The reproducibility of late gadolinium enhancement cardiovascular magnetic resonance imaging of post-ablation atrial scar: a cross-over study
Henry Chubb, Rashed Karim, Sébastien Roujol, Marta Nuñez-Garcia, Steven E Williams, John Whitaker, James Harrison, Constantine Butakoff, Oscar Camara, Amedeo Chiribiri, Tobias Schaeffter, Matthew Wright, Mark O'Neill, Reza Razavi, Henry Chubb, Rashed Karim, Sébastien Roujol, Marta Nuñez-Garcia, Steven E Williams, John Whitaker, James Harrison, Constantine Butakoff, Oscar Camara, Amedeo Chiribiri, Tobias Schaeffter, Matthew Wright, Mark O'Neill, Reza Razavi
Abstract
Background: Cardiovascular magnetic resonance (CMR) imaging has been used to visualise post-ablation atrial scar (PAAS), generally employing a three-dimensional (3D) late gadolinium enhancement (LGE) technique. However the reproducibility of PAAS imaging has not been determined. This cross-over study is the first to investigate the reproducibility of the technique, crucial for both future research design and clinical implementation.
Methods: Forty subjects undergoing first time ablation for atrial fibrillation (AF) had detailed CMR assessment of PAAS. Following baseline pre-ablation scan, two scans (separated by 48 h) were performed at three months post-ablation. Each scan session included 3D LGE acquisition at 10, 20 and 30 min post administration of gadolinium-based contrast agent (GBCA). Subjects were allocated at second scan post-ablation to identical imaging parameters ('Repro', n = 10), 3 T scanner ('3 T', n = 10), half-slice thickness ('Half-slice', n = 10) or half GBCA dose ('Half-gad', n = 10). PAAS was compared to baseline scar and then reproducibility was assessed for two measures of thresholded scar (% left atrial (LA) occupied by PAAS (%LA PAAS) and Pulmonary Vein Encirclement (PVE)), and then four measures of non-thresholded scar (point-by-point assessment of PAAS, four normalisation methods). Thresholded measures of PAAS were evaluated against procedural outcome (AF recurrence).
Results: A total of 271 3D acquisitions (out of maximum 280, 96.7%) were acquired. At 20 and 30 min, inter-scan reproducibility was good to excellent (coefficient of variation at 20 min and 30 min: %LA PAAS 0.41 and 0.20; PVE 0.13 and 0.04 respectively for 'Repro' group). Changes in imaging parameters, especially reduced GBCA dose, reduced inter-scan reproducibility, but for most measures remained good to excellent (ICC for %LA PAAS 0.454-0.825, PVE 0.618-0.809 at 30 min). For non-thresholded scar, highest reproducibility was observed using blood pool z-score normalisation technique: inter-scan ICC 0.759 (absolute agreement, 'Repro' group). There was no significant relationship between indices of PAAS and AF recurrence.
Conclusion: PAAS imaging is a reproducible finding. Imaging should be performed at least 20 min post-GBCA injection, and a blood pool z-score should be considered for normalisation of signal intensities. The clinical implications of these findings remain to be established in the absence of a simple correlation with arrhythmia outcome.
Trial registration: United Kingdom National Research Ethics Service 08/H0802/68 - 30th September 2008.
Keywords: Atrial fibrillation; Atrium; Cardiac magnetic resonance imaging; Catheter ablation; Late gadolinium enhancement; Optimization.
Conflict of interest statement
Consent for publicationPatient information sheet and consent form included provision for consent for publication (08/H0802/68). All data presented in this article is non-identifiable.
Competing interestsThe authors declare that they have no competing interests.
Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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References
- Peters DC, Wylie J V., Hauser TH, Kissinger K V., Botnar RM, Essebag V, et al. Detection of Pulmonary Vein and Left Atrial Scar after Catheter Ablation with Three-dimensional Navigator-gated Delayed Enhancement MR Imaging: Initial Experience. Radiology [Internet]. 2007 [cited 2013 Oct 22];243:690–695. Available from:
- McGann CJ, Kholmovski EG, Oakes RS, Blauer JJEE, Daccarett M, Segerson N, et al. New Magnetic Resonance Imaging-Based Method for Defining the Extent of Left Atrial Wall Injury After the Ablation of Atrial Fibrillation. J. Am. Coll. Cardiol. [Internet]. 2008 [cited 2014 Dec 18];52:1263–1271. Available from: .
- Akoum N, Wilber D, Hindricks G, Jais P, Cates J, Marchlinski F, et al. MRI Assessment of Ablation-Induced Scarring in Atrial Fibrillation: Analysis from the DECAAF Study. J. Cardiovasc. Electrophysiol. [Internet]. 2015;26:473–480. Available from:
- Fukumoto K, Habibi M, Gucuk Ipek E, Khurram IM, Zimmerman SL, Zipunnikov V, et al. Comparison of preexisting and ablation-induced late gadolinium enhancement on left atrial magnetic resonance imaging. Heart Rhythm [Internet]. 2015;12:668–672. Available from: 10.1016/j.hrthm.2014.12.021
- Bisbal F, Guiu E, Cabanas-Grandío P, Berruezo A, Prat-Gonzalez S, Vidal B, et al. CMR-Guided Approach to Localize and Ablate Gaps in Repeat AF Ablation Procedure. JACC. Cardiovasc. Imaging [Internet]. 2014 [cited 2014 Aug 4];7:653–663. Available from: .
- Harrison JL, Sohns C, Linton NW, Karim R, Williams SE, Rhode KS, et al. Repeat Left Atrial Catheter Ablation: Cardiac Magnetic Resonance Prediction of Endocardial Voltage and Gaps in Ablation Lesion Sets. Circ. Arrhythmia Electrophysiol. [Internet]. 2015 [cited 2015 Jan 16];8:270–278. Available from:
- Hunter RJ, Jones D a, Boubertakh R, Malcolme-Lawes LC, Kanagaratnam P, Juli CF, et al. Diagnostic accuracy of cardiac magnetic resonance imaging in the detection and characterization of left atrial catheter ablation lesions: a multicenter experience. J. Cardiovasc. Electrophysiol. [Internet]. 2013 [cited 2014 Oct 16];24:396–403. Available from: .
- Taclas JE, Nezafat R, Wylie J V, Josephson ME, Hsing J, Manning WJ, et al. Relationship between intended sites of RF ablation and post-procedural scar in AF patients, using late gadolinium enhancement cardiovascular magnetic resonance. Heart Rhythm [Internet]. 2010 [cited 2014 Aug 14];7:489–496. Available from:
- Bellenger NG, Davies LC, Francis JM, Coats a J, Pennell DJ. Reduction in sample size for studies of remodeling in heart failure by the use of cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 2000;2:271–278. doi: 10.3109/10976640009148691.
- Badger TJ, Daccarett M, Akoum NW, Adjei-Poku Y a, Burgon NS, Haslam TS, et al. Evaluation of left atrial lesions after initial and repeat atrial fibrillation ablation: lessons learned from delayed-enhancement MRI in repeat ablation procedures. Circ. Arrhythm. Electrophysiol. [Internet]. 2010 [cited 2014 Aug 12];3:249–259. Available from:
- Karim R, Housden RJ, Balasubramaniam M, Chen Z, Perry D, Uddin A, et al. Evaluation of current algorithms for segmentation of scar tissue from late Gadolinium enhancement cardiovascular magnetic resonance of the left atrium: an open-access grand challenge. J. Cardiovasc. Magn. Reson. [Internet]. 2013;15:105. Available from:
- Groarke JD, Waller AH, Vita TS, Michaud GF, Di Carli MF, Blankstein R, et al. Feasibility study of electrocardiographic and respiratory gated, gadolinium enhanced magnetic resonance angiography of pulmonary veins and the impact of heart rate and rhythm on study quality. J. Cardiovasc. Magn. Reson. [Internet]. 2014 [cited 2014 Jul 2];16:43. Available from: .
- Denton ER, Sonoda LI, Rueckert D, Rankin SC, Hayes C, Leach MO, et al. Comparison and evaluation of rigid, affine, and nonrigid registration of breast MR images. J. Comput. Assist. Tomogr. [Internet]. 1999 [cited 2016 Aug 17];23:800–805. Available from: .
- Malcolme-Lawes LC, Juli C, Karim R, Bai W, Quest R, Lim PB, et al. Automated analysis of atrial late gadolinium enhancement imaging that correlates with endocardial voltage and clinical outcomes: A 2-center study. Heart Rhythm [Internet]. 2013 [cited 2013 Oct 29];10:1184–91. Available from:
- Khurram IM, Beinart R, Zipunnikov V, Dewire J, Yarmohammadi H, Sasaki T, et al. Magnetic resonance image intensity ratio, a normalized measure to enable interpatient comparability of left atrial fibrosis. Heart Rhythm [Internet]. 2014 [cited 2014 Feb 21];11:85–92. Available from: .
- Benito EM, Carlosena-Remirez A, Guasch E, Prat-González S, Perea RJ, Figueras R, et al. Left atrial fibrosis quantification by late gadolinium-enhanced magnetic resonance: a new method to standardize the thresholds for reproducibility. EP Eur. [Internet]. 2016;1272–1279. Available from:
- Harrison JL, Jensen HK, Peel SA, Chiribiri A, Grøndal AK, Bloch LØ, et al. Cardiac magnetic resonance and electroanatomical mapping of acute and chronic atrial ablation injury: a histological validation study. Cardiac magnetic resonance and electroanatomical mapping of acute and chronic atrial ablation injury: a histological valiEur. Heart J. [Internet]. 2014 [cited 2014 Jan 16];35:1486–1495. Available from:
- Crum WR, Camara O, Hill DLG. Generalized overlap measures for evaluation and validation in medical image analysis. IEEE Trans Med Imaging. 2006;25:1451–1461. doi: 10.1109/TMI.2006.880587.
- Calkins H, Kuck KH, Cappato R, Brugada J, Camm AJ, Chen S-A, et al. 2012 HRS/EHRA/ECAS Expert Consensus Statement on Catheter and Surgical Ablation of Atrial Fibrillation: Recommendations for Patient Selection, Procedural Techniques, Patient Management and Follow-up, Definitions, Endpoints, and Research Trial Design. Europace [Internet]. 2012 [cited 2013 Aug 11];14:528–606. Available from:
- Quan H, Shih WJ. Assessing Reproducibility by the Within-Subject Coefficient of Variation with Random Effects Models Author ( s ): Hui Quan and Weichung J. Shih Published by : International Biometric Society Stable URL : REFERENCES Lin. Biometrics. 1996;52:1195–203.
- McGraw KO, Wong SP. Forming inferences about some intraclass correlations coefficients. Psychol Methods 1996;1:390–390.
- Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–174. doi: 10.2307/2529310.
- Morton G, Jogiya R, Plein S, Schuster A, Chiribiri A, Nagel E. Quantitative cardiovascular magnetic resonance perfusion imaging: Inter-study reproducibility. Eur Heart J Cardiovasc Imaging. 2012;13:954–960. doi: 10.1093/ehjci/jes103.
- Mahrholdt H, Wagner A, Holly TA, Elliott MD, Bonow RO, Kim RJ, et al. Reproducibility of chronic infarct size measurement by contrast-enhanced magnetic resonance imaging. Circulation. 2002;106:2322–2327. doi: 10.1161/01.CIR.0000036368.63317.1C.
- Vermes E, Childs H, Carbone I, Barckow P, Friedrich MG. Auto-threshold quantification of late gadolinium enhancement in patients with acute heart disease. J. Magn. Reson. Imaging [internet]. 2013;37:382–390. Available from: .
- D’Angelo T, Grigoratos C, Mazziotti S, Bratis K, Pathan F, Blandino A, et al. High-throughput gadobutrol-enhanced CMR: A time and dose optimization study. J. Cardiovasc. Magn. Reson. J Cardiovasc Magn Reson. 2017;19:1–8. doi: 10.1186/s12968-016-0318-2.
- Goldfarb JW, Arnold S, Roth M. Gadolinium pharmacokinetics of chronic myocardial infarcts: implications for late gadolinium-enhanced infarct imaging. J Magn Reson Imaging. 2009;30:763–770. doi: 10.1002/jmri.21901.
- Spragg DD, Khurram I, Zimmerman SL, Yarmohammadi H, Barcelon B, Needleman M, et al. Initial experience with magnetic resonance imaging of atrial scar and co-registration with electroanatomic voltage mapping during atrial fibrillation: success and limitations. Heart Rhythm [Internet]. 2012;9:2003–2009. doi: 10.1016/j.hrthm.2012.08.039.
- Peters DC, Wylie J V, Hauser TH, Nezafat R, Han Y, Woo JJ, et al. Recurrence of atrial fibrillation correlates with the extent of post-procedural late gadolinium enhancement: a pilot study. JACC. Cardiovasc. Imaging [Internet]. Elsevier Inc.; 2009 [cited 2014 May 29];2:308–316. Available from:
- Nery PB, Belliveau D, Nair GM, Bernick J, Redpath CJ, Szczotka A, et al. Relationship between pulmonary vein reconnection and atrial fibrillation recurrence. JACC Clin Electrophysiol [Internet] 2016;2:474–483. Available from:
- Jiang RH, Po SS, Tung R, Liu Q, Sheng X, Zhang ZW, et al. Incidence of pulmonary vein conduction recovery in patients without clinical recurrence after ablation of paroxysmal atrial fibrillation: mechanistic implications. Heart Rhythm. 2014;11:969–976. doi: 10.1016/j.hrthm.2014.03.015.
- Kuck K-H, Hoffmann BA, Ernst S, Wegscheider K, Treszl A, Metzner A, et al. Impact of complete versus incomplete circumferential lines around the pulmonary veins during catheter ablation of paroxysmal atrial fibrillation: results from the gap-atrial fibrillation-German atrial fibrillation competence network 1 trial. Circ Arrhythm Electrophysiol. 2016;9:e003337. doi: 10.1161/CIRCEP.115.003337.
- Sohns C, Karim R, Harrison JL, Arujuna A, Linton N, Sennett R, et al. Quantitative Magnetic Resonance Imaging Analysis of the Relationship between Contact Force and Left Atrial Scar Formation after Catheter Ablation of Atrial Fibrillation. J. Cardiovasc. Electrophysiol. [Internet]. 2013 [cited 2014 Feb 12];1–8. Available from:
- Higuchi K, Akkaya M, Koopmann M, Blauer JJE, Burgon NS, Damal K, et al. The effect of fat pad modification during ablation of atrial fibrillation: late gadolinium enhancement MRI analysis. Pacing Clin. Electrophysiol. [Internet]. 2013 [cited 2014 Aug 12];36:467–476. Available from:
- Halbfass PM, Mitlacher M, Turschner O, Brachmann J, Mahnkopf C. Lesion formation after pulmonary vein isolation using the advance cryoballoon and the standard cryoballoon: lessons learned from late gadolinium enhancement magnetic resonance imaging. Europace [Internet]. 2015;17:566–573. Available from:
- Badger TJ, Oakes RS, Daccarett M, Burgon NS, Akoum N, Fish EN, et al. Temporal left atrial lesion formation after ablation of atrial fibrillation. Heart Rhythm [Internet] 2009;6:161–168. Available from: 10.1016/j.hrthm.2008.10.042
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