Skip to main content
Top
Published in: Pediatric Cardiology 6/2017

Open Access 01-08-2017 | Original Article

Abnormal Myocardial Contractility After Pediatric Heart Transplantation by Cardiac MRI

Authors: Heynric B. Grotenhuis, Emile C. A. Nyns, Paul F. Kantor, Anne I. Dipchand, Steven C. Greenway, Shi-Joon Yoo, George Tomlinson, Rajiv R. Chaturvedi, Lars Grosse-Wortmann

Published in: Pediatric Cardiology | Issue 6/2017

Login to get access

Abstract

Acute cellular rejection (ACR) compromises graft function after heart transplantation (HTX). The purpose of this study was to describe systolic myocardial deformation in pediatric HTX and to determine whether it is impaired during ACR. Eighteen combined cardiac magnetic resonance imaging (CMR)/endomyocardial biopsy (EMBx) examinations were performed in 14 HTX patients (11 male, age 13.9 ± 4.7 years; 1.2 ± 1.3 years after HTX). Biventricular function and left ventricular (LV) circumferential strain, rotation, and torsion by myocardial tagging CMR were compared to 11 controls as well as between patients with and without clinically significant ACR. HTX patients showed mildly reduced biventricular systolic function when compared to controls [LV ejection fraction (EF): 55 ± 8% vs. 61 ± 3, p = 0.02; right ventricular (RV) EF: 48 ± 7% vs. 53 ± 6, p = 0.04]. Indexed LV mass was mildly increased in HTX patients (67 ± 14 g/m2 vs. 55 ± 13, p = 0.03). LV myocardial deformation indices were all significantly reduced, expressed by global circumferential strain (−13.5 ± 2.3% vs. −19.1 ± 1.1%, p < 0.01), basal strain (−13.7 ± 3.0% vs. −17.5 ± 2.4%, p < 0.01), mid-ventricular strain (−13.4 ± 2.7% vs. −19.3 ± 2.2%, p < 0.01), apical strain (−13.5 ± 2.8% vs. −19.9 ± 2.0%, p < 0.01), basal rotation (−2.0 ± 2.1° vs. −5.0 ± 2.0°, p < 0.01), and torsion (6.1 ± 1.7° vs. 7.8 ± 1.1°, p < 0.01). EMBx demonstrated ACR grade 0 R in 3 HTX cases, ACR grade 1 R in 11 HTX cases and ACR grade 2 R in 4 HTX cases. When comparing clinically non-significant ACR (grades 0–1 R vs. ACR 2 R), basal rotation, and apical rotation were worse in ACR 2 R patients (−1.4 ± 1.8° vs. −4.2 ± 1.4°, p = 0.01 and 10.2 ± 2.9° vs. 2.8 ± 1.9°, p < 0.01, respectively). Pediatric HTX recipients demonstrate reduced biventricular systolic function and decreased myocardial contractility. Myocardial deformation indices by CMR may serve as non-invasive markers of graft function and, perhaps, rejection in pediatric HTX patients.
Literature
1.
go back to reference Dipchand AI, Kirk R, Edwards LB et al (2013) International Society for Heart and Lung Transplantation. The Registry of the International Society for Heart and Lung Transplantation: sixteenth Official Pediatric Heart Transplantation Report–2013; focus theme: age. J Heart Lung Transplant 32(10):979–988CrossRefPubMed Dipchand AI, Kirk R, Edwards LB et al (2013) International Society for Heart and Lung Transplantation. The Registry of the International Society for Heart and Lung Transplantation: sixteenth Official Pediatric Heart Transplantation Report–2013; focus theme: age. J Heart Lung Transplant 32(10):979–988CrossRefPubMed
2.
go back to reference Phelps CM, Tissot C, Buckvold S et al (2011) Outcome of acute graft rejection associated with hemodynamic compromise in pediatric heart transplant recipients. Pediatr Cardiol 32:1–7CrossRefPubMed Phelps CM, Tissot C, Buckvold S et al (2011) Outcome of acute graft rejection associated with hemodynamic compromise in pediatric heart transplant recipients. Pediatr Cardiol 32:1–7CrossRefPubMed
3.
go back to reference Canter CE, Shaddy RE, Bernstein D et al (2007) Indications for heart transplantation in pediatric heart disease: a scientific statement from the American Heart Association Council on Cardiovascular Disease in the Young; the Councils on Clinical Cardiology, Cardiovascular Nursing, and Cardiovascular Surgery and Anesthesia; and the Quality of Care and Outcomes Research Interdisciplinary Working Group. Circulation 115:658–676CrossRefPubMed Canter CE, Shaddy RE, Bernstein D et al (2007) Indications for heart transplantation in pediatric heart disease: a scientific statement from the American Heart Association Council on Cardiovascular Disease in the Young; the Councils on Clinical Cardiology, Cardiovascular Nursing, and Cardiovascular Surgery and Anesthesia; and the Quality of Care and Outcomes Research Interdisciplinary Working Group. Circulation 115:658–676CrossRefPubMed
4.
go back to reference Zuppan CW, Wells LM, Kerstetter JC, Johnston JK, Bailey LL, Chinnock RE (2009) Cause of death in pediatric and infant heart transplant recipients: review of a 20-year, single-institution cohort. J Heart Lung Transplant 28:579–584CrossRefPubMed Zuppan CW, Wells LM, Kerstetter JC, Johnston JK, Bailey LL, Chinnock RE (2009) Cause of death in pediatric and infant heart transplant recipients: review of a 20-year, single-institution cohort. J Heart Lung Transplant 28:579–584CrossRefPubMed
5.
go back to reference Lunze FI, Colan SD, Gauvreau K et al (2012) Cardiac allograft function during the first year after transplantation in rejection-free children and young adults. Circ Cardiovasc Imaging 5:756–764CrossRefPubMed Lunze FI, Colan SD, Gauvreau K et al (2012) Cardiac allograft function during the first year after transplantation in rejection-free children and young adults. Circ Cardiovasc Imaging 5:756–764CrossRefPubMed
6.
go back to reference Kato TS, Oda N, Hashimura K et al (2010) Strain rate imaging would predict sub-clinical acute rejection in heart transplant recipients. Eur J Cardiothorac Surg 37(5):1104–1110CrossRefPubMed Kato TS, Oda N, Hashimura K et al (2010) Strain rate imaging would predict sub-clinical acute rejection in heart transplant recipients. Eur J Cardiothorac Surg 37(5):1104–1110CrossRefPubMed
7.
go back to reference Moran AM, Lipshultz SE, Rifai N et al (2000) Non-invasive assessment of rejection in pediatric transplant patients: serologic and echocardiographic prediction of biopsy-proven myocardial rejection. J Heart Lung Transplant 19:756–764CrossRefPubMed Moran AM, Lipshultz SE, Rifai N et al (2000) Non-invasive assessment of rejection in pediatric transplant patients: serologic and echocardiographic prediction of biopsy-proven myocardial rejection. J Heart Lung Transplant 19:756–764CrossRefPubMed
8.
go back to reference Donofrio MT, Clark BJ, Ramaciotti C et al (1999) Regional wall motion and strain of transplanted hearts in pediatric patients using magnetic resonance tagging. Am J Physiol 277:R1481–R1487PubMed Donofrio MT, Clark BJ, Ramaciotti C et al (1999) Regional wall motion and strain of transplanted hearts in pediatric patients using magnetic resonance tagging. Am J Physiol 277:R1481–R1487PubMed
9.
go back to reference Cameli M, Ballo P, Lisi M et al (2013) Left ventricular twist in clinically stable heart transplantation recipients: a speckle tracking echocardiography study. Int J Cardiol 168(1):357–361CrossRefPubMed Cameli M, Ballo P, Lisi M et al (2013) Left ventricular twist in clinically stable heart transplantation recipients: a speckle tracking echocardiography study. Int J Cardiol 168(1):357–361CrossRefPubMed
10.
go back to reference Hansen DE, Daughters GT, Alderman EL, Ingels NB Jr, Miller DC (1988) Torsional deformation of the left ventricular midwall in human hearts with intramyocardial markers: regional heterogeneity and sensitivity to the inotropic effects of abrupt rate changes. Circ Res 62:941–952CrossRefPubMed Hansen DE, Daughters GT, Alderman EL, Ingels NB Jr, Miller DC (1988) Torsional deformation of the left ventricular midwall in human hearts with intramyocardial markers: regional heterogeneity and sensitivity to the inotropic effects of abrupt rate changes. Circ Res 62:941–952CrossRefPubMed
11.
go back to reference Hansen DE, Daughters GT, Alderman EL, Stinson EB, Baldwin JC, Miller DC (1987) Effect of acute human cardiac allograft rejection on left ventricular systolic torsion and diastolic recoil measured by intramyocardial markers. Circulation 76:998–1008CrossRefPubMed Hansen DE, Daughters GT, Alderman EL, Stinson EB, Baldwin JC, Miller DC (1987) Effect of acute human cardiac allograft rejection on left ventricular systolic torsion and diastolic recoil measured by intramyocardial markers. Circulation 76:998–1008CrossRefPubMed
12.
go back to reference Buchalter MB, Weiss JL, Rogers WJ et al (1990) Noninvasive quantification of left ventricular rotational deformation in normal humans using magnetic resonance imaging myocardial tagging. Circulation 81:1236–1244CrossRefPubMed Buchalter MB, Weiss JL, Rogers WJ et al (1990) Noninvasive quantification of left ventricular rotational deformation in normal humans using magnetic resonance imaging myocardial tagging. Circulation 81:1236–1244CrossRefPubMed
13.
go back to reference Constantine G, Shan K, Flamm SD, Sivananthan MU (2004) Role of MRI in clinical cardiology. Lancet 363:2162–2171CrossRefPubMed Constantine G, Shan K, Flamm SD, Sivananthan MU (2004) Role of MRI in clinical cardiology. Lancet 363:2162–2171CrossRefPubMed
14.
go back to reference Garot J, Bluemke DA, Osman NF et al (2000) Fast determination of regional myocardial strain fields from tagged cardiac images using harmonic phase MRI. Circulation 101:981–988CrossRefPubMed Garot J, Bluemke DA, Osman NF et al (2000) Fast determination of regional myocardial strain fields from tagged cardiac images using harmonic phase MRI. Circulation 101:981–988CrossRefPubMed
15.
go back to reference Gotte MJ, Germans T, Russel IK et al (2006) Myocardial strain and torsion quantified by cardiovascular magnetic resonance tissue tagging: studies in normal and impaired left ventricular function. J Am Coll Cardiol 48:2002–2011CrossRefPubMed Gotte MJ, Germans T, Russel IK et al (2006) Myocardial strain and torsion quantified by cardiovascular magnetic resonance tissue tagging: studies in normal and impaired left ventricular function. J Am Coll Cardiol 48:2002–2011CrossRefPubMed
16.
go back to reference Osman NF, Kerwin WS, McVeigh ER, Prince JL (1999) Cardiac motion tracking using CINE harmonic phase (HARP) magnetic resonance imaging. Magn Reson Med 42:1048–1060CrossRefPubMedPubMedCentral Osman NF, Kerwin WS, McVeigh ER, Prince JL (1999) Cardiac motion tracking using CINE harmonic phase (HARP) magnetic resonance imaging. Magn Reson Med 42:1048–1060CrossRefPubMedPubMedCentral
17.
go back to reference Russel IK, Gotte MJ, Bronzwaer JG, Knaapen P, Paulus WJ, van Rossum AC (2009) Left ventricular torsion: an expanding role in the analysis of myocardial dysfunction. JACC Cardiovasc Imaging 2:648–655CrossRefPubMed Russel IK, Gotte MJ, Bronzwaer JG, Knaapen P, Paulus WJ, van Rossum AC (2009) Left ventricular torsion: an expanding role in the analysis of myocardial dysfunction. JACC Cardiovasc Imaging 2:648–655CrossRefPubMed
18.
20.
go back to reference Mehra MR, Crespo-Leiro MG, Dipchand A et al (2010) International Society for Heart and Lung Transplantation working formulation of a standardized nomenclature for cardiac allograft vasculopathy-2010. J Heart Lung Transplant 29:717–727CrossRefPubMed Mehra MR, Crespo-Leiro MG, Dipchand A et al (2010) International Society for Heart and Lung Transplantation working formulation of a standardized nomenclature for cardiac allograft vasculopathy-2010. J Heart Lung Transplant 29:717–727CrossRefPubMed
21.
go back to reference Van der Geest RJ, Reiber JH (1999) Quantification in cardiac MRI. J Magn Reson Imaging 10:602–608CrossRefPubMed Van der Geest RJ, Reiber JH (1999) Quantification in cardiac MRI. J Magn Reson Imaging 10:602–608CrossRefPubMed
22.
go back to reference Stewart S, Winters GL, Fishbein MC et al (2005) Revision of the 1990 working formulation for the standardization of nomenclature in the diagnosis of heart rejection. J Heart Lung Transplant 24:1710–1720CrossRefPubMed Stewart S, Winters GL, Fishbein MC et al (2005) Revision of the 1990 working formulation for the standardization of nomenclature in the diagnosis of heart rejection. J Heart Lung Transplant 24:1710–1720CrossRefPubMed
23.
go back to reference Reed EF, Demetris AJ, Hammond E et al (2006) Acute antibody-mediated rejection of cardiac transplants. J Heart Lung Transplant 25:153–159CrossRefPubMed Reed EF, Demetris AJ, Hammond E et al (2006) Acute antibody-mediated rejection of cardiac transplants. J Heart Lung Transplant 25:153–159CrossRefPubMed
25.
go back to reference Clemmensen TS, Løgstrup BB, Eiskjær H, Poulsen SH (2015) Changes in longitudinal myocardial deformation during acute cardiac rejection: the clinical role of two-dimensional speckle-tracking echocardiography. J Am Soc Echocardiogr 28(3):330–339CrossRefPubMed Clemmensen TS, Løgstrup BB, Eiskjær H, Poulsen SH (2015) Changes in longitudinal myocardial deformation during acute cardiac rejection: the clinical role of two-dimensional speckle-tracking echocardiography. J Am Soc Echocardiogr 28(3):330–339CrossRefPubMed
26.
go back to reference Miller CA, Naish JH, Shaw SM et al (2014) Multiparametric cardiovascular magnetic resonance surveillance of acute cardiac allograft rejection and characterisation of transplantation-associated myocardial injury: a pilot study. J Cardiovasc Magn Reson 20(16):52CrossRef Miller CA, Naish JH, Shaw SM et al (2014) Multiparametric cardiovascular magnetic resonance surveillance of acute cardiac allograft rejection and characterisation of transplantation-associated myocardial injury: a pilot study. J Cardiovasc Magn Reson 20(16):52CrossRef
27.
go back to reference Cifra B, Dragulescu A, Brun H et al (2014) Left ventricular myocardial response to exercise in children after heart transplant. J Heart Lung Transplant 33(12):1241–1247CrossRefPubMed Cifra B, Dragulescu A, Brun H et al (2014) Left ventricular myocardial response to exercise in children after heart transplant. J Heart Lung Transplant 33(12):1241–1247CrossRefPubMed
28.
go back to reference Koyama J, Ray-Sequin PA, Falk RH (2003) Longitudinal myocardial function assessed by tissue velocity, strain, and strain rate tissue Doppler echocardiography in patients with AL (primary) cardiac amyloidosis. Circulation 107(19):2446–2452CrossRefPubMed Koyama J, Ray-Sequin PA, Falk RH (2003) Longitudinal myocardial function assessed by tissue velocity, strain, and strain rate tissue Doppler echocardiography in patients with AL (primary) cardiac amyloidosis. Circulation 107(19):2446–2452CrossRefPubMed
29.
go back to reference Wu YL, Ye Q, Sato K, Foley LM, Hitchens TK, Ho C (2009) Noninvasive evaluation of cardiac allograft rejection by cellular and functional cardiac magnetic resonance. JACC Cardiovasc Imaging 2:731–741CrossRefPubMedPubMedCentral Wu YL, Ye Q, Sato K, Foley LM, Hitchens TK, Ho C (2009) Noninvasive evaluation of cardiac allograft rejection by cellular and functional cardiac magnetic resonance. JACC Cardiovasc Imaging 2:731–741CrossRefPubMedPubMedCentral
30.
go back to reference Kailin JA, Miyamoto SD, Younoszai AK, Landeck BF (2012) 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 33:749–756CrossRefPubMed Kailin JA, Miyamoto SD, Younoszai AK, Landeck BF (2012) 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 33:749–756CrossRefPubMed
31.
go back to reference Saleh HK, Villarraga HR, Kane GC et al (2011) Normal left ventricular mechanical function and synchrony values by speckle-tracking echocardiography in the transplanted heart with normal ejection fraction. J Heart Lung Transplant 30(6):652–658CrossRefPubMed Saleh HK, Villarraga HR, Kane GC et al (2011) Normal left ventricular mechanical function and synchrony values by speckle-tracking echocardiography in the transplanted heart with normal ejection fraction. J Heart Lung Transplant 30(6):652–658CrossRefPubMed
32.
go back to reference Sato T, Kato TS, Komamura K et al (2011) Utility of left ventricular systolic torsion derived from 2-dimensional speckle-tracking echocardiography in monitoring acute cellular rejection in heart transplant recipients. J Heart Lung Transplant 30(5):536–543CrossRefPubMed Sato T, Kato TS, Komamura K et al (2011) Utility of left ventricular systolic torsion derived from 2-dimensional speckle-tracking echocardiography in monitoring acute cellular rejection in heart transplant recipients. J Heart Lung Transplant 30(5):536–543CrossRefPubMed
Metadata
Title
Abnormal Myocardial Contractility After Pediatric Heart Transplantation by Cardiac MRI
Authors
Heynric B. Grotenhuis
Emile C. A. Nyns
Paul F. Kantor
Anne I. Dipchand
Steven C. Greenway
Shi-Joon Yoo
George Tomlinson
Rajiv R. Chaturvedi
Lars Grosse-Wortmann
Publication date
01-08-2017
Publisher
Springer US
Published in
Pediatric Cardiology / Issue 6/2017
Print ISSN: 0172-0643
Electronic ISSN: 1432-1971
DOI
https://doi.org/10.1007/s00246-017-1642-5

Other articles of this Issue 6/2017

Pediatric Cardiology 6/2017 Go to the issue