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. Author manuscript; available in PMC: 2021 Apr 1.
Published in final edited form as: Magn Reson Med. 2019 Sep 30;83(4):1368–1379. doi: 10.1002/mrm.28001

Acute enhancement of necrotic radio-frequency ablation lesions in left atrium and pulmonary vein ostia in swine model with non-contrast-enhanced T1-weighted MRI

Michael A Guttman 1, Susumu Tao 1, Sarah Fink 1, Rick Tunin 1, Ehud J Schmidt 1, Daniel A Herzka 2, Henry R Halperin 1,3, Aravindan Kolandaivelu 1
PMCID: PMC6949368  NIHMSID: NIHMS1048823  PMID: 31565818

Abstract

Purpose:

To evaluate non-contrast-enhanced MRI of acute radio-frequency ablation (RFA) lesions in the left atrium (LA) and pulmonary vein (PV) ostia. The goal is to provide a method for discrimination between necrotic (permanent) lesions and reversible injury, which is associated with recurrence after treatment of atrial fibrillation.

Methods:

Fifteen normal swine underwent RFA around the right-superior PV ostia. Electrical pulmonary vein isolation (PVI) was verified by electro-anatomic mapping (EAM) and pacing. MRI was performed using a 3D respiratory-gated T1-WeIghted Long Inversion TimE (TWILITE) sequence without contrast agent. Key settings were: inversion time 700ms, triggering over 2 cardiac cycles, pixel size 1.1 mm3. Contrast-enhanced imaging and T2-weighted imaging were performed for comparison. Six animals were sacrificed on ablation day for TTC-stained gross pathology, nine animals were sacrificed after 2–3 months after repeat EAM and MRI. Image Intensity Ratio (IIR) was used to measure lesion enhancement, and gross pathology was used to validate image enhancement patterns and compare lesion widths.

Results:

RFA lesions exhibited unambiguous enhancement in acute TWILITE imaging (IIR=2.34±0.49 at 1.5T), and the enhancement patterns corresponded well with gross pathology. Lesion widths in MRI correlated well with gross pathology (R2=0.84), with slight underestimation by 0.9±0.5 mm. Lesion enhancement subsided chronically.

Conclusion:

TWILITE imaging allowed acute detection of permanent RFA lesions in swine LA and PV ostia, without the need for contrast agent. Lesion enhancement pattern showed good correspondence to gross pathology and was well visualized by volume rendering. This method may provide valuable intra- or post-procedural assessment of RFA treatment.

Keywords: Magnetic resonance imaging; T1-weighted; non-contrast-enhanced, atrial arrhythmia; left atrium; radiofrequency ablation; pulmonary vein isolation; lesion gaps; recurrence

Introduction

Atrial fibrillation (AF) is the most common clinical cardiac arrhythmia (1), and catheter-based radio-frequency ablation (RFA) has emerged as an effective therapy for managing symptoms (2,3). However, AF recurrence rates post-RFA remain high, over 30% for paroxysmal AF and over 50% for persistent AF (4). Most cases of paroxysmal AF recurrence are associated with regions of incomplete ablation that are not detected during the procedure, causing reversible injury and transient conduction block (5–7). To achieve permanent conduction block, ablation must lead to tissue necrosis (cell death). However, the conventional electrophysiology suite lacks tools for accurately indicating regional tissue necrosis.

Magnetic resonance imaging (MRI) has been considered for years in this role, with its soft-tissue contrast to indicate damaged or necrotic myocardium. Acute imaging of tissue necrosis could reveal gaps for targeting of additional ablations to complete treatment and reduce recurrence (6,8–14). Several groups have reported MRI studies to visualize myocardial ablation lesions acutely, some employing contrast-enhanced (CE) imaging with early gadolinium enhancement (EGE) or late enhancement (LGE) techniques (15–17). Non-CE imaging with T1-weighted (T1w) (18–23) or T2-weighted (T2w) (18,19,22,24,25) pulse sequences have also been investigated. Real-time MRI temperature imaging has been proposed to monitor ablations in progress (26–28).

CE MRI methods do not differentiate permanent from transient tissue injury acutely post-ablation. EGE depicts the necrotic lesion as hypo-enhanced regions with accumulation of contrast agent around the edges (15,29–31). However, as imaging is repeated every few minutes, lesion appearance evolves with time as contrast agent enters the core regions, obscuring the borders and confounding estimation of lesion size using contrast enhancement (15,31,32). LGE also enhances reversible tissue injury such as edema (33–35), which limits its use for confirming permanent lesions at the time of ablation. In addition, dosage restrictions severely limit the number of times a CE protocol can be run during a procedure.

Non-CE T2w imaging enhances sites of acute ablation but is sensitive to edema, which is a transient form of tissue injury, and leads to overestimation of lesion size (19,24,36–38). Non-CE T1w imaging appears more specific for permanent lesions (19,20,23,30). Our group recently reported improved imaging of acute RF ablation lesions with non-CE 3D T1w Long Inversion TimE (TWILITE) sequence (30), using inversion recovery, respiratory gating and longer image acquisition times. The technique allowed robust visualization of ablation lesions in the left ventricle (LV) and thin-walled sections of the right ventricle. Enhancement was confined to the necrotic core, easily visible against normal myocardium, suppressed cavitary blood, or even scarred myocardium, and stable for weeks post-ablation. The 3D image data was displayed in volume renderings, created without segmentation, for improved appreciation of the lesion topology.

An acute imaging method which reliably identifies necrotic ablation lesions and gaps could reduce the risk of recurrence. This study evaluates TWILITE in a swine model for acute imaging of necrotic RFA lesions in the left atrium (LA) and right superior pulmonary vein (RSPV), of relevance to ablative treatment of AF. Imaging results were compared with conventional electro-physiological assessment and gross pathology.

Methods

Animal Experiments

All animal experiments were approved by the Johns Hopkins University, School of Medicine, Institutional Animal Care and Use Committee. Prior to the invasive procedure, swine were sedated with tiletamine, ketamine and xylazine (TKX), and maintained under anesthesia with 1–2% isoflurane.

In 15 swine, a trans-septal puncture was performed via femoral venous access to the LA using fluoroscopy guidance. The LA and RSPV anatomy was defined by electro-anatomical mapping (EAM) using an Ensite Velocity system (Abbott Inc., Minnetonka, MN) with multi-electrode catheters (AFocusII, 1–2.5–1 mm inter-electrode spacing, 1-mm electrode size, Abbott Inc.). Saline irrigated RFA of the LA and RSVP ostium was performed at 30 W for 30–40 seconds with a contact-force sensing catheter (TactiCath, Abbott Inc.).

A small number of target points (1–3) were ablated in the LA to test conspicuity in MRI. A larger number of points (10–20) were ablated circumferentially around the RSPV ostium to simulate a pulmonary vein isolation (PVI) procedure (39). Electrical isolation was confirmed after ablation using conventional methods of EAM and pacing. After ablation, animals were transported to the MR scanner for in vivo imaging.

Acute protocol (N=6):

Animals were sacrificed after imaging, using injection with 20 mL of a 20% solution of 2,3,5-triphenyltetrazolium chloride (TTC) for staining and euthanized with potassium chloride solution. After excision of the heart, slices were made for gross pathology of the lesions and comparison with MR images.

Chronic protocol (N=9):

Points were ablated circumferentially in the ostium until PVI was confirmed, without attempting to produce a completely contiguous ablation ring. This was to increase the chance of chronic reconnection for our study, while still achieving the conventional treatment endpoint. Animals were kept for 2–3 months after ablation, which is the conventional blanking period for the post-ablative evaluation of atrial fibrillation (40). Repeat MRI was performed during this period. On day of termination, EAM was repeated to test for electrical isolation followed by MRI, sacrifice and gross pathology examination as in the acute protocol.

Imaging Protocol

MR imaging was performed on 1.5 T Avanto and 3 T Prisma clinical scanners (Siemens, Erlangen, Germany) using a phased-array surface coil on the chest, and surface coils embedded in the patient table. The MR imaging sequence (TWILITE) was described previously (30).

The mechanism of T1 enhancement in RF-ablated myocardium was described in prior work (20,41–45): ablation of muscle tissue causes oxidation of iron within myoglobin (Mb), found in muscle tissue, and hemoglobin (Hb), found in red blood cells, changing the ferrous (Fe+2) to the ferric (Fe+3) state, resulting in metmyoglobin (metMb) and methemoglobin (metHb), respectively. metMb and metHb molecules are paramagnetic, causing T1 shortening and signal enhancement in T1w images.

The inversion time (TI) in TWILITE which maximizes the contrast between normal and ablated myocardium was found experimentally to occur in the range of 700–800 ms, depending on heart rate (20,30). Blood signal is suppressed, since it has a longer T1. To permit this longer TI with faster heart rates, inversion and image acquisition occurred over two heart beats (2RR triggering). Other parameters: TR/TE/flip angle = 5.4ms / 2.7ms / 25°, reconstructed pixel size 1.1 mm3 with 2x interpolation in the slice direction (acquired pixel size 1.1×1.1×2.2 mm3), fat saturation, segmented centric phase-encoding order with 16 k-space segments per acquisition window (about 100 ms duration), GRAPPA acceleration factor (R)=2, field of view (FOV) 280×280 mm2 (depending on body size), matrix 256×256, 20% oversampling in slice direction, bandwidth (BW) 250 Hz/pixel, and 60–80 axial slices/volume as required to cover the LA, default tracking factor of 0.6, and respiratory navigator acceptance window 3 mm wide. The narrow acceptance window was made practical by the repeatability of mechanical respiration. The same imaging parameters were used at 1.5T and 3T.

The 3D sequence was first run as a shorter scan (1RR triggering, 2.5 mm slice thickness) to confirm that the slab contained the anatomy of interest. Cine imaging was then used to determine a delay time after ECG trigger for data acquisition during minimal atrial motion. This was used to prescribe the longer 3D scan at higher resolution. Images were acquired in the transverse orientation, typical for clinical atrial imaging, offering in-plane views of the PVs.

CE images were then obtained for comparison. The same sequence was used, but with TI=400 ms, 1RR triggering and 15° flip angle. EGE scans were acquired post-contrast agent injection (Magnevist, Berlex, Inc.), using a quicker scan with fewer slices (2.5 mm) to observe the transient early enhancement pattern. At 15–20 minutes post-injection, LGE was performed using the same sequence with 1.1 mm slices for higher resolution imaging of the ablation lesion pattern.

Volume renderings of the 3D data sets were created in commercially available software (OsiriX, Pixmeo, Inc.). Image preparation for volume rendering was straightforward, using the ‘Scissors Editing’ tool to isolate the heart, then adjusting the window/level. A color map was optionally used to render background anatomy and enhanced regions in different hues.

Acute Imaging Comparison to Gross Pathology and Data Analysis

Lesion size measurements were performed on the acutely sacrificed animals, where acute imaging could be compared to acute gross pathology. The widths of lesions were measured in vivo by MRI and ex vivo by gross pathology along lines of similar orientation and maximum width. For gross pathology, necrotic lesions were cut in cross-section and photographed for digital measurement. TTC stained gross pathology showed a pale outer region, which corresponded to the necrotic lesion extent, as well as a darker brown inner region. Lesions were measured at their maximum widths for both the brown inner regions and pale outer regions.

Measurements in MRI were based on widths of regions enhanced at least 2σ above adjacent normal myocardium. Multi-planar reformatting (MPR) was used where necessary to obtain similar slices to the gross pathology cross sections. Widths measured in MRI were matched with those from gross pathology, where possible, and were compared with linear regression and Bland-Altman analysis. Contiguous lesions (i.e. those which might overlap) were not separable in MRI, thus comparisons were performed only for distinct, non-overlapping lesions.

Enhancement of individual lesions were measured using Image Intensity Ratio (IIR) (46), which we computed as the ratio between the maximum pixel intensity in the lesion and the mean intensity of normal myocardial tissue. IIR was used to compare lesion contrast between 1.5T and 3T, and to analyze reduction in contrast at approximately one week post-ablation.

Results

For the TWILITE acquisition with 1.1 mm slices and 2RR triggering, imaging time was 16–20 minutes, depending on heart rate (80 ± 11 bpm) and respiratory navigator efficiency (typically 55–65%). In all experiments, RF ablation lesions were clearly visible as enhanced regions in the walls of the LA and RSPV (Figure 1). As measured in images using non-CE TWILITE, IIR of acute lesion enhancement was similar but slightly higher at 1.5T (2.34 ± 0.49, n=17) than at 3T (1.94 ± 0.25, n=15) with p < 0.008.

Figure 1.

Figure 1.

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(A-H) Selected slices from non-CE T1w (TWILITE) imaging acutely post-RFA at 1.5T. Two locations were ablated in the LA (orange arrows) and several around the RSPV ostium (e.g. yellow arrows). Lesion enhancement is readily discernable from normal tissue and dark blood. (D) The RSPV ostium location is indicated by a dashed yellow ellipse.

Acute Experiments with Gross Pathology

In the acute protocol, six animals were ablated and sacrificed, with four completing gross pathology with TTC staining (two of the animals expired before TTC stain could be completed). Three were imaged at 1.5T, and the remainder at 3T.

Figure 1 illustrates a typical result from acute non-CE T1w imaging of RFA lesions. Ablation was performed at 2 sites in the LA and additional sites around the RSPV ostium. Electrical isolation of the RSPV was confirmed using EAM-guided sensing and pacing. Imaging was performed within 2 hours of ablation using the TWILITE sequence at 1.5T, followed by CE imaging for comparison. Parallel slices from the 3D scan are shown with anatomical regions marked (D). Enhancement of the RF ablation lesions is clearly visible in both the LA (orange arrows) and RSPV (yellow arrows). Gaps are visible due to the lower image intensity of normal myocardium. Blood signal is suppressed in all chambers, permitting discrimination of ablation lesions from the blood pool.

Figure 2 compares acute non-CE imaging with early and late CE, for the slice shown in Figure 1E. In EGE (B), lesions appear hypo-intense, as reported in prior LV studies (30), whereas in LGE (C), enhancement occurs at the edges of the lesions. Lesions on the posterior wall (orange arrows), and a gap in anterior lesions (red arrow) are clearly visible in the non-CE images, but difficult to identify on CE images. In LGE, enhancement is also seen in several non-ablated structures such as the aorta wall.

Figure 2.

Figure 2.

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Comparison between non-CE and CE scans, using the slice location from Figure 1E. (A) Lesions and gaps are enhanced in non-CE T1w TWILITE images. (B) Hypo-intense regions are seen in early CE (EGE), consistent with prior studies in the LV. Note that (B) was acquired at lower resolution, immediately post-injection, to capture early-phase contrast distribution. (C) On LGE acquired 34 minutes after injection, anterior lesions (yellow arrows) are still hypo-intense at the center with contrast agent accumulation at the edges. Posterior wall lesions (orange arrows), and a gap in anterior lesions (red arrow) are clearly visible in non-CE T1w but difficult to identify with EGE or LGE.

The selective enhancement of ablation lesions and suppression of cavity blood signal in non-CE T1w imaging allows volume rendering without detailed (and error-prone) tissue segmentation. Figure 3 shows volume renderings of the ablation lesions produced from the 3D TWILITE image data. The ring-like arrangement of lesions in the RSPV ostium is apparent in the volume rendering shown in Figure 3 (A), as are the independent lesions in the LA. All lesions are shown in anatomical context against the background of normal tissue. A posterior/inferior segment of the ablation ring appears thinner than the rest (arrow). See Supporting Information Video S1 for a video of this data set. Displaying image intensity with a color map (B) can assist in discrimination between enhanced lesions and background tissue. During EAM, ablations were recorded by marking the position of the catheter tip (C, red spheres), the arrangement of which resembled the enhancement pattern in the volume rendering.

Figure 3.

Figure 3.

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Volume rendered TWILITE reveals the 3D spatial relationship of acute ablation lesions. (A, B) Individual lesions in the LA and a ring pattern in the RSPV are apparent, with a thin segment on the posterior wall (arrow). (B) A color-map can assist in discriminating between enhanced lesions (light blue) and normal tissue (orange). (C) EAM ablation map in RL view shows a similar ablation pattern (red/white spheres) to that seen in MRI. A coronary sinus catheter position is represented in green.

Figure 4 compares volume rendering of TWILITE images to gross pathology. The volume rendering (A) was rotated for similar orientation as the gross pathology photograph (B). The correspondence in lesion pattern is evident between in vivo images and gross pathology. The lesions marked by red and yellow arrows were cut in cross-section along the dashed line in (B) and folded open as shown in (C). The zoomed lesion in (D) shows that the unstained necrotic ablation lesion contains a brown inner region surrounded by a pale outer region.

Figure 4.

Figure 4.

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Comparison between TWILITE lesion enhancement and gross pathology. (A) Volume rendering of TWILITE image data image rotated for en face view of RSPV ostium (I-S view); aorta is adjacent to the RSPV. (B) Corresponding TTC stained pathology, where viable myocardium is stained deep red while necrotic ablation lesions and connective tissue remain pale. The LA is opened to reveal endocardial surface with ablation lesions around the RSPV ostium and LA wall. Matching lesions between imaging and pathology are denoted by colored arrows. (C) Tissue was cut along dashed line in B and folded open to reveal cross-sections of lesions marked with yellow and red arrows. In this view, the arrows point to the endocardial surface. Lesion topology compares favorably between in vivo MRI and gross pathology. (D) Enlarged view of a lesion (red arrow) shows unstained necrotic region, with brown inner subregion.

In the acute studies, the widths of the brown inner regions and pale outer regions, as measured in gross pathology, differed by 1.5 ± 0.4 mm (n=10), suggesting a mean thickness of 0.75 mm for the outer band of pale tissue. Figure 5 shows matched pair comparisons between MRI and gross pathology using linear regression and Bland-Altman analysis. Widths measured in MRI were well correlated with those from gross pathology for both inner regions (R2 = 0.97, p < 0.0001) and outer regions (R2 = 0.84, p < 0.0002). Widths measured in MRI were consistently between the inner and outer widths from gross pathology, as shown in the Bland-Altman plots, and overestimates the width of the brown inner region by 0.6 ± 0.2 mm (p < 0.0001), and underestimates the outer width by 0.9 ± 0.5 mm (p < 0.0002).

Figure 5.

Figure 5.

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Comparisons of lesion widths measured in TWILITE MRI versus gross pathology. Left and right columns use widths of inner brown regions (A,C), and outer pale regions (B,D), respectively, as measured in gross pathology. Linear regression plots in the top row (A,B) show good correlation between width measurements from MRI and gross pathology (black dashed line denotes y = x). Bland-Altman plots in the bottom row (C,D) indicate the MRI measurements have a 0.6 mm bias to the inner region, and −0.9 mm bias to the outer region, as compared to gross pathology. Red dotted lines denote the 95% confidence interval, while the blue dashed lines denote limits of agreement to ±1.96×SD.

Chronic experiments with followup EAM and imaging

Of the nine animals completing the chronic protocol, one developed chronic PV occlusion and was excluded, and four developed electrical reconnection between RSPV and LA. Four were imaged at 1.5T and the remainder at 3T.

Figure 6 shows EAM results from a case in which chronic reconnection occurred. The color maps show peak-to-peak (P-P) bipolar myocardial voltage, and recorded potentials at different stages of the experiment: (A) pre-ablation, (B) acutely post-ablation, (C) chronically (11 weeks) post-ablation; signals from surface ECG and coronary sinus are shown for timing reference to determine atrial versus ventricular activation. Electrical isolation of the RSPV was confirmed acutely post-ablation (B) by reduced voltage around the ostium, lack of potentials within the vessel, and absence of left atrial atrial capture while pacing from within the vessel. Chronic EAM (C) shows recovery of tissue voltage (white arrow), and late potential (yellow arrow) in the anterior-right portion of the RSPV ostium indicating reconnection to the LA, which was verified by pacing from within the vessel.

Figure 6.

Figure 6.

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Peak-to-peak bipolar voltage amplitude from EAM is shown (A) pre-ablation, (B) acutely post-RFA, and (C) chronically 11 weeks post-RFA. EAM was limited to the regions near and in the RSPV ostium; with the remainder of LA is outside the mapped region. Purple indicates higher P-P voltage while orange/red indicates low voltage. Corresponding electrogram tracings are shown to the right of each EAM including surface reference (ECG), coronary sinus (CS), and lasso mapping catheter. (A) RSPV ostium (near the dashed hoop) initially exhibits high voltage. (B) Electrical isolation is indicated acutely post-ablation by reduced voltage in ostium and proximal RSPV. Ablation positions are marked by white spheres. (C) Chronic reconnection is indicated by return to higher voltage level (white arrow), and late potentials (yellow arrow).

In the same case, Figure 7 shows acute non-CE ablation lesion imaging using TWILITE. Although PVI was confirmed acutely after ablation, non-CE T1w imaging showed gaps in ablation regions, marked by red arrows. Lesion enhancement is visible in the individual 2D image slices (A-D) but the topology of lesions and gaps is more easily appreciated in the volume rendering (E). One of the acute lesion gaps are in the anterior-right portion of the RSPV, corroborated by the chronic EAM finding. See Supporting Information Video S2 for a video of this data set.

Figure 7.

Figure 7.

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Acute non-CE MRI at 1.5T on ablation day, same case as Figure 6. Contiguous image slices (A-D) were acquired within two hours post-RFA using TWILITE. RSPV is within the yellow ellipse. Ablation lesions are visibly enhanced in the 2D images (yellow arrows), with some gaps evident (red arrows). (E) The relative positions of lesions and gaps are more easily visualized in 3D volume rendering, shown in I-S orientation, with some apparent gaps marked by red arrows.

Figure 8 compares image contrast in another animal by non-CE (T1w and T2w) and CE MRI (EGE and LGE) at four stages of the protocol: 1) pre-ablation, 2) acutely post-ablation (same day), 3) ~1 week post-ablation, and 4) chronically (~4 weeks) post-ablation. Lesions were most easily identifiable in acute non-CE T1w, followed by chronic LGE. Lesion enhancement in non-CE T1w was greatest acutely, reduced after one week, and absent by four weeks post-ablation. Acutely post-ablation, T2w imaging showed broad areas of enhancement and discrete lesions are not easily identified. EGE showed lesion cores as hypo-intense regions, similar to enhanced regions seen in non-CE T1w. However, hypo-intensity was also visible in additional non-ablated regions which may represent transient injury. Hypo-intense regions in EGE were reduced by one week and absent by four weeks, similarly to non-CE T1w. In LGE, enhancement of lesions was visible both acutely and chronically post-ablation, however, other non-ablated regions were also enhanced, especially at the acute stage. The delay times for the LGE images shown in Figure 8 were 40, 32 and 35 minutes for acute, one-week, and chronic stages, respectively. We used delay times longer than typically recommended since the darker blood improves contrast with enhanced tissue on the endocardium. These observations were similar across all chronic studies performed.

Figure 8.

Figure 8.

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Longitudinal imaging after RFA in and around RSPV ostium. Images were acquired at four stages (columns): 1) pre-ablation, 2) same day as ablation (acute), 3) approximately one week (9-days in this case, subacute), and 4) 4-weeks post-ablation (chronic). The rows show different imaging protocols used at each stage for comparison: non-CE T1w (TWILITE), T2w, early (EGE) and late CE (LGE). T2w images were acquired only acutely, and CE acquired only post-ablation (blank where not acquired). Lesion enhancement (yellow arrows) is seen most clearly in acute T1w followed by non-acute LGE. T1w enhancement is reduced after one week (column 3), and absent by four weeks (column 4). Acute T2w shows broad areas of enhancement post-RFA, typical of edema (e.g. blue arrow). Acute EGE exhibits hypo-intensity (no-flow) at the lesion sites (orange arrow), but also other areas (e.g. red arrow). Acute LGE shows enhancement at the lesion sites (orange arrow), but also in several non-ablated regions (e.g. red arrows). Chronically, LGE exhibits more selective enhancement for the lesion sites (yellow arrow), although other tissues still enhance.

In three cases which underwent repeat imaging approximately one week after ablation (two at 7 days, one at 9 days), attenuation of lesion enhancement in non-CE T1w imaging was evident. For ten matched lesions evaluated at 1.5T, the mean IIR value dropped significantly from 2.14 ± 0.18 to 1.58 ± 0.06 (p < 0.0001). At chronic stages (> 4 weeks, 9 animals), enhancement in non-CE T1w imaging was not visible at any lesion site.

Discussion

This study illustrated that RF ablation lesions in the thin walled left atrium can be well visualized shortly after ablation using a non-contrast-enhanced inversion-recovery MRI sequence with a long TI of 700–800 ms (TWILITE). We expanded on our previous work that evaluated this method for visualizing permanent, necrotic, ablation lesions in the LV (30). To simulate treatment of AF, lesions were placed around the ostium of the RSPV to achieve electrical isolation (PVI). In all cases, lesions were unambiguously enhanced and gaps between lesions were visible due to the high contrast between necrotic lesions and non-necrotic (preserved) myocardial tissue. Using the same imaging parameters, enhancement was slightly greater at 1.5T than 3T, however the IIR metric used does not take into account relative noise level, which is lower at 3T.

Minor postprocessing was needed to produce 3D volume renderings for appreciation of the lesion topology. The window and level settings used in volume renderings were subjective, but the strong lesion-tissue contrast facilitated the process. This method could reduce the need for detailed, time consuming, error-prone, tissue segmentation and surface rendering.

Enhanced regions in acute non-CE T1w MRI correlated well with necrotic regions in gross pathology after acute sacrifice and TTC stain. Measurements indicated that MRI underestimated the total lesion width by ~0.9 mm, and overestimated a darker brown inner region by ~0.6 mm. One hypothesis for these observations involves the mechanism for T1 shortening from RF ablation. The temperature required to reach tissue necrosis is roughly 50°C (47), while a slightly higher temperature of 54.4°C (130°F) is needed to cause the oxidation from Mb to metMb, which gives cooked meat a brownish appearance (41). The met- forms of Mb and Hb are paramagnetic and a source of T1 shortening (20,42). Lack of metMb within the pale outer region of the necrotic zone would support this hypothesis of underestimation.

Non-CE T1w lesion size underestimation might lead to additional ablation to eliminate apparent gaps between lesions. This is likely preferable to overestimation of lesion size which could lead to incomplete ablation, a known source of arrhythmia recurrence (6,48). T2w or CE MRI, which have also been used for assessment of RF ablation lesions, are known to overestimate the region of necrosis (49). Nevertheless, these techniques could prove useful for identifying edematous tissue which may be more difficult to ablate (38), and CE imaging remains the standard for identification of chronic scar. T2w images were not acquired for each case and presented only for example, however, further study is warranted to determine the best use of T2 contrast in MR guided ablative treatment.

Since T1w imaging can be used acutely to predict durable lesions created by RFA (23), TWILITE may play a role in improving the efficacy of RFA treatment by revealing gaps in the lesion pattern. For clinical utility, further study is needed to determine characteristics of gaps (e.g. sizes and locations) which are likely to be associated with chronic reconnection.

While non-CE T1w MRI yields robust enhancement in acute RFA lesions, longitudinal imaging showed that enhancement was reduced by one week and absent by four weeks. This trend agrees with (50) and our previous work in the LV, where the enhanced region reduced as necrotic myocardium was replaced by fibrous scar tissue from the outer edges (51). The absence of chronic enhancement is advantageous, since it allows differentiation between pre-existing scar and acute lesions (52).

Since oxidation of Mb and Hb to their met- forms is likely the endogenous contrast agent which causes T1 shortening in necrotic lesions, TWILITE may be limited to those ablation methods which cause this oxidation. For example, our preliminary testing has shown that cryoablation does not result in this type of enhancement.

The presence of arrhythmia during imaging can pose a challenge for segmented ECG-gated MRI techniques such as TWILITE. However, cardioversion to sinus rhythm is routinely performed in the clinical setting, and there are techniques that reduce the sensitivity of MRI to arrhythmia (53–55). Another limitation is the time required to complete the higher resolution 3D scan. Although GRAPPA (R=2) was used in this work, future work will evaluate other acceleration techniques such as compressed sensing (56), and methods to improve respiratory navigator efficiency (57). Furthermore, validation in human subjects is needed, and data collection is now in progress.

In the conventional EP setting, the proposed non-CE imaging technique for acute identification of necrotic RF ablation lesions may be useful to assess the completeness of treatment before discharging the patient. In future settings where ablation treatment could be performed in the MR scanner (58–60), non-CE imaging assessment of lesions may be performed multiple times, to direct additional treatment to areas of incomplete ablation, and potentially reduce arrhythmia recurrence.

Conclusion

Non-CE T1w imaging of RFA lesions in the LA and RSPV was demonstrated in a swine model. Positive contrast of necrotic ablation lesions was achieved using inversion recovery with long TI (TWILITE), exploiting the intrinsic T1 shortening within the region of myocardial necrosis. Individual and contiguous lesions were readily visible, as well as gaps between lesions, with good correspondence to gross pathology. Volume-rendered 3D display showed ablation lesions and gaps in anatomical context. The proposed imaging technique may provide valuable intra- or post-procedural assessment of RF ablative treatment in the atrium with the potential to improve efficacy in currently difficult to treat arrhythmias like AF.

Supplementary Material

Supp VideoS1

Supporting Information Video S1: This video shows a rotating volume rendering of the image data shown in Figure 3. Images were acquired acutely post-ablation using non-CE T1w (TWILITE) technique. Regions of necrotic RF ablation are most enhanced, while some normal myocardium and ascending aorta wall appear gray, and blood is suppressed. A ring of ablation in the RSPV ostium is apparent as well as two isolated lesions in the LA

Download video file (1MB, mov)
Supp VideoS2

Supporting Information Video S2: This video shows a rotating volume rendering of the image data shown in Figure 7. In this non-CE T1w (TWILITE) data set, ablation lesions and gaps are apparent in the RSPV ostium. The volume rendering allows rapid appreciation of the lesion topology and gaps. PVI was confirmed acutely post-ablation, however, this animal developed chronic reconnection.

Download video file (444.1KB, mov)

Acknowledgements

This study was supported by NIH R01 EB022011–22 and HL094610

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supp VideoS1

Supporting Information Video S1: This video shows a rotating volume rendering of the image data shown in Figure 3. Images were acquired acutely post-ablation using non-CE T1w (TWILITE) technique. Regions of necrotic RF ablation are most enhanced, while some normal myocardium and ascending aorta wall appear gray, and blood is suppressed. A ring of ablation in the RSPV ostium is apparent as well as two isolated lesions in the LA

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Supp VideoS2

Supporting Information Video S2: This video shows a rotating volume rendering of the image data shown in Figure 7. In this non-CE T1w (TWILITE) data set, ablation lesions and gaps are apparent in the RSPV ostium. The volume rendering allows rapid appreciation of the lesion topology and gaps. PVI was confirmed acutely post-ablation, however, this animal developed chronic reconnection.

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