Detection and grading of coronary allograft vasculopathy in children with contrast-enhanced magnetic resonance imaging of the coronary vessel wall

Circulation: Cardiovascular Imaging

Volumn 6, Issue 1, 2013, Pages 91-98

  Hussain, Tarique ^a   Fenton, Matthew ^b   Peel, Sarah A ^a   Wiethoff, Andrea J ^c   Taylor, Andrew ^b,d   Muthurangu, Vivek ^b,d   Razavi, Reza ^a   Botnar, Rene M ^a   Burch, Michael ^b   Greil, Gerald F ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^c PHILIPS HEALTHCARE   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Coronary artery disease; Heart transplantation; Intravascular ultrasound; MRI; Pediatrics

Indexed keywords

GADOBUTROL; GADOLINIUM; CONTRAST MEDIUM; DIAGNOSTIC AGENT; ORGANOMETALLIC COMPOUND;

ADOLESCENT; ANGIOCARDIOGRAPHY; ARTICLE; BLOOD VESSEL WALL; CARDIAC ALLOGRAFT VASCULOPATHY; CARDIOVASCULAR MAGNETIC RESONANCE; CHILD; CLINICAL ARTICLE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; CORONARY BLOOD VESSEL; FEMALE; HUMAN; INTRAVASCULAR ULTRASOUND; MALE; PRIORITY JOURNAL; SCHOOL CHILD; SENSITIVITY AND SPECIFICITY; ALLOTRANSPLANTATION; COMPARATIVE STUDY; CORONARY ARTERY DISEASE; FOLLOW UP; GRAFT REJECTION; HEART TRANSPLANTATION; INFANT; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PRESCHOOL CHILD; REPRODUCIBILITY;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; CONTRAST MEDIA; CORONARY ARTERY DISEASE; CORONARY VESSELS; FEMALE; FOLLOW-UP STUDIES; GADOLINIUM; GRAFT REJECTION; HEART TRANSPLANTATION; HUMANS; INFANT; MAGNETIC RESONANCE IMAGING, CINE; MALE; ORGANOMETALLIC COMPOUNDS; REPRODUCIBILITY OF RESULTS; TRANSPLANTATION, HOMOLOGOUS;

MLCS; MLOWN;

EID: 84874513267     PISSN: 19419651     EISSN: 19420080     Source Type: Journal    
DOI: 10.1161/CIRCIMAGING.112.975797     Document Type: Article

References (42)

1. Pahl E, Naftel DC, Kuhn MA, Shaddy RE, Morrow WR, Canter CE, Kirklin J; Pediatric Heart Transplant Study. The impact and outcome of transplant coronary artery disease in a pediatric population: a 9-year multi-institutional study. J Heart Lung Transplant. 2005;24:645-651.
2. Schmauss D, Weis M. Cardiac allograft vasculopathy: recent developments. Circulation. 2008;117:2131-2141.
3. van Loosdregt J, van Oosterhout MF, Bruggink AH, van Wichen DF, van Kuik J, de Koning E, Baan CC, de Jonge N, Gmelig-Meyling FH, de Weger RA. The chemokine and chemokine receptor profle of infltrating cells in the wall of arteries with cardiac allograft vasculopathy is indicative of a memory T-helper 1 response. Circulation. 2006;114:1599-1607.
4. Johnson DE, Alderman EL, Schroeder JS, Gao SZ, Hunt S, DeCampli WM, Stinson E, Billingham M. Transplant coronary artery disease: histo-pathologic correlations with angiographic morphology. J Am Coll Cardiol. 1991;17:449-457.
5. Kobashigawa JA, Tobis JM, Starling RC, Tuzcu EM, Smith AL, Valan-tine HA, Yeung AC, Mehra MR, Anzai H, Oeser BT, Abeywickrama KH, Murphy J, Cretin N. Multicenter intravascular ultrasound validation study among heart transplant recipients: outcomes after fve years. J Am Coll Cardiol. 2005;45:1532-1537.
6. Spes CH, Klauss V, Rieber J, Schnaack SD, Tammen AR, Uberfuhr P, Reichart B, Theisen K, Angermann CE, Mudra H. Functional and morphological fndings in heart transplant recipients with a normal coronary angiogram: an analysis by dobutamine stress echocardiography, intra-coronary Doppler and intravascular ultrasound. J Heart Lung Transplant. 1999;18:391-398.
7. St Goar FG, Pinto FJ, Alderman EL, Valantine HA, Schroeder JS, Gao SZ, Stinson EB, Popp RL. Intracoronary ultrasound in cardiac transplant recipients: in vivo evidence of "angiographically silent" intimal thickening. Circulation. 1992;85:979-987.
8. Tuzcu EM, Hobbs RE, Rincon G, Bott-Silverman C, De Franco AC, Robinson K, McCarthy PM, Stewart RW, Guyer S, Nissen SE. Occult and frequent transmission of atherosclerotic coronary disease with cardiac transplantation: insights from intravascular ultrasound. Circulation. 1995;91:1706-1713.
9. Carr DH, Brown J, Bydder GM, Steiner RE, Weinmann HJ, Speck U, Hall AS, Young IR. Gadolinium-DTPA as a contrast agent in MRI: initial clinical experience in 20 patients. Am J Roentgenol. 1984;143:215-224.
10. Pujadas S, Bordes R, Bayes-Genis A. Ventricular non-compaction cardio-myopathy: CMR and pathology fndings. Heart. 2005;91:582.
11. Kim RJ, Wu E, Rafael A, Chen EL, Parker MA, Simonetti O, Klocke FJ, Bonow RO, Judd RM. The use of contrast-enhanced magnetic resonance imaging to identify reversible myocardial dysfunction. N Engl J Med. 2000;343:1445-1453.
12. Maintz D, Ozgun M, Hoffmeier A, Fischbach R, Kim WY, Stuber M, Manning WJ, Heindel W, Botnar RM. Selective coronary artery plaque visualization and differentiation by contrast-enhanced inversion prepared MRI. Eur Heart J. 2006;27:1732-1736.
13. Spuentrup E, Buecker A, Stuber M, Botnar R, Nguyen TH, Börnert P, Kölker C, Günther RW. Navigator-gated coronary magnetic resonance angiography using steady-state-free-precession: comparison to standard T2-prepared gradient-echo and spiral imaging. Invest Radiol. 2003;38:263-268.
14. Botnar RM, Buecker A, Wiethoff AJ, Parsons EC Jr, Katoh M, Katsi-maglis G, Weisskoff RM, Lauffer RB, Graham PB, Gunther RW, Manning WJ, Spuentrup E. In vivo magnetic resonance imaging of coronary thrombosis using a fbrin-binding molecular magnetic resonance contrast agent. Circulation. 2004;110:1463-1466.
15. Moody AR, Murphy RE, Morgan PS, Martel AL, Delay GS, Allder S, MacSweeney ST, Tennant WG, Gladman J, Lowe J, Hunt BJ. Characterization of complicated carotid plaque with magnetic resonance direct thrombus imaging in patients with cerebral ischemia. Circulation. 2003;107:3047-3052.
16. Etienne A, Botnar RM, Van Muiswinkel AM, Boesiger P, Manning WJ, Stuber M. "Soap-Bubble" visualization and quantitative analysis of 3D coronary magnetic resonance angiograms. Magn Reson Med. 2002;48:658-666.
17. Oakes RS, Badger TJ, Kholmovski EG, Akoum N, Burgon NS, Fish EN, Blauer JJ, Rao SN, DiBella EV, Segerson NM, Daccarett M, Windfelder J, McGann CJ, Parker D, MacLeod RS, Marrouche NF. Detection and quan-tifcation of left atrial structural remodeling with delayed-enhancement magnetic resonance imaging in patients with atrial fbrillation. Circulation. 2009;119:1758-1767.
18. McConnell MV, Khasgiwala VC, Savord BJ, Chen MH, Chuang ML, Edelman RR, Manning WJ. Comparison of respiratory suppression methods and navigator locations for MR coronary angiography. Am J Roent-genol. 1997;168:1369-1375.
19. Costanzo MR, Naftel DC, Pritzker MR, Heilman JK 3rd, Boehmer JP, Brozena SC, Dec GW, Ventura HO, Kirklin JK, Bourge RC, Miller LW. Heart transplant coronary artery disease detected by coronary angiogra-phy: a multiinstitutional study of preoperative donor and recipient risk factors: Cardiac Transplant Research Database. J Heart Lung Transplant. 1998;17:744-753.
20. Koning G, Dijkstra J, von Birgelen C, Tuinenburg JC, Brunette J, Tardif JC, Oemrawsingh PW, Sieling C, Melsa S, Reiber JH. Advanced contour detection for three-dimensional intracoronary ultrasound: a validation-in vitro and in vivo. Int J Cardiovasc Imaging. 2002;18:235-248.
21. Radovancevic B, Poindexter S, Birovljev S, Velebit V, McAllister HA, Duncan JM, Vega D, Lonquist J, Burnett CM, Frazier OH. Risk factors for development of accelerated coronary artery disease in cardiac transplant recipients. Eur J Cardiothorac Surg. 1990;4:309-312.
22. Hussain T, Burch M, Fenton MJ, Whitmore PM, Rees P, Elliott M, Aurora P. Positive pretransplantation cytomegalovirus serology is a risk factor for cardiac allograft vasculopathy in children. Circulation. 2007;115:1798-1805.
23. Madani MH, Canter CE, Balzer DT, Watkins MP, Wickline SA. Noninva-sive detection of transplant coronary artery disease with contrast-enhanced cardiac MRI in pediatric cardiac transplants. J Heart Lung Transplant. 2012;31:1234-1235.
24. Arora S, Ueland T, Wennerblom B, Sigurdadottir V, Eiskjær H, Bøtker HE, Ekmehag B, Jansson K, Mortensen SA, Saunamaki K, Simonsen S, Gude E, Bendz B, Solbu D, Aukrust P, Gullestad L. Effect of everolimus introduction on cardiac allograft vasculopathy-results of a randomized, multicenter trial. Transplantation. 2011;92:235-243.
25. Pethig K, Heublein B, Wahlers T, Dannenberg O, Oppelt P, Haverich A. Mycophenolate mofetil for secondary prevention of cardiac allograft vas-culopathy: infuence on infammation and progression of intimal hyperpla-sia. J Heart Lung Transplant. 2004;23:61-66.
26. Mehra MR, Crespo-Leiro MG, Dipchand A, Ensminger SM, Hiemann NE, Kobashigawa JA, Madsen J, Parameshwar J, Starling RC, Uber PA. International Society for Heart and Lung Transplantation working formulation of a standardized nomenclature for cardiac allograft vasculopa-thy-2010. J Heart Lung Transplant. 2010;29:717-727.
27. Schepis T, Achenbach S, Weyand M, Raum P, Marwan M, Pfederer T, Daniel WG, Tandler R, Kondruweit M, Ropers D. Comparison of dual source computed tomography versus intravascular ultrasound for evaluation of coronary arteries at least one year after cardiac transplantation. Am J Cardiol. 2009;104:1351-1356.
28. Bae KT, Hong C, Takahashi N, Gutierrez F, Sharkey AM, Hirsch R, Canter CE. Multi-detector row computed tomographic angiography in pe-diatric heart transplant recipients: initial observations. Transplantation. 2004;77:599-602.
29. Peng Y, Zeng J, Du Z, Sun G, Guo H. Usefulness of 64-slice MDCT for follow-up of young children with coronary artery aneurysm due to Kawasaki disease: initial experience. Eur J Radiol. 2009;69:500-509.
30. Dipchand AI, Bharat W, Manlhiot C, Saf M, Lobach NE, McCrindle BW. A prospective study of dobutamine stress echocardiography for the assessment of cardiac allograft vasculopathy in pediatric heart transplant recipients. Pediatr Transplant. 2008;12:570-576.
31. Larsen RL, Applegate PM, Dyar DA, Ribeiro PA, Fritzsche SD, Mulla NF, Shirali GS, Kuhn MA, Chinnock RE, Shah PM. Dobutamine stress echo-cardiography for assessing coronary artery disease after transplantation in children. J Am Coll Cardiol. 1998;32:515-520.
32. Di Filippo S, Semiond B, Roriz R, Sassolas F, Raboisson MJ, Bozio A. Non-invasive detection of coronary artery disease by dobutamine-stress echocardiography in children after heart transplantation. J Heart Lung Transplant. 2003;22:876-882.
33. Schwitter J, Wacker CM, van Rossum AC, Lombardi M, Al-Saadi N, Ahlstrom H, Dill T, Larsson HB, Flamm SD, Marquardt M, Johansson L. MR-IMPACT: comparison of perfusion-cardiac magnetic resonance with single-photon emission computed tomography for the detection of coronary artery disease in a multicentre, multivendor, randomized trial. Eur Heart J. 2008;29:480-489.
34. Nagel E, Lehmkuhl HB, Bocksch W, Klein C, Vogel U, Frantz E, Ellmer A, Dreysse S, Fleck E. Noninvasive diagnosis of ischemia-induced wall motion abnormalities with the use of high-dose dobutamine stress MRI: comparison with dobutamine stress echocardiography. Circulation. 1999;99:763-770.
35. Muehling OM, Wilke NM, Panse P, Jerosch-Herold M, Wilson BV, Wilson RF, Miller LW. Reduced myocardial perfusion reserve and transmural perfusion gradient in heart transplant arteriopathy assessed by magnetic resonance imaging. J Am Coll Cardiol. 2003;42:1054-1060.
36. Steen H, Merten C, Refe S, Klingenberg R, Dengler T, Giannitsis E, Katus HA. Prevalence of different gadolinium enhancement patterns in patients after heart transplantation. J Am Coll Cardiol. 2008;52: 1160-1167.
37. McGann CJ, Kholmovski EG, Oakes RS, Blauer JJ, Daccarett M, Seger-son N, Airey KJ, Akoum N, Fish E, Badger TJ, DiBella EV, Parker D, MacLeod RS, Marrouche NF. New magnetic resonance imaging-based method for defning the extent of left atrial wall injury after the ablation of atrial fbrillation. J Am Coll Cardiol. 2008;52:1263-1271.
38. Katscher U, Börnert P. Parallel RF transmission in MRI. NMR Biomed. 2006;19:393-400.
39. Desai MY, Stone JH, Foo TK, Hellmann DB, Lima JA, Bluemke DA. Delayed contrast-enhanced MRI of the aortic wall in Takayasu's arteritis: initial experience. Am J Roentgenol. 2005;184:1427-1431.
40. Dill T, Ekinci O, Hansel J, Kluge A, Breidenbach C, Hamm CW. Delayed contrast-enhanced magnetic resonance imaging for the detection of autoimmune myocarditis and long-term follow-up. J Cardiovasc Magn Reson. 2005;7:521-523.
41. Bley TA, Wieben O, Leupold J, Uhl M. Images in cardiovascular medicine: magnetic resonance imaging fndings in temporal arteritis. Circulation. 2005;111:e260.
42. Kobashigawa JA. Cardiac allograft vasculopathy in heart transplant patients: pathologic and clinical aspects for angioplasty/stenting. J Am Coll Cardiol. 2006;48:462-463.