CA, Naish JH, Bishop P, Coutts G, Clark D, Zhao S, et al. Comprehensive validation of cardiovascular magnetic resonance techniques for the assessment of myocardial extracellular volume. Circ Cardiovasc Imaging. 2013;6:373–83.CrossRefPubMed
25.
go back to reference Lee SP, Lee W, Lee JM, Park EA, Kim HK, Kim YJ, et al. Assessment of diffuse myocardial fibrosis by using MR imaging in asymptomatic patients with aortic stenosis. Radiology. 2015;274:359–69.CrossRefPubMed Lee SP, Lee W, Lee JM, Park EA, Kim HK, Kim YJ, et al. Assessment of diffuse myocardial fibrosis by using MR imaging in asymptomatic patients with aortic stenosis. Radiology. 2015;274:359–69.CrossRefPubMed
26.
go back to reference Ausdem Siepen F, Buss SJ, Messroghli D, Andre F, Lossnitzer D, Seitz S, et al. T1 mapping in dilated cardiomyopathy with cardiac magnetic resonance: quantification of diffuse myocardial fibrosis and comparison with endomyocardial biopsy. Eur Heart J Cardiovasc Imaging. 2015;16:210–6.CrossRef Ausdem Siepen F, Buss SJ, Messroghli D, Andre F, Lossnitzer D, Seitz S, et al. T1 mapping in dilated cardiomyopathy with cardiac magnetic resonance: quantification of diffuse myocardial fibrosis and comparison with endomyocardial biopsy. Eur Heart J Cardiovasc Imaging. 2015;16:210–6.CrossRef
27.
go back to reference Wong TC, Piehler K, Meier CG, Testa SM, Klock AM, Aneizi AA, et al. Association between extracellular matrix expansion quantified by cardiovascular magnetic resonance and short-term mortality. Circulation. 2012;126:1206–16.CrossRefPubMedPubMedCentral Wong TC, Piehler K, Meier CG, Testa SM, Klock AM, Aneizi AA, et al. Association between extracellular matrix expansion quantified by cardiovascular magnetic resonance and short-term mortality. Circulation. 2012;126:1206–16.CrossRefPubMedPubMedCentral
28.
go back to reference Schelbert EB, Piehler KM, Zareba KM, Moon JC, Ugander M, Messroghli DR, et al. Myocardial fibrosis quantified by extracellular volume is associated with subsequent hospitalization for heart failure, death, or both across the spectrum of ejection fraction and heart failure stage. J Am Heart Assoc. 2015. doi:10.1161/JAHA.115.002613. Schelbert EB, Piehler KM, Zareba KM, Moon JC, Ugander M, Messroghli DR, et al. Myocardial fibrosis quantified by extracellular volume is associated with subsequent hospitalization for heart failure, death, or both across the spectrum of ejection fraction and heart failure stage. J Am Heart Assoc. 2015. doi:10.​1161/​JAHA.​115.​002613.
29.
go back to reference Grosse-Wortmann L, Roche S, Yoo S-J, Seed M, Kantor P. Early changes in right ventricular function and their clinical consequences in childhood and adolescent dilated cardiomyopathy. Cardiol Young. 2010;20:418–25.CrossRefPubMed Grosse-Wortmann L, Roche S, Yoo S-J, Seed M, Kantor P. Early changes in right ventricular function and their clinical consequences in childhood and adolescent dilated cardiomyopathy. Cardiol Young. 2010;20:418–25.CrossRefPubMed
30.
go back to reference Messroghli D, Radjenovic A, Kozerke S, Higgins D, Sivananthan M, Ridgway J. Modified look-locker inversion recovery (MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med. 2004;52:141–6.CrossRefPubMed Messroghli D, Radjenovic A, Kozerke S, Higgins D, Sivananthan M, Ridgway J. Modified look-locker inversion recovery (MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med. 2004;52:141–6.CrossRefPubMed
31.
go back to reference Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, et al. Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart. A statement for healthcare professionals from the cardiac imaging committee of the council on Clinical Cardiology of the American Heart Association. Int J Cardiovasc Imaging. 2002;18:539–42.PubMed Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, et al. Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart. A statement for healthcare professionals from the cardiac imaging committee of the council on Clinical Cardiology of the American Heart Association. Int J Cardiovasc Imaging. 2002;18:539–42.PubMed
32.
go back to reference Orwat S, Diller GP, Kempny A, Radke R, Peters B, Kuhne T, et al. Myocardial deformation parameters predict outcome in patients with repaired tetralogy of Fallot. Heart. 2016;102:209–15.CrossRefPubMed Orwat S, Diller GP, Kempny A, Radke R, Peters B, Kuhne T, et al. Myocardial deformation parameters predict outcome in patients with repaired tetralogy of Fallot. Heart. 2016;102:209–15.CrossRefPubMed
33.
go back to reference Hundley WG, Bluemke D, Bogaert JG, Friedrich MG, Higgins CB, Lawson MA, et al. Society for cardiovascular magnetic resonance guidelines for reporting cardiovascular magnetic resonance examinations. J Cardiovasc Magn Reson. 2009;11:5.CrossRefPubMedPubMedCentral Hundley WG, Bluemke D, Bogaert JG, Friedrich MG, Higgins CB, Lawson MA, et al. Society for cardiovascular magnetic resonance guidelines for reporting cardiovascular magnetic resonance examinations. J Cardiovasc Magn Reson. 2009;11:5.CrossRefPubMedPubMedCentral
34.
go back to reference Hadi AM, Mouchaers KT, Schalij I, Grunberg K, Meijer GA, Vonk-Noordegraaf A, et al. Rapid quantification of myocardial fibrosis: a new macro-based automated analysis. Cell Oncol (Dordr). 2011;34:343–54.CrossRef Hadi AM, Mouchaers KT, Schalij I, Grunberg K, Meijer GA, Vonk-Noordegraaf A, et al. Rapid quantification of myocardial fibrosis: a new macro-based automated analysis. Cell Oncol (Dordr). 2011;34:343–54.CrossRef
35.
go back to reference Yilmaz A, Kindermann I, Kindermann M, Mahfoud F, Ukena C, Athanasiadis A, et al. Comparative evaluation of left and right ventricular endomyocardial biopsy differences in complication rate and diagnostic performance. Circulation. 2010;122:900–9.CrossRefPubMed Yilmaz A, Kindermann I, Kindermann M, Mahfoud F, Ukena C, Athanasiadis A, et al. Comparative evaluation of left and right ventricular endomyocardial biopsy differences in complication rate and diagnostic performance. Circulation. 2010;122:900–9.CrossRefPubMed
36.
go back to reference Chen CA, Dusenbery SM, Valente AM, Powell AJ, Geva T. Myocardial ECV fraction assessed by CMR is associated with type of hemodynamic load and arrhythmia in repaired tetralogy of fallot. JACC Cardiovasc Imaging. 2016;9:1–10.CrossRefPubMed Chen CA, Dusenbery SM, Valente AM, Powell AJ, Geva T. Myocardial ECV fraction assessed by CMR is associated with type of hemodynamic load and arrhythmia in repaired tetralogy of fallot. JACC Cardiovasc Imaging. 2016;9:1–10.CrossRefPubMed
37.
go back to reference Rogers T, Dabir D, Mahmoud I, Voigt T, Schaeffter T, Nagel E, et al. Standardization of T1 measurements with MOLLI in differentiation between health and disease--the ConSept study. J Cardiovasc Magn Reson. 2013;15:78.CrossRefPubMedPubMedCentral Rogers T, Dabir D, Mahmoud I, Voigt T, Schaeffter T, Nagel E, et al. Standardization of T1 measurements with MOLLI in differentiation between health and disease--the ConSept study. J Cardiovasc Magn Reson. 2013;15:78.CrossRefPubMedPubMedCentral
38.
go back to reference Kawel N, Nacif M, Zavodni A, Jones J, Liu S, Sibley C, et al. T1 mapping of the myocardium: Intra-individual assessment of the effect of field strength, cardiac cycle and variation by myocardial region. J Cardiovasc Magn Reson. 2012;14:1–10.CrossRef Kawel N, Nacif M, Zavodni A, Jones J, Liu S, Sibley C, et al. T1 mapping of the myocardium: Intra-individual assessment of the effect of field strength, cardiac cycle and variation by myocardial region. J Cardiovasc Magn Reson. 2012;14:1–10.CrossRef
39.
go back to reference Dabir D, Child N, Kalra A, Rogers T, Gebker R, Jabbour A, et al. Reference values for healthy human myocardium using a T1 mapping methodology: results from the international T1 multicenter cardiovascular magnetic resonance study. J Cardiovasc Magn Reson. 2014;16:69.CrossRefPubMedPubMedCentral Dabir D, Child N, Kalra A, Rogers T, Gebker R, Jabbour A, et al. Reference values for healthy human myocardium using a T1 mapping methodology: results from the international T1 multicenter cardiovascular magnetic resonance study. J Cardiovasc Magn Reson. 2014;16:69.CrossRefPubMedPubMedCentral
40.
go back to reference Dobson G, Cieslar J. Intracellular, interstitial and plasma spaces in the rat myocardiumin vivo. J Mol Cell Cardiol. 1997;29:3357–63.CrossRefPubMed Dobson G, Cieslar J. Intracellular, interstitial and plasma spaces in the rat myocardiumin vivo. J Mol Cell Cardiol. 1997;29:3357–63.CrossRefPubMed
41.
go back to reference Ferreira VM, Piechnik SK, Dall'Armellina E, Karamitsos TD, Francis JM, Choudhury RP, et al. Non-contrast T1-mapping detects acute myocardial edema with high diagnostic accuracy: a comparison to T2-weighted cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2012;14:1–12.CrossRef Ferreira VM, Piechnik SK, Dall'Armellina E, Karamitsos TD, Francis JM, Choudhury RP, et al. Non-contrast T1-mapping detects acute myocardial edema with high diagnostic accuracy: a comparison to T2-weighted cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2012;14:1–12.CrossRef
42.
go back to reference Pickering JG, Boughner DR. Fibrosis in the transplanted heart and its relation to donor ischemic time. Assessment with polarized light microscopy and digital image analysis. Circulation. 1990;81:949–58.CrossRefPubMed Pickering JG, Boughner DR. Fibrosis in the transplanted heart and its relation to donor ischemic time. Assessment with polarized light microscopy and digital image analysis. Circulation. 1990;81:949–58.CrossRefPubMed
43.
go back to reference Armstrong A, Binkley P, Baker P, Myerowitz PD, Leier C. Quantitative investigation of cardiomyocyte hypertrophy and myocardial fibrosis over 6 years after cardiac transplantation. J Am Coll Cardiol. 1998;32:704–10.CrossRefPubMed Armstrong A, Binkley P, Baker P, Myerowitz PD, Leier C. Quantitative investigation of cardiomyocyte hypertrophy and myocardial fibrosis over 6 years after cardiac transplantation. J Am Coll Cardiol. 1998;32:704–10.CrossRefPubMed
44.
go back to reference Gramley F, Lorenzen J, Pezzella F, Kettering K, Himmrich E, Plumhans C, et al. Hypoxia and myocardial remodeling in human cardiac allografts: a time-course study. J Hear Lung Transplant. 2009;28:1119–26.CrossRef Gramley F, Lorenzen J, Pezzella F, Kettering K, Himmrich E, Plumhans C, et al. Hypoxia and myocardial remodeling in human cardiac allografts: a time-course study. J Hear Lung Transplant. 2009;28:1119–26.CrossRef
45.
go back to reference Hiemann NE, Wellnhofer E, Knosalla C, Lehmkuhl HB, Stein J, Hetzer R, et al. Prognostic impact of microvasculopathy on survival after heart transplantation: evidence from 9713 endomyocardial biopsies. Circulation. 2007;116:1274–82.CrossRefPubMed Hiemann NE, Wellnhofer E, Knosalla C, Lehmkuhl HB, Stein J, Hetzer R, et al. Prognostic impact of microvasculopathy on survival after heart transplantation: evidence from 9713 endomyocardial biopsies. Circulation. 2007;116:1274–82.CrossRefPubMed
46.
go back to reference Ahn J, Kim J. Mechanisms and consequences of inflammatory signaling in the myocardium. Curr Hypertens Rep. 2012;14:510–6.CrossRefPubMed Ahn J, Kim J. Mechanisms and consequences of inflammatory signaling in the myocardium. Curr Hypertens Rep. 2012;14:510–6.CrossRefPubMed
47.
go back to reference Riesenkampff E, Luining W, Seed M, Chungsomprasong P, Manlhiot C, Elders B, et al. Increased left ventricular myocardial extracellular volume is associated with longer cardiopulmonary bypass times, biventricular enlargement and reduced exercise tolerance in children after repair of tetralogy of fallot. J Cardiovasc Magn Reson. 2016;18:75.CrossRefPubMedPubMedCentral Riesenkampff E, Luining W, Seed M, Chungsomprasong P, Manlhiot C, Elders B, et al. Increased left ventricular myocardial extracellular volume is associated with longer cardiopulmonary bypass times, biventricular enlargement and reduced exercise tolerance in children after repair of tetralogy of fallot. J Cardiovasc Magn Reson. 2016;18:75.CrossRefPubMedPubMedCentral
48.
go back to reference Shah AM, Claggett B, Sweitzer NK, Shah SJ, Deswal A, Anand IS, et al. Prognostic importance of changes in cardiac structure and function in heart failure with preserved ejection fraction and the impact of spironolactone. Circ Heart Fail. 2015;8:1052–8.PubMedPubMedCentral Shah AM, Claggett B, Sweitzer NK, Shah SJ, Deswal A, Anand IS, et al. Prognostic importance of changes in cardiac structure and function in heart failure with preserved ejection fraction and the impact of spironolactone. Circ Heart Fail. 2015;8:1052–8.PubMedPubMedCentral
49.
go back to reference Eleid MF, Caracciolo G, Cho E, Scott RL, Steidley ED, Wilansky S, et al. Natural history of left ventricular mechanics in transplanted hearts: relationships with clinical variables and genetic expression profiles of allograft rejection. J Am Coll Cardiol Img. 2010;3:989–1000.CrossRef Eleid MF, Caracciolo G, Cho E, Scott RL, Steidley ED, Wilansky S, et al. Natural history of left ventricular mechanics in transplanted hearts: relationships with clinical variables and genetic expression profiles of allograft rejection. J Am Coll Cardiol Img. 2010;3:989–1000.CrossRef
50.
go back to reference Kailin JA, Miyamoto SD, Younoszai AK, Landek BF. Longitudinal myocardial deformation is selectively decreased after pediatric cardiac transplantation: a comparison of children 1 year after transplantation with normal subjects using velocity vector imaging. Pediatr Cardiol. 2012;33:749–56.CrossRefPubMed Kailin JA, Miyamoto SD, Younoszai AK, Landek BF. Longitudinal myocardial deformation is selectively decreased after pediatric cardiac transplantation: a comparison of children 1 year after transplantation with normal subjects using velocity vector imaging. Pediatr Cardiol. 2012;33:749–56.CrossRefPubMed
Metadata
Title
Histological validation of cardiovascular magnetic resonance T1 mapping markers of myocardial fibrosis in paediatric heart transplant recipients
Authors
Seiko Ide
Eugenie Riesenkampff
David A. Chiasson
Anne I. Dipchand
Paul F. Kantor
Rajiv R. Chaturvedi
Shi-Joon Yoo
Lars Grosse-Wortmann
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/s12968-017-0326-x

Other articles of this Issue 1/2017

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