First-in-Man Analysis of the Relationship Between Electrical Rotors From Noninvasive Panoramic Mapping and Atrial Fibrosis From Magnetic Resonance Imaging in Patients With Persistent Atrial Fibrillation
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Abstract
Background—Late gadolinium enhancement (LGE) cardiovascular magnetic resonance (CMR) imaging can be used to evaluate characteristics of atrial fibrosis. The novel noninvasive epicardial and endocardial electrophysiology system (NEEES) allows for the identification of sources with rotor activity. This study describes a new technique to examine the relationship between rotors and LGE signal intensity in patients with persistent atrial fibrillation (PERS) scheduled for ablation.
Methods and Results—Ten consecutive patients underwent pulmonary vein isolation for persistent atrial fibrillation. LGE CMR of both atria was performed, and NEEES-based analysis was conducted to identify rotors. For each mapping point, the intracardiac locations were transferred onto an individual CMR-derived 3-dimensional shell. This allowed the LGE signal intensity to be projected onto the anatomy from the NEEES analysis. NEEES analysis identified a total number of 410 electric rotors, 47.8% were located in the left atrium and 52.2% in the right atrium. Magnetic resonance imaging analysis was performed from 10 right atria and 10 left atria data sets, including 86 axial LGE CMR planes per atrium. The mean LGE burden for left atrium and right atrium was 23.9±1.6% and 15.9±1.8%, respectively. Statistical analysis demonstrated a lack of regional association between the extent of LGE signal intensity and the presence of rotors.
Conclusions—This is the first study demonstrating that the presence of rotors based on NEEES analysis is not directly associated with the extent and anatomic location of LGE signal intensity from CMR. Further studies evaluating the relationship between rotors and fibrosis in patients with persistent atrial fibrillation are mandatory and may inform strategies to improve ablation outcome.
Introduction
WHAT IS KNOWN
Late gadolinium enhancement cardiovascular magnetic resonance imaging can be used to evaluate characteristics of atrial fibrosis.
Sources with electric rotor activity in atrial fibrillation can be identified from noninvasive panoramic mapping.
WHAT THE STUDY ADDS
The novel noninvasive epicardial and endocardial electrophysiology system allows for identification of sources with rotor activity in atrial fibrillation.
The overall distribution of electric rotor activity seems to be individual, whereas we observed a good interindividual correlation for the presence of atrial fibrosis.
The presence of atrial rotors based on noninvasive epicardial and endocardial electrophysiology system analysis is not directly associated with the extent and anatomic location of late gadolinium enhancement signal intensity from cardiovascular magnetic resonance imaging.
Catheter ablation for persistent atrial fibrillation (PERS) is challenging and associated with only moderate outcome.1–3 The mechanisms initiating and perpetuating atrial fibrillation (AF) are still not completely understood, and, therefore, ablation strategies are heterogeneous.1–4 Novel pathophysiological findings, mapping systems, and ablation strategies are currently under investigation and may improve clinical outcomes in chronic forms of AF.
As a potential new approach to improve understanding of the underlying substrate, the translation of phase mapping into clinical applications is promising.5,6 In parallel, recent progress in numerically solving the inverse problem of electrocardiography opened ways for noninvasive electrocardiography imaging. On the basis of body surface ECG mapping, the electrocardiography imaging allows for the reconstruction of unipolar electrograms and promising results of noninvasive mapping in AF were reported recently.7 On the basis of this technology, electric rotors and focal sources were demonstrated in patients with PERS.8–10 In this context, a novel noninvasive epicardial and endocardial electrophysiology system (NEEES) allows for reproducible identification of ectopic electric sources and activity.11
Atrial remodeling, including fibrosis and scar, is suggested to play an important role for a potential anchor point of anatomic reentrant circuits.12,13 Late gadolinium enhancement (LGE) cardiovascular magnetic resonance (CMR) imaging can be used to evaluate characteristics of atrial wall abnormalities14 and might therefore assist in detecting specific area with fibrotic tissue as a substrate for rotor clustering.
In this study, we sought to examine the regional relationship between electric rotors from NEEES and LGE signal intensity (SI) from CMR in patients with PERS scheduled for catheter ablation.
Methods
Ten consecutive patients with drug-refractory, symptomatic PERS were scheduled to undergo catheter ablation, and all clinical, imaging, and procedural data were recorded. All patients underwent LGE CMR followed by rotor mapping using NEEES in AF the day before ablation. Written informed consent was obtained from each patient before the procedures, and the study was approved by the institutional review board.
CMR Acquisition
All patients underwent CMR according to our standard protocol.15 In brief, MRI was performed in a 1.5-T scanner (Magnetom Avanto, Siemens, Germany), using standard body and spine surface coils. To visualize LGE SI, a 3-dimensional (3D) ECG-triggered, inversion recovery prepared turbo gradient echo sequence with respiratory navigator gating was performed. Typical other scan parameters for LGE of the atria were axial imaging volume with a field of view: 360×360×110 mm, voxel size 1.3×1.3×2.5 mm3, repetition time=5.2 ms, echo time=2.4 ms, flip angle of 20°. Depending on patient’s respiration, typical scan time for the LGE imaging was 6 to 12 minutes. Data were acquired at mid-diastole, with a 150 ms acquisition window and a low–high k-space ordering, as well as spatial presaturation with inversion recovery fat suppression. The inversion recovery delay time for LGE imaging was determined from an inversion time (TI) scout sequence and was set at a TI value intermediate between the optimal TI values to null myocardium and blood. Previous work has validated this method for reproducible visualization of the late enhancement signal from necrotic tissue.16 LGE scans were performed 15 minutes after contrast agent administration (0.2 mmol/kg gadoteric acid; Dotarem, Guerbet, France). The number of slices was set for complete atrial coverage (44 slices).
CMR Image Processing
CMR images were processed as described previously.15–18 In brief, an automatic 3D segmentation of the RA and LA was created from the balanced steady-state–free precession whole-heart acquisition. The LGE acquisition was registered to the 3D balanced steady-state–free precession acquisition and projected on to the 3D shell using a maximum intensity projection technique, whereby the maximum SI within 3 mm of the 3D surface was selected. SIs were then displayed on the 3D RA and LA shells as a number of SDs from the mean SI of the LA blood pool to avoid the need for thresholding. Importantly, this methodology has been previously reported and validated for atrial fibrosis and scar quantification from LGE CMR images.17–19
Noninvasive Epicardial and Endocardial Electrophysiological Mapping
The methodology of electrocardiography imaging with the NEEES system has been reported previously.20 The Amycard 01C EP laboratory (EP Solutions SA, Yverdon-les-Bains, Switzerland) was used for noninvasive ECG imaging. A total of 224 MRI-compatible body surface mapping electrodes were applied on the patient’s torso and connected to the multichannel ECG amplifier (EP Solutions SA). To proof for rotor stability over time, continuous ECGs were recorded for 30 minutes applying a bandwidth of 0.05 to 500 Hz, a sampling rate of 1000 samples/s, and an optional notch filter of 50 Hz (Figure 1). Afterward, the obtained data from CMR were imported into Amycard 01C EP system software in DICOM (Digital Imaging and Communications in Medicine) format to reconstruct a 3D model of the torso and heart. Epicardial atrial 3D models were obtained in high resolution by segmentation and polygonal mesh reconstruction. Furthermore, epicardial unipolar electrograms and phase maps were reconstructed by NEEES inverse problem solution software (EP Solutions SA).
Noninvasive Identification of Rotors in PERS
Ten ECG fragments of 30 s each, with 800 to 1000 ms pauses between adjacent QRS complexes (interval T-Q), were selected and exported into the Amycard 01C EP laboratory software for each patient. Global bandpass filtration from 3 to 9 Hz was used before phase calculation. Each T-Q segment with the length >800 ms was processed to find rotor activity during AF. Sites with rotations on the phase map around stable pivot points were considered as a rotor. Stable rotor criteria were defined as phase front rotation of at least 360° and rotor core meandering area not exceeding 20 mm along the atrial surface during 1 rotation cycle. Each location of rotor activity was marked and registered onto the reconstructed 3D atrial model (Figure 1). For this purpose, and to compare with LGE data, the LA and RA were systematically divided into segments as demonstrated in Figure 2.
Comparison of LGE and Rotor Location
Rotor and LGE maps were created from the same CMR data and imported into software custom written with Python (Python Software Foundation). The 2 maps (Figure 3A and 3B) were fused using the iterative closest point algorithm,21 which computes an optimal affine-based registration for fusion of 2 surfaces.22 Rotor information could thus be directly analyzed with LGE data as every vertex on the fused shell had an associated rotor and LGE label (Figure 3D). After fusion of the rotor and LGE maps, both quantitative and qualitative comparisons were performed. For each fusion, the registration error was calculated as the mean distance from each vertex on the rotor shell to the nearest vertex on the registered LGE shell (Figure 4), and a map of absolute distances between the fused models was created (Figure 3C). For further analysis, the rotor and LGE maps were visualized using Paraview (Kitware Inc) and analyzed based on the anatomic segments.
Statistical Analysis
The preliminary exploratory analysis was conducted to evaluate the distribution of different data; an initially P value <0.05 was considered as statistically significant. Patient clinical characteristics and spatial anatomic distribution of rotors and LGE SI data were reported using descriptive statistics. The amount of rotor data for each atrial segment was not normally distributed, whereas LGE data did not severely differ from normal distribution. On the basis of these findings, continuous variables are expressed as median with min/max range or 25% to 75% interquartile range for patient clinical characteristics and rotor spatial distribution and as mean and SD for the LGE data. Categorical data are presented as numbers and percentages. The Pearson χ2 and Fisher exact tests were used for the analysis of cross tabulation tables of categorical data for clinical parameters. The Mann–Whitney U test was performed to compare independent samples, including patients’ characteristics with LGE SI and rotor distribution. These tests were used as exploratory analysis tools.
The Spearman rank correlation was calculated to compare the continuous variables of LGE data and rotors. The Wilcoxon signed-rank test was performed to compare 2 continuous variables by means of LGE SI and mean values of rotors in the RA and LA. Furthermore, Friedman 1-way ANOVA by ranks test was used to compare multiple continuous variables of LGE SI and rotor values for all atrial segments. After that, we performed joining cluster analysis (Ward method, 1-Pearson r criterion) of LGE data and rotor distribution among all patients. All comparisons were made in accordance with cross-sectional study design. Finally, a P value <0.01 was considered as statistically significant because of the Bonferroni correction and relatively small number of analyzed patients. Comprehensive statistical analysis was performed using Statistica v.10 (Statsoft Inc) and SPSS v.23 (IBM Corp).
Results
Clinical Characteristics
Ten patients (median age 67 years; range 46–77 years, 5 male) with PERS underwent LGE CMR followed by rotor analysis using NEEES. Median AF duration per patient was 8 months (range 1–45); none of the patients underwent previous ablation. In all patients at least 1 antiarrhythmic drug failed prior the indication to undergo catheter ablation. The clinical baseline characteristics of the entire study population are depicted in Table 1. There was no significant association between clinical characteristics and the amount of LGE SI or anatomic localization of rotors.
Rotor Analysis and Location
In all 10 patients, a total number of 410 rotors were identified from NEEES, with 196 (47.8%) occurring in the LA and 214 (52.2%) in the RA. Mean value of total observation time for NEEES was 18.9 s; mean (SD) value of ECG fragment length was 561 ms (154 ms). The median (interquartile range, 25%–75%) number of revealed rotors per patient was n=20 (14–30), n=20 (11–22), and n=44 (24–56) for the RA, LA, and total, respectively. The majority of the rotors in the LA was located along the inferior wall n=66 (minimal 1–17 maximal rotor(s) at this location) and in vicinity to the right superior pulmonary vein (PV) n=35 (0–10). RA sources were predominantly detected in the superior lateral segment n=84 (0–18). Anatomic distribution of rotors and rotor occurrence rate were completely different in the RA, LA, and between all segments (P<0.001). There was no significant difference between mean number of rotors for the RA and LA (P=0.72). Table 2 shows the whole distribution of right- and left-sided rotors and the total number of rotors per patient. Rotors were not sustained and showed meandering rotor activity with their core traveling over an area of >2 cm2. Yet, the occurrence of rotational activity demonstrated a stochastic pattern with clustering in regions specific for each individual. In consequence, a rotor location could not be observed at a certain site but more broadly as region or anatomic segment. In this context, Figure 5A demonstrates the rotor distribution in both atria per segment. In addition, the interindividual distribution of rotors was also totally different as demonstrated in Figure 6 (P=0.006).
Anatomic Distribution of LGE SI
The majority of the LGE SI burden from preprocedural CMR was observed in the LA, predominantly at the posterior wall and along the left atrial appendage. In this context, the total extent of LGE SI was higher when compared with the RA when considering all patients. The mean LGE burden as a percentage of the total LA and RA surface was 23.9±1.6% and 15.9±1.8%, as well as 20.5±1.2% in both atria, respectively. Focusing on the mean LGE burden, we observed a significant difference for the LA and RA (P=0.005). In this context, the sectors with the highest amount of LGE SI were located along the posterior wall (40.5±4.4%) and in the left atrial appendage (34.9±6.2%). For the RA, the highest amount of LGE SI was detected in the superior septal (22.6±5.28%) and inferior septal wall (21.2±7.7%), respectively. Table 2 shows the whole distribution of mean LGE SI per patient, as well as the total LGE burden for the RA and LA, whereas Figure 5B demonstrates the distribution of LGE SI per atrial segment for the RA and LA. The interindividual distribution of LGE SIs for all segments irrespective of their anatomic location was completely different among the patients (P<0.001). In contrast, the interpatients distribution of the LGE SIs was not significantly different (Figure 6B; P=0.056), and a significant correlation was observed for the LGE SI extent when comparing all patients.
Relationship Between Atrial Fibrosis and Rotor Distribution
The distribution of LGE SI and rotors among all patients is demonstrated in Table 2. There was no statistical significant correlation between anatomic rotor location from NEEES and the amount of LGE SI from CMR in the RA and LA, as to be appreciated from the correlation diagram in Figure 7. In addition, NEEES identified the minimal presence of segmental rotor activity (<6% for the LA and <2% for the RA) inside atrial segments with LGE SI >25% (LA) and 20% (RA), respectively (Figure 5).
Despite this fact, we observed a higher interindividual correlation for the presence of LGE SI per segment when compared with the anatomic distribution of rotors. An additional joining cluster analysis using the Ward method (1-Pearson r criterion) was performed as demonstrated in Figure 8. The results of this cluster analysis demonstrate a clear structure of clusters where the strongest similarities (short linkage distances) were observed between patients inside the LGE SI group, and the strongest dissimilarities were found between the group of LGE SI and rotors. This finding can be regarded as a lack of direct anatomic association between the extent of LGE SI and presence of rotors in the current patient cohort.
Fusion Accuracy of the Left and Right Atrial Models
The mean number of vertices per fused atrial model was 1523, and the mean (SD) distance between each LGE SI and rotor model was 5.4±3.8 mm. The absolute values for minimal distance between the fused models were <0.1 mm and 20.9 mm for the maximal distance, whereas the 25% to 75% range was 2.5 to 7.2 mm (Figure 4A). In this context, the cumulative histogram analysis of the mean distances between the fused models shows that 89% of all vertices had distance <10 mm, and even 51% <5 mm (Figure 4B). Furthermore, 11% of the area with distances >10 mm was located in the pulmonary veins and the distal part of the left atrial appendage.
Discussion
Main Finding
The main finding of this study was that in patients with PERS, rotors identified applying NEEES have no direct anatomic relationship with regions of elevated LGE SI in the RA and LA. This is the first study to specifically analyze the correlation between rotors in PERS from noninvasive panoramic mapping and the amount of preprocedural atrial fibrosis from CMR.
Role of NEEES and Invasive Mapping for Rotors in AF
Identification and localization of AF-initiating triggers and AF-maintaining substrate is a prerequisite for effective AF treatment strategies either applying invasive or noninvasive mapping methods. In contrast to body surface mapping, the focal impulse and rotor modulation–guided ablation strategy is an invasive approach. A potential limitation of this system is that stable rotors may be underestimated because of a mismatch of the multipolar basket catheter and the atrial anatomy and thereby a lack of atrial wall-to-tissue contact. Moreover, the multipolar basket catheter cannot cover the total atrial surface of the RA and LA at the same time, which is a pivotal requirement for correct mapping of unstable arrhythmias, such as AF. This could be an explanation why no correlation was found between rotor localization from invasive mapping and complex fractionated atrial electrogram sites23 and area of low voltage from electroanatomical mapping.24 In this context, our data from NEEES clearly show that the distribution of rotors demonstrated some common trends. On the one hand, rotors were not sustained and showed meandering rotor activity with their core traveling along the atrial surface. Yet, the occurrence of rotational activity demonstrated a stochastic pattern with clustering in regions specific for every patient. This finding is in line with previous data from Haissaguerre et al9 also evaluating another panoramic noninvasive atrial mapping system in AF. In particular, in all patients, the majority of identified rotors were observed in the LA inferior wall (20.1%) and RA superior lateral wall (17.9%), respectively (Table 2; Figure 5). On the other hand, the distribution of the rotors between all segments and among all patients was completely different, and these findings were statistically significant. Thereby, our data demonstrate that the overall spatial distribution of atrial rotors seems to be individual, which may explain the lack of significant interindividual correlation. Furthermore, we observed higher interindividual correlations for the presence of fibrosis when compared with the anatomic distribution of rotors. A potential benefit of NEEES when compared with invasive rotor mapping is the panoramic visualization of rotor activity and therefore a more detailed information about its location and activity with equal spatial resolution for the whole atrial surface. However, the specific anatomic rotor location from NEEES might differ from endocardial rotor mapping, and a direct comparison of invasive and noninvasive rotor mapping approaches is still pending in humans. It has to be taken into consideration that data derived from prospective multicenter studies are necessary before a conclusion with focus on advantages and disadvantages of invasive and noninvasive mapping strategies for rotors in AF can be drawn.
Relationship Between Atrial Fibrosis and Rotor Distribution
There is evidence from experimental models that structural modalities, such as fibrosis or scar tissue, may be important in anchoring fibrillatory rotors.13 Furthermore, recent data suggest that stable rotors in AF are located along the border zone between fibrotic and healthy atrial tissue.25 In this context, CMR allows to distinguish between atrial fibrosis and normal atrial tissue in patients with AF.13 Also, in virtual studies using in silico CMR-based models of patient-specific LA structure and LGE SI, AF was inducible according to the level of LGE SI.26 Recently, Chrispin et al27 reported their data about regional association between atrial LGE SI from CMR and AF rotors from a focal impulse and rotor modulation–guided mapping approach. The authors found that there was no correlation between the incidence of rotors in PERS from invasive mapping and the global extent of atrial LGE SI.27 This is in line with our findings as one can see from Figures 6 through 8. NEEES identified a total number of 410 rotors (41 rotors per patient), with 47.8% occurring in the LA and 52.2% in the RA. The mean LGE SI burden was 23.9±1.6% for the LA and 15.9±1.8% for the RA. In concordance with the findings of Chrispin et al,27 statistical analysis could not detect a significant association between the extent of LGE SI and the presence of rotors in our cohort. This might lead to the suggestion that electroanatomic remodeling in patients with PERS has some different components, which are still not completely understood. On the one hand, our data indicate that fibrosis and scar tissue can be visualized using CMR at typical locations representing an anatomic substrate as a target for catheter ablation, which is in line with previous data.28,29 On the other hand, NEEES and invasive mapping methods identified the presence of electric rotors without any anatomic reference.27 This could probably be explained by the fact that rotors move and meander around a core8,9,13 and might therefore not stay stable at the same position during MRI and NEEES. To finally understand that phenomenon, an analysis of rotor stability over the time and its correlation with LGE SI would be essential.
Clinical Implication
Strategies to improve the efficacy of catheter ablation in patients with PERS are warranted. New ablation targets include among others complex fractionated atrial electrograms, additional linear lesions sets, homogenization of atrial fibrosis, modulation of the autonomic nervous system, left atrial appendage isolation, and targeting electric rotors from invasive and noninvasive mapping. The initial results of rotor-guided ablation approaches are heterogeneous,30,31 and the idea to ablate electric rotors needs further validation.32 In addition, Akoum et al29,33 recently reported their interesting ablation approach to target preprocedural fibrosis in patients with PERS. However, currently, we have to conclude that fibrosis from CMR cannot predict the presence of electric rotors based on standard anatomic segmentation, and further data are necessary to determine whether a rotor-based ablation strategy alone or a combination with another ablation target may have the potential to improve the outcomes after ablation for PERS.
Study Limitations
This is not an outcome-based study. It seeks to demonstrate a new method applying CMR to quantify the correlation between LGE SI and the presence of rotors from noninvasive mapping in patients with PERS before catheter ablation. Therefore, the patient numbers are small, and a follow-up of the ablation outcome was not assessed. One very useful outcome of the study is the lack of direct anatomic correlation between the extent of LGE SI and rotors from NEEES-based segmentation, demonstrating that LGE SI could not be used as a surrogate parameter for the presence of electric rotors. However, it has to be considered that the specific algorithm for the NEEES-based rotor distribution might differ from endocardial rotor mapping findings, and a direct comparison of invasive and noninvasive rotor mapping approaches has not yet been performed in vivo. In addition, the software used for the analysis of atrial fibrosis does not differentiate between preablation fibrosis and atrial ablation-induced scar tissue. In this context, a recent study by Karim et al19 found no significant differences with focus on segmentation of scar tissue from LGE CMR of the LA comparing different algorithms. The segmentation software used in this study has been described previously and can be considered as reproducible.15–18 It remains questionable whether this is also true for the analysis of preablation scar formation. However, we cannot completely exclude that another algorithm for segmentation of atrial scar tissue from LGE CMR might result in different results, especially when using a software that allows for differentiation of fibrosis and ablation-induced scar tissue.
Conclusions
There is no direct anatomic relationship between the amount and location of RA and LA LGE SI and the presence of electric rotors identified from NEEES. Further prospective studies are necessary to determine whether the amount of LGE SI is associated with rotor activity before final conclusions can be drawn.
Acknowledgments
We greatly appreciate the help of Maria Chaykovskaya (EP Solutions SA, Yverdon-les-Bains, Switzerland) with the segmentation of atrial models.
Disclosures
Drs Chmelevsky and Schulze are consultants of EP Solutions SA. The other authors report no conflicts.
- Received June 12, 2016.
- Accepted June 29, 2017.
- © 2017 American Heart Association, Inc.
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- First-in-Man Analysis of the Relationship Between Electrical Rotors From Noninvasive Panoramic Mapping and Atrial Fibrosis From Magnetic Resonance Imaging in Patients With Persistent Atrial FibrillationChristian Sohns, Christine Lemes, Andreas Metzner, Thomas Fink, Mikhail Chmelevsky, Tilman Maurer, Margarita Budanova, Vladislav Solntsev, Walther H.W. Schulze, Wieland Staab, Shibu Mathew, Christian Heeger, Bruno Reißmann, Eugene Kholmovski, Dietmar Kivelitz, Feifan Ouyang and Karl-Heinz KuckCirculation: Arrhythmia and Electrophysiology. 2017;10:e004419, originally published August 8, 2017https://doi.org/10.1161/CIRCEP.116.004419
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- First-in-Man Analysis of the Relationship Between Electrical Rotors From Noninvasive Panoramic Mapping and Atrial Fibrosis From Magnetic Resonance Imaging in Patients With Persistent Atrial FibrillationChristian Sohns, Christine Lemes, Andreas Metzner, Thomas Fink, Mikhail Chmelevsky, Tilman Maurer, Margarita Budanova, Vladislav Solntsev, Walther H.W. Schulze, Wieland Staab, Shibu Mathew, Christian Heeger, Bruno Reißmann, Eugene Kholmovski, Dietmar Kivelitz, Feifan Ouyang and Karl-Heinz KuckCirculation: Arrhythmia and Electrophysiology. 2017;10:e004419, originally published August 8, 2017https://doi.org/10.1161/CIRCEP.116.004419