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Quantitative cardiac magnetic resonance T2 imaging offers ability to non-invasively predict acute allograft rejection in children

Published online by Cambridge University Press:  27 May 2020

Neeta Sethi Open the ORCID record for Neeta Sethi [Opens in a new window] ,
Ashish Doshi ,
Tina Doshi ,
Russell Cross ,
Ileen Cronin ,
Elena Amin ,
Joshua Kanter ,
Janet Scheel ,
Sairah Khan  and
Adrienne Campbell-Washburn
...Show all authors
Neeta Sethi
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC20010, USA
Ashish Doshi
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC20010, USA Institute for Computational Medicine, Johns Hopkins University, Baltimore, MD21218, USA
Tina Doshi
Affiliation:
Division of Pain Medicine, Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University, Baltimore, MD21205, USA
Russell Cross
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC20010, USA
Ileen Cronin
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC20010, USA
Elena Amin
Affiliation:
Department of Pediatrics, University of California San Francisco, San Francisco, CA94143, USA
Joshua Kanter
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC20010, USA
Janet Scheel
Affiliation:
Division of Cardiology, St. Louis Children’s Hospital, St. Louis, MO, 63110, USA
Sairah Khan
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC20010, USA
Adrienne Campbell-Washburn
Affiliation:
National Heart, Lung, Blood Institute, National Institutes of Health, Bethesda, MD, 20892, USA
Laura Olivieri*
Affiliation:
Division of Cardiology, Children’s National Hospital, Washington, DC20010, USA
*
Author for correspondence: Laura Olivieri, MD, 111 Michigan Avenue NW, W3-200, Washington, DC20010, USA. Tel: +1 202 476 2020; Fax: +1 202 476 3900. E-mail: [email protected]
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Abstract

Background:

Monitoring for acute allograft rejection improves outcomes after cardiac transplantation. Endomyocardial biopsy is the gold standard test defining rejection, but carries risk and has limitations. Cardiac magnetic resonance T2 mapping may be able to predict rejection in adults, but has not been studied in children. Our aim was to evaluate T2 mapping in identifying paediatric cardiac transplant patients with acute rejection.

Methods:

Eleven paediatric transplant patients presenting 18 times were prospectively enrolled for non-contrast cardiac magnetic resonance at 1.5 T followed by endomyocardial biopsy. Imaging included volumetry, flow, and T2 mapping. Regions of interest were manually selected on the T2 maps using the middle-third technique in the left ventricular septal and lateral wall in a short-axis and four-chamber slice. Mean and maximum T2 values were compared with Student’s t-tests analysis.

Results:

Five cases of acute rejection were identified in three patients, including two cases of grade 2R on biopsy and three cases of negative biopsy treated for clinical symptoms attributed to rejection (new arrhythmia, decreased exercise capacity). A monotonic trend between increasing T2 values and higher biopsy grades was observed: grade 0R T2 53.4 ± 3 ms, grade 1R T2 54.5 ms ± 3 ms, grade 2R T2 61.3 ± 1 ms. The five rejection cases had significantly higher mean T2 values compared to cases without rejection (58.3 ± 4 ms versus 53 ± 2 ms, p = 0.001).

Conclusions:

Cardiac magnetic resonance with quantitative T2 mapping may offer a non-invasive method for screening paediatric cardiac transplant patients for acute allograft rejection. More data are needed to understand the relationship between T2 and rejection in children.

Keywords

Paediatriccardiac magnetic resonanceT2 mappingheart transplantallograft rejection
Type
Original Article
Information
Cardiology in the Young , Volume 30 , Issue 6 , June 2020 , pp. 852 - 859
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Thrush, PT, Hoffman, TM. Pediatric heart transplantation-Indications and outcomes in the current era. J Thorac Dis. 2014; 6: 1080–1096. doi: 10.3978/j.issn.2072-1439.2014.06.16.Google ScholarPubMed
Dipchand, AI, Rossano, JW, Edwards, LB, 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: 1233–1243.CrossRefGoogle ScholarPubMed
Gossett, JG, Canter, CE, Zheng, J, et al.Decline in rejection in the first year after pediatric cardiac transplantation: a multi-institutional study. J Hear Lung Transplant. 2010; 29: 625–632. doi: 10.1016/j.healun.2009.12.009.Google ScholarPubMed
Ameduri, RK, Zheng, J, Schechtman, KB, et al.Has late rejection decreased in pediatric heart transplantation in the current era? A multi-institutional study. J Hear Lung Transplant. 2012; 31: 980–986. doi: 10.1016/j.healun.2012.05.016.Google Scholar
Vermes, E, Pantaleon, C, Ucheux, J, Aupart, M, Cazeneuve, N, Brunereau, L. Cardiac Magnetic Resonance in heart transplant patients: diagnostic value of quantitative tissue markers (T2 mapping and ECV) for acute cardiac rejection diagnosis. J Cardiovasc Magn Reson. 2016; 18: 1–12. http://www.embase.com/search/results?subaction=viewrecord&from=export&id=L72182792%5Cnhttp://rug.on.worldcat.org/atoztitles/link/?sid=EMBASE&issn=10976647&id=doi:&atitle=Cardiac+Magnetic+Resonance+in+heart+transplant+patients%3A+Diagnostic+value+of+quantiCrossRefGoogle Scholar
Patel, J, Kittleson, M, Rafiei, M, et al.The natural history of biopsy negative rejection after heart transplantation. J Hear Lung Transplant. 2013; 2013: S235. doi: 10.1155/2013/236720.Google Scholar
Entrez, A, Version, T. Complications of endomyocardial biopsy in children. 2005; 10588231; 1–2.Google Scholar
Daly, KP, Marshall, AC, Vincent, JA, et al.Endomyocardial biopsy and selective coronary angiography are low-risk procedures in pediatric heart transplant recipients: results of a multicenter experience. J Hear Lung Transplant. 2012; 31: 398–409. doi: 10.1016/j.healun.2011.11.019.CrossRefGoogle ScholarPubMed
Butler, CR, Savu, A, Bakal, JA, et al.Correlation of cardiovascular magnetic resonance imaging findings and endomyocardial biopsy results in patients undergoing screening for heart transplant rejection. J Hear Lung Transplant Off Publ Int Soc Hear Transplant. 2015; 34: 643–650. doi: 10.1016/j.healun.2014.12.020.CrossRefGoogle ScholarPubMed
Thorn, EM, de Filippi, CR. Echocardiography in the cardiac transplant recipient. Heart Fail Clin. 2007; 3: 51–67. doi: 10.1016/j.hfc.2007.02.008.Google ScholarPubMed
Kindel, SJ, Hsu, HH, Hussain, T, Johnson, JN, McMahon, CJ, Kutty, S. Multimodality noninvasive imaging in the monitoring of pediatric heart transplantation. J Am Soc Echocardiogr. 2017; 30: 859–870. doi: 10.1016/j.echo.2017.06.003.CrossRefGoogle ScholarPubMed
Labarrere, CA, Jaeger, BR. Biomarkers of heart transplant rejection: the good, the bad, and the ugly! Transl Res. 2012; 159: 238–251. doi: 10.1016/j.trsl.2012.01.018.CrossRefGoogle ScholarPubMed
Kellman, P, Aletras, AH, Mancini, C, McVeigh, ER, Arai, AE. T2-prepared SSFP improves diagnostic confidence in edema imaging in acute myocardial infarction compared to turbo spin echo. Magn Reson Med. 2007; 57: 891–897. doi: 10.1002/mrm.21215.CrossRefGoogle ScholarPubMed
Cornicelli, MD, Rigsby, CK, Rychlik, K, Pahl, E, Robinson, JD. Diagnostic performance of cardiovascular magnetic resonance native T1 and T2 mapping in pediatric patients with acute myocarditis. J Cardiovasc Magn Reson. 2019; 21: 40. doi: 10.1186/s12968-019-0550-7.CrossRefGoogle ScholarPubMed
Usman, AA, Taimen, K, Wasielewski, M, et al.Cardiac magnetic resonance T2 mapping in the monitoring and follow-up of acute cardiac transplant rejection: a pilot study. Circ Cardiovasc Imag. 2012; 5: 782–790. doi: 10.1161/CIRCIMAGING.111.971101.CrossRefGoogle ScholarPubMed
Vermes, E, Pantaleaon, C, Pucheux, J, Mirza, A, Delhommais, A, Sirinelli, A. Diagnostic value of quantitative tissue markers (T2 mapping and ECV) for acute cardiac rejection diagnosis: a preliminary experience. J Hear Lung Transplant. 2016; 35: S193.Google Scholar
Butler, CR, Thompson, R, Haykowsky, M, Toma, M, Paterson, I. Cardiovascular magnetic resonance in the diagnosis of acute heart transplant rejection: a review. J Cardiovasc Magn Reson. 2009; 11: 7. doi: 10.1186/1532-429X-11-7.CrossRefGoogle Scholar
Bonnemains, L, Villemin, T, Escanye, J, et al.Diagnostic and prognostic value of MRI T2 quantification in heart transplant patients. Transpl Int. 2005: 69–76. doi: 10.1111/tri.12222.Google Scholar
Dolan, RS, Rahsepar, AA, Blaisdell, J. Multiparametric cardiac magnetic resonance imaging can detect acute cardiac allograft rejection after heart transplantation. JACC Cardiovasc Imag 2019: 1–10. doi: 10.1016/j.jcmg.2019.01.026.Google ScholarPubMed
Imran, M, Wang, L, McCrohon, J, et al.Native T1 mapping in the diagnosis of cardiac allograft rejection. JACC Cardiovasc Imag. 2019; 12: 947–948. doi: 10.1016/j.jcmg.2018.10.027.CrossRefGoogle Scholar
Ide, S, Riesenkampff, E, Chiasson, DA, et al.Histological validation of cardiovascular magnetic resonance T1 mapping markers of myocardial fibrosis in paediatric heart transplant recipients. J Cardiovasc Magn Reson. 2017; 19: 1–11. doi: 10.1186/s12968-017-0326-x.CrossRefGoogle ScholarPubMed
Stewart, S, Fishbein, MC, Snell, GI, et al.Revision of the 1996 working formulation for the standardization of nomenclature in the diagnosis of lung rejection. J Hear Lung Transplant. 2007; 26: 1229–1242. doi: 10.1016/j.healun.2007.10.017.Google Scholar
Berry, GJ, Burke, MM, Andersen, C, et al.The 2013 international society for heart and lung transplantation working formulation for the standardization of nomenclature in the pathologic diagnosis of antibody-mediated rejection in heart transplantation. J Hear Lung Transplant. 2013; 32: 1147–1162. doi: 10.1016/j.healun.2013.08.011.CrossRefGoogle ScholarPubMed
Cross, R, Olivieri, L, O’Brien, K, Kellman, P, Xue, H, Hansen, M. Improved workflow for quantification of left ventricular volumes and mass using free-breathing motion corrected cine imaging. J Cardiovasc Magn Reson. 2016; 18: 1–12. doi: 10.1186/s12968-016-0231-8.CrossRefGoogle ScholarPubMed
Kellman, P, Hansen, MS. T1-mapping in the heart: accuracy and precision. J Cardiovasc Magn Reson. 2014; 16: 1–20. doi: 10.1186/1532-429X-16-2.CrossRefGoogle ScholarPubMed
Moon, JC, Messroghli, DR, Kellman, P, 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. doi: 10.1186/1532-429X-15-92.CrossRefGoogle Scholar
Messroghli, DR, Moon, JC, Ferreira, VM, et al.Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2 * and extracellular volume a consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular. J Cardiovasc Magn Reson. 2017; 19: 1–25. doi: 10.1186/s12968-017-0389-8.Google Scholar
Hammer-Hansen, S, Ugander, M, Hsu, L-Y, et al.Distinction of salvaged and infarcted myocardium within the ischaemic area-at-risk with T2 mapping. Eur Hear J - Cardiovasc Imaging. 2014; 15: 1048–1053. doi: 10.1093/ehjci/jeu073.CrossRefGoogle ScholarPubMed
Giri, S, Chung, Y-C, Merchant, A, et al.T2 quantification for improved detection of myocardial edema. J Cardiovasc Magn Reson. 2009; 11: 56. doi: 10.1186/1532-429X-11-56.CrossRefGoogle ScholarPubMed
Olivieri, LJ, Kellman, P, McCarter, RJ, Cross, RR, Hansen, MS, Spurney, CF. Native T1 values identify myocardial changes and stratify disease severity in patients with Duchenne muscular dystrophy. J Cardiovasc Magn Reson. 2017; 18: 72. doi: 10.1186/s12968-016-0292-8.CrossRefGoogle Scholar
Hagio, T, Huang, C, Abidov, A, et al.T2 mapping of the heart with a double-inversion radial fast spin-echo method with indirect echo compensation. J Cardiovasc Magn Reson. 2015; 17: 24. doi: 10.1186/s12968-015-0108-2.CrossRefGoogle ScholarPubMed
Sparrow, P, Amirabadi, A, Sussman, MS, Paul, N, Merchant, N. Quantitative assessment of myocardial T2 relaxation times in cardiac amyloidosis. J Magn Reson Imag. 2009; 30: 942–946. doi: 10.1002/jmri.21918.CrossRefGoogle ScholarPubMed
Blume, U, Lockie, T, Stehning, C, et al.Interleaved T(1) and T(2) relaxation time mapping for cardiac applications. J Magn Reson Imag. 2009; 29: 480–487. doi: 10.1002/jmri.21652.CrossRefGoogle Scholar
Greenway, SC, Dallaire, F, Kantor, PF, et al.Magnetic resonance imaging of the transplanted pediatric heart as a potential predictor of rejection. World J Transplant. 2016; 6: 751. doi: 10.5500/wjt.v6.i4.751.CrossRefGoogle ScholarPubMed
Messroghli, DR, Moon, JC, Ferreira, VM, et al.Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2 and extracellular volume: a consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular Imagin. J Cardiovasc Magn Reson. 2017; 19: 1–3. doi: 10.1186/s12968-017-0389-8.CrossRefGoogle Scholar
Aherne, T, Tscholakoff, D, Finkbeiner, W, et al.Magnetic resonance imaging of cardiac transplants: the evaluation of rejection of cardiac allografts with and without immunosuppression. Circulation. 1986; 74: 145–156. http://www.ncbi.nlm.nih.gov/pubmed/3518982.CrossRefGoogle ScholarPubMed
Aherne, T, Yee, ES, Tscholakoff, D, Gollin, G, Higgins, C, Ebert, PA. Diagnosis of acute and chronic cardiac rejection by magnetic resonance imaging: a non-invasive in-vivo study. J Cardiovacular Surg. 1988; 29: 587–590.Google ScholarPubMed
Tscholakoff, D. Magnetic resonance tomography of the heart. Experimental study of a non-invasive characterization of myocardial tissue. Rofo. 1987; 146: 82–88.Google ScholarPubMed