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Abstract

Objective

To compare lesion size and depth between a 1-step, a sequential, and a delayed radio-frequency ablation in a hybrid setup.

Methods

Left atrium tissues obtained from fresh porcine hearts were mounted into the ABLABOX simulator. Based on the time differences between the index epicardial (epi) and consequent endocardial (endo) ablation, 3 study groups were compared: a 1-stage (SEQ- 0) group (0-minute delay), an SEQ 1 group (60-minute delay), and an SEQ 2 group (240-minute delay). During the experiment, a constant epicardial (300 gr) and endocardial (30 gr) force were applied. Per group, 20 samples were studied, and the resulting lesion size and depth were quantified with morphometric evaluation.

Results

Overall, no transmural lesion was obtained. Lesions in SEQ 0 had better maximum and minimum diameters (P < 0.001), a larger total area (P < 0.001), and volume (P < 0.001) than SEQ 1 and SEQ 2. There was no statistical difference in morphometric parameters (all, P > 0.05) between the delayed procedures (SEQ 1 and SEQ 2).

Conclusions

In our in vitro model, different time sequences of combined epi–endo ablation did not result in transmural lesions. However, simultaneous epi–endo ablation produced broader and deeper lesions. Our findings need to be confirmed by further research.

Keywords

ablation catheter ablation surgical ablation hybrid ablation

Central Message

Using fresh porcine heart tissue, morphometric results indicated that in hybrid ablation, the lesion transmurality is not dependent on the time frame between the epicardial and the endocardial procedure.

Introduction

Hybrid ablation of atrial fibrillation (AF) is a treatment approach that combines 2 separate steps: a thoracoscopic epicardial ablation with an endocardial catheter ablation.¹ The early report on hybrid AF ablation showed promising results,² and these initial results have been confirmed in other, more recent reports.^3,4 Nevertheless, the hybrid approach is based on a mutually reinforcing collaboration between the surgeon and the electrophysiologist and by concept inextricable linked to the continued search for improvements, resulting in a more effective treatment approach.^5
-7

Potential development is the optimization of the time lapse between the endocardial and epicardial stage, which can vary from minutes to months.^5,8
-10 To date, it is not known whether a 1-stage or a 2-stage procedure translates in better efficacy.¹¹ The objective of this study is to evaluate, in a vitro model, the size and depth of lesions made through simultaneous, sequential, or delayed epi–endocardial approach.

Methods

Samples

The left atrium tissue was obtained from freshly slaughtered porcine hearts, washed with NaCl 0.9% (B. Braun, Melsungen, Hessen, Germany) and put into a transport medium RPMI 1640 (Sigma-A Samples Aldrich, St Louis, MO, USA). This medium was also used for sample conservation.

The Simulator

The ABLA-BOX simulator (IDEE—Instrument Development Engineering and Evaluation, Maastricht University, The Netherlands) has been previously described.¹² Briefly, the chamber mimicking the internal part of the left atrium has an inlet and outlet access plugged into an external pump (COBE precision blood pump, COBE Cardiovascular Inc, Arvada, CO, USA) for blood circulation (Fig. 1a and b). A heating plate (IDEE—Instrument Development Engineering and Evaluation, Maastricht University, Maastricht, The Netherlands) and a heating exchange device (Bio Cal 370, Medtronic, Minneapolis, MN, USA) are employed to keep the temperature constant throughout the experiments. The stirring motor mimicking AF blood turbulence is connected with its dedicated controller (Cyclone 1Y100, HMCEurope, Tuessling, Germany). Two pressure transducers (AE sensors, Dordrecht, The Netherlands) allow accurate control of the applied forces.

Fig. 1

(a) Ablabox: 1 = pump flow outlet, 2 = endocardial catheter holder, 3 = pump flow inlet, 4 = heating plate, 5 = epicardial catheter holder. (b) Ablabox System: 1,2 = digital screen for catheter force application, 3 = heating plate control console, 4 = magnetic stirrer motor control console, 5,6 = catheter contact force sensors.

The 2 cm × 2 cm specimens were mounted between 2 plastic plates magnetically held to keep the samples of tissue firmly (Fig. 2).

Fig. 2

Specimen holder open and closed with its lid (a, b, c). Placement into the Ablabox (d, e, f).

Catheters

An epicardial pen (Isolator long-pen TT, AtriCure, Cincinnati, OH, USA) and an endocardial catheter (Celsius FLTR, Biosense Webster Inc, Diamond Bar, CA, USA) were employed. The epicardial catheter was plugged in a power console (Ablation Sensing Unit ASU, AtriCure, Cincinnati, OH, USA). In contrast, a Biosense Webster Stockert 70 RF Generator was used to power the endocardial catheter. The energy power was set up at 25 and 30 W (probe temperature, 65°C; impedance 100 Ω impedance; tissue temperature, 38°C) for the epicardial and the endocardial catheters, respectively.¹³

Experimental Setup

Left atrial tissue samples were randomly assigned to 3 groups, based on the time delay between the epicardial and the endocardial ablation application: (1) SEQ 0 (0-minute delay), i.e., simultaneous procedure; (2) SEQ 1 (60-minute delay); and (3) SEQ 2 (240-minute delay). A total of 60 samples were analyzed/studied (20 for each group).

The thicknesses of the samples were 4.3 ± 0.2, 4.2 ± 0.2, and 4.3 ± 0.2 in SEQ 0, SEQ 1, and SEQ 2, respectively (P ≥ 0.09).

In the delayed procedures (SEQ 1 and SEQ 2), the epicardial approach was performed first, followed by the endocardial ablation, to mimic the sequence in the clinical setting.¹ In all samples, the epicardial ablation cycle was automatically terminated by the console, whereas the endocardial ablation time was 30 seconds.

Based on our previous experiences,^12,14 the endocardial contact force was set up at 30 gr. From the epicardial side was chosen a 300 gr force as currently employed in surgery.

Moreover, the flow rate was set up at 5 L/min, the temperature at 38°C, and the stirrer motor at 400 rpm.

Morphometric Evaluation of Myocardial Tissue Ablation

The samples were included in 10% neutral buffered formalin (NBF) for 48 hours, immerged in a sucrose solution (20%), and finally put on a metallic disc and embedded to Tissue-Tek^® OCT ™ compound. The blocks obtained were put into a cryostat at −20°C and sliced in consecutive sections (100 µm) perpendicular to the direction of the catheter ablation. The slices were laid down on the acetate sheet and covered and dried at room temperature for 1 hour. Afterward, the slices were digitalized at 300 dpi using a flatbed scanner. Later, the images were imported into computer software for image processing (Image J version 1.48 software; National Institutes of Health, Bethesda, MD, USA). In total, we obtained 42.05 ± 4.33 layers from each sample, and for every single slice, total maximum diameter (D _max), total minimum diameter (D _min), and total ablated area (AA) were measured. Besides, for any slice, volume (V) was obtained multiplying the area by the thickness of a single slice, fixed to 100 µm by the setup of the cryostat. Likewise, maximum and minimum lesion’s diameter (D _epi and D _endo, d _epi and d _endo), area (a _epi and a _endo), and volume (v _epi and v _endo) were measured at both epicardial and endocardial sides (Fig. 3).

Fig. 3

Scheme of the measurements acquired: maximum endocardial diameter (D _endo), maximum epicardial diameter (D _epi), minimum endocardial diameter (d _endo), minimum epicardial diameter (d _epi), endocardial area (a _endo), epicardial area (a _epi), epicardial penetration volume (v _epi), endocardial penetration volume (v _endo).

Statistical Analysis

The Shapiro–Wilk normality test was performed and variables were expressed as median and interquartile range. Lesion measurements were compared with the Kruskal–Wallis test. Intraobserver and interobserver variabilities were tested on 5 samples randomly chosen, and κ-statistics were used to determine the degree of intraobserver and interobserver agreement after correction for the agreement expected by chance. The variables tested were D _max and AA. A κ-value has a maximum of 1.0 when the agreement is perfect. A value of 0 indicates no agreement better than chance agreement. All statistical analyses were conducted using SPSS Statistics Version 18.0 (SPSS Inc., Chicago, IL, USA).

Results

The intraobserver and interobserver variabilities were D _max (k = 0.98), AA (k = 0.93), and D _max (k = 0.88), AA (k = 0.86), respectively. During the experiment, no overheating steam pops occurred. Overall, no transmural lesion was identified (Fig. 4, Fig. 5). Morphometric data are shown in Table 1.

Fig. 4

Progression of lesions within the groups and the number of corresponding slices. There is no transmurality evidence. In the 1-stage sample, the ablation lesion disappears at the 27th slice, whereas in the other 2, the lesion stops before, showing a lower penetration.

Fig. 5

Lesion depth is plotted against tissue thickness. If the lesion is transmural, its point will fall on the line of identity. (a) SEQ 0 group, (b) SEQ 1 group, (c) SEQ 2 group.

Table 1

Ablation Lesion Results.

Measurements	Time points			P value
Measurements	SEQ 0	SEQ 1	SEQ 2	P value
Transmurality (%)	0	0	0
D _max (mm)	8.61 [3.25]	7.94 [3.17]^a	7.80 [2.76]^b	<0.001
D _min (mm)	7.10 [2.84]	5.91 [2.74]^a	5.81 [2.30]^b	<0.001
AA (mm²)	58.66 [43.23]	47.40 [43.73]^a	47.30 [36.83]^b	<0.001
V (mm³)	5.77 [4.39]	4.66 [4.52]^a	4.73 [3.68]^b	<0.001
D _epi (mm)	9.12 [3.53]	8.63 [2.77]^a	8.27 [2.47]^b	<0.001
D _endo (mm)	8.57 [2.40]	7.89 [2.84]^a	7.99 [2.18]^b	<0.001
d _epi (mm)	7.65 [2.59]	6.70 [2.26]^a	6.59 [2.16]^b	<0.001
d _endo (mm)	6.96 [2.42]	5.68 [2.40]^a	5.64 [1.79]^b	<0.001
a _epi (mm²)	66.72 [47.32]	62.44 [38.33]^a	61.43 [39.82]^b	0.014
a _endo (mm²)	57.01 [33.41]	45.43 [39.21]^a	45.13 [27.50]^b	<0.001
v _epi (mm³)	6.67 [4.73]	6.24 [3.83]^a	6.14 [3.98]^b	0.014
v _endo (mm³)	5.70 [3.34]	4.54 [3.92]^a	4.51 [2.75]	<0.001

Abbreviations: AA, total area; a _endo, endocardial area; a _epi, epicardial area; d _endo, minimum diameter endocardial side; D _endo, maximum diameter endocardial side; d _epi, minimum diameter epicardial side; D _epi, maximum diameter epicardial side;D _max, total maximum diameter; D _min, total minimum diameter; V, total volume; v _endo, endocardial volume; v _epi, epicardial volume.

Data are shown as median [interquartile range] or number (percentage).

All morphometric data were referred to single slices.

^asignificant SEQ 1 vs. 1-stage.

^bsignificant SEQ 2 vs. 1-stage.

Lesion Size

D _max was comparable between SEQ 1 and SEQ 2 (P = 0.149), but it was broader in SEQ 0 (P < 0.001). Also, D _min was larger in simultaneous ablated tissue compared to both SEQ 1 and SEQ 2 (both, P < 0.001), which did not show any difference between them (P = 0.118). Moreover, AA was different between 1-stage and SEQ 1 (P < 0.001) and SEQ 2 (P < 0.001) that were comparable (P = 0.706).

Additionally, D _epi did not differ in SEQ 1 and SEQ 2 (P = 0.121), while both resulted smaller than in the 1-stage (both, P < 0.001). Furthermore, D _endo was similar in SEQ 1 and SEQ 2 (P = 0.842), but lesions in both were smaller than in the 1-stage (P = 0.018 and P < 0.001, respectively). Besides, d _epi and d _endo were wider in 1-stage (both, P < 0.001), but they were comparable in SEQ 1 and SEQ 2 (P = 0.780 and P = 0.161, respectively).

Likewise, a _epi and a _endo were larger in 1-stage (a _epi, P = 0.031 vs. SEQ1 and P = 0.045 vs. SEQ2; a _endo, P < 0.001 vs. SEQ 1 and P < 0.001 vs. SEQ 2, respectively) but they did not differ between the 2-stage procedures (P = 0.965 and P = 0.295, respectively).

Lesion Depth

Likewise, V was similar in SEQ 1 and SEQ 2 (P = 0.997) but it was larger in 1-stage (P < 0.001 vs. both). Finally, v _epi and v _endo were comparable between SEQ 1 and SEQ 2 (P = 0.965 and P = 0.295, respectively), while it was bigger in 1-stage (v _epi, P = 0.031 vs. SEQ 1, P = 0.045 vs. SEQ 2; v _endo, P < 0.001 vs. SEQ 1, P < 0.001 vs. SEQ 2).

Discussion

Hybrid AF ablation is a treatment approach that combines thoracoscopic epicardial ablation with endocardial transcatheter ablation.^2,5,7 The epicardial step is performed first because it allows long-lasting isolation of the pulmonary veins and the creation of additional lines in the left atrium, resulting in a so-called box lesion.⁴ The second part, carried out by the electrophysiologist, consists of mapping-guided demonstration of entry/exit block and offers the possibility of additional tailored substrate modification.

Although hybrid AF ablation is well defined as a concept, the time frame between both steps is not so clearly specified yet, and varies from a few hours up to 6 months.^8,10,15 For example, Mahaptra et al. performed the endocardial procedure 4 days after the surgical ablation,^16,17 and the other clinicians 30 to 45 days after the surgical procedure.^15,18 Bulava et al. completed the second step 6 to 8 weeks after surgery,¹⁰ and Gaita and co-workers carried out the catheter ablation after a blanking period of 3 months.¹⁹ Other clinicians performed either 1-stage or 2-stage procedures.^20
-22 Supporters of the delayed approach claim that a catheter ablation performed in a second stage significantly increases the likelihood of identifying conduction gaps in the surgical lesions, which potentially translates in a higher mid-term success rate.^15,18 Advocators of a contemporary approach argue that it strengthens the cooperation and mutual understanding between the surgeon and the electrophysiologist. Nonetheless, results were comparable in series using both approaches.²²

However, the superiority of one technique over the others is still debated.²³ As far as we know, no study has specifically addressed this issue. Furthermore, no evidence exists on simultaneous ablation, performed in 1 step with the atrial tissue interposed between the catheters.

In this study, we tested whether simultaneous ablation results in deeper transmural lesions compared to 1-stage ablation (SEQ 1, after 60 minutes) or sequential ablation (SEQ 2, after 240 minutes). The tests were performed on the ABLA-BOX that allows to control contact force, blood temperature, and flow to mimic physiological conditions.¹⁴

In our observations, we checked diameter maximum, diameter minimum, ablated area, ablated volume, as well as maximum and minimum diameters and volumes measured at epicardial and endocardial sides.

We observed smaller ablation diameters on the endocardial surface compared to the epicardial one (P < 0.001). This finding is not surprising because of the different sizes and shapes and differences in the applied force of the 2 catheters. Nonetheless, noteworthy is that all the lesions measured were larger in the 1-stage samples.

D _max and D _min, and consequently AA and V, were significantly larger in the 1-stage group. First, this might be the result of a deeper penetration during simultaneous ablation, as a result of higher forces, and thus better contact. Nonetheless, we failed to find transmurality in the samples. We might postulate that the pressure applied from both sides reduces the extracellular space of tissue, increasing its impedance,²⁴ leading to lateral irradiation of the radiofrequency. This lateral irradiation could lead to energy loss that may be responsible for the lack of transmurality. Importantly, we could expect that the tissue compression negatively affects the penetration of RF, but, in contrast, we found that the penetration into the tissue, expressed as volume v _endo and v _epi, was higher in the 1-stage group (P < 0.001). In contrast, we failed to find any difference between the 60- and 240-minute delay (P = 0.29). This difference could be attributed to the higher contact force of the epicardial catheter. Nonetheless, despite the contact, the force applied was the same in the 3 groups, and v _epi and v _endo were higher in the 1-stage samples, so this is more likely related to RF physics properties. Indeed, it is known that approximately 90% of the RF energy delivered is adsorbed in the first 1 mm of tissue, and the remainder of tissue heating occurs for indirect conduction. The heating transmission inside the tissue is slower than the RF, and, for this reason, the heating continues rising for several seconds after RF delivery interruption (thermal latency phenomenon).²⁵

In our previous experience,¹⁴ we obtained transmural lesions using a different setup. In the experiments reported here, we tried to mimic clinical settings. For instance, the endocardial contact force was set up to 300 gr and the endocardial force at 30 gr and endocardial impedance close to ideal 120 Ω.²⁶ Therefore, we might postulate that the lower impedance, employed in our previous experiments, as well as the difference in tip temperature, could explain the different outcomes.

However, it can be concluded from our findings that the lack of transmurality was not related to different time frames between the endocardial and the epicardial step, and this is a call for specifically improved catheters with optimized design for hybrid AF ablation.

To address the lateral dispersion and enhance more penetration by the RF energy, after some preliminary tests, we are developing a specific “true-bipolar” catheter with the atrial tissue compressed between the 2 ablation poles. This prototype will be the object of an upcoming study. The aim is to obtain fully linear transmural ablations in 1 step and to get a complete, effective left atrium isolation, which is a key feature of AF ablation.^27,28

Also, the lack of postablation edema that, in vivo, may reduce the lesion effectiveness^10,23 prevents us from drawing conclusions. Hence, further in vivo studies to compare 1-step, sequential, and delayed approaches, including electromapping and pathophysiologic changes, are needed.

Finally, the findings from the study add to the voluminous experimental and clinical evidence that unipolar RF does not reliably produce linear, transmural lesions.

However, our findings must be read with caution. Indeed, the real application of simultaneous epi–endocardial ablation is far from being applied to the hybrid clinical arena. Further research is necessary to explore the reliability and feasibility of this technique and whether the challenges entailed in the implementation of this technique can be overcome.

Limitations

Our study suffers from some limitations that should be highlighted. First, we did not make histological evaluations to demonstrate the necrosis induced by the RF. The “TUNEL” (Terminal deoxynucleotidyl transferase [TdT] dUTP Nick-End Labeling) assay might have been the best method for indicating the necrosis but, in our setup, it was impossible due to the number of layers from each sample. This technique is mainly in use, and it has been designed to detect apoptotic cells undergoing extensive DNA degradation during the late stages of apoptosis. It is based on the ability of TdT to mark the blunt ends of double-stranded DNA breaks following apoptosis as well as other forms of cellular necrosis .^29
-31 Second, we employed tools that were not designed to be used simultaneously. Therefore, the lack of transmurality may be due to the in vitro setup and the characteristics of the catheters used, and this must be taken into account when reading our results.

Third, dead tissue was used, thus excluding all pathophysiologic mechanisms occurring in vivo. In addition, the absence of microvascularization that performs as a heat sink decreases the penetration of RF in alive tissue.²⁵ Fourth, we did not test other devices. This was beyond the aims of our paper, but it will be the object of further research.

Fifth, the delay from the first ablation not being longer than 240 minutes related to tissue conservation issues. Furthermore, we did not perform multiple ablations. This issue might have led to improved depth of penetration. Sixth, the tissue employed was not viable, and as a consequence, either microcirculation or intrinsic electrophysiological properties were absent, thus excluding all pathophysiologic mechanisms occurring in vivo in response to heating stress. In addition, the absence of microvascularization that performs as a heat sink decreases the penetration of RF in alive tissue.²⁵ These aspects may limit the applicability to the clinical settings, and thus data have to be confirmed in further studies with a different setup.

Finally, porcine tissue came from young, healthy, 7-month- to 1-year-old animals bred for human consumption. It is likely that the heart tissue did not show any pathologic event typical of AF, like fibrosis development.

Conclusions

In this ex vivo evaluation of different hybrid procedure techniques, 1-stage, sequential, and delayed, transmurality was not reached by any procedure. Nonetheless, the 1-stage approach showed deeper and broader lesions. Our findings need to be confirmed by further research.

Supplemental Material

Visual Abstract - Supplemental material for One-Stage Versus Sequential Hybrid Radiofrequency Ablation: An In Vitro Evaluation

Supplemental material, Visual Abstract, for One-Stage Versus Sequential Hybrid Radiofrequency Ablation: An In Vitro Evaluation by Francesco Matteucci, Bart Maesen, Kevin Vernooy, Carlo De Asmundis, Jos G. Maessen, Mark La Meir and Sandro Gelsomino in Innovations: Technology and Techniques in Cardiothoracic and Vascular Surgery

Footnotes

Authors’ Contributions

All authors actively contributed to the paper in the following domains: conception or design of the work, data collection, data analysis, and interpretation, drafting the article, critical revision of the article, final approval of the version to be published.

The last two authors equally contributed to the paper.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Bart Maesen

Sandro Gelsomino

References

La Meir

Gelsomino

Lorusso

et al. The hybrid approach for the surgical treatment of lone atrial fibrillation: one-year results employing a monopolar radiofrequency source. J Cardiothorac Surg 2012; 7: 71.doi:10.1186/1749-8090-7-71

http://www.ncbi.nlm.nih.gov/pubmed/22812613

Pison

La Meir

van Opstal

et al. Hybrid thoracoscopic surgical and transvenous catheter ablation of atrial fibrillation. J Am Coll Cardiol 2012; 60: 54–61.doi:10.1016/j.jacc.2011.12.055

http://www.ncbi.nlm.nih.gov/pubmed/22742400

de Asmundis

Chierchia

GB.

Mugnai

et al. Midterm clinical outcomes of concomitant thoracoscopic epicardial and transcatheter endocardial ablation for persistent and long-standing persistent atrial fibrillation: a single-centre experience. Europace 2017; 19: 58–65.doi:10.1093/europace/euw026

http://www.ncbi.nlm.nih.gov/pubmed/27247011

Maesen

Pison

Vroomen

et al. Three-year follow-up of hybrid ablation for atrial fibrillation. Eur J Cardiothorac Surg 2018; 53(suppl_1): i26–i32.doi:10.1093/ejcts/ezy117

http://www.ncbi.nlm.nih.gov/pubmed/29590387

van der Heijden

CAJ.

Vroomen

Luermans

et al. Hybrid versus catheter ablation in patients with persistent and longstanding persistent atrial fibrillation: a systematic review and meta-analysis. Eur J Cardiothorac Surg 2019; 56: 433–443.doi:10.1093/ejcts/ezy475

http://www.ncbi.nlm.nih.gov/pubmed/30698685

Maesen

Weberndörfer

Bidar

et al. The importance of bipolar bidirectional radiofrequency in surgical AF ablation. Int J Cardiol Heart Vasc 2020; 26: 100478.doi:10.1016/j.ijcha.2020.100478

http://www.ncbi.nlm.nih.gov/pubmed/32142078

Marchlinski

Kumareswaran

. Hybrid ablation for atrial fibrillation: better or just different? JACC Clin Electrophysiol 2017; 3: 350–352.doi:10.1016/j.jacep.2016.12.020

http://www.ncbi.nlm.nih.gov/pubmed/29759447

Pison

Gelsomino

Luc

et al. Effectiveness and safety of simultaneous hybrid thoracoscopic and endocardial catheter ablation of lone atrial fibrillation. Ann Cardiothorac Surg 2014; 3: 38–44.doi:10.3978/j.issn.2225-319X.2013.12.10

http://www.ncbi.nlm.nih.gov/pubmed/24516796

Umbrain

Verborgh

Chierchia

et al. One-stage approach for hybrid atrial fibrillation treatment. Arrhythm Electrophysiol Rev 2017; 6: 210–216.doi:10.15420/2017.36.2

http://www.ncbi.nlm.nih.gov/pubmed/29326837

10.

Bulava

Mokracek

Hanis

et al. Sequential hybrid procedure for persistent atrial fibrillation. J Am Heart Assoc 2015; 4: e001754.doi:10.1161/JAHA.114.001754

http://www.ncbi.nlm.nih.gov/pubmed/25809548

11.

McGann

CJ.

Kholmovski

EG.

Oakes

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 2008; 52: 1263–1271.doi:10.1016/j.jacc.2008.05.062

http://www.ncbi.nlm.nih.gov/pubmed/18926331

12.

Lozekoot

PW.

de Jong

MM.

Parise

et al. The ABLA-BOX: an in vitro module of hybrid atrial fibrillation ablation. Innovations 2016; 11: 201–209.doi:10.1097/imi.0000000000000256

http://www.ncbi.nlm.nih.gov/pubmed/27355130

13.

Vaccari

Giacopelli

Rocchetto

et al. Atrial fibrillation radiofrequency ablation: safety using contact force catheter in a low-volume centre. J Atr Fibrillation 2014; 7: 1043.doi:10.4022/jafib.1043

27957093

14.

Lozekoot

PW.

de Jong

MM.

Gelsomino

et al. Contact forces during hybrid atrial fibrillation ablation: an in vitro evaluation. J Interv Card Electrophysiol 2016; 45: 189–197.doi:10.1007/s10840-015-0089-y

http://www.ncbi.nlm.nih.gov/pubmed/26728030

15.

Muneretto

Bisleri

Bontempi

et al. Durable staged hybrid ablation with thoracoscopic and percutaneous approach for treatment of long-standing atrial fibrillation: a 30-month assessment with continuous monitoring. J Thorac Cardiovasc Surg 2012; 144: 1460–1465.doi:10.1016/j.jtcvs.2012.08.069

http://www.ncbi.nlm.nih.gov/pubmed/23062968

16.

Mahapatra

LaPar

DJ.

Kamath

et al. Initial experience of sequential surgical epicardial-catheter endocardial ablation for persistent and long-standing persistent atrial fibrillation with long-term follow-up. Ann Thorac Surg 2011; 91: 1890–1898.doi:10.1016/j.athoracsur.2011.02.045

http://www.ncbi.nlm.nih.gov/pubmed/21619988

17.

Lee

HM.

Chung

SR.

Jeong

. Initial experience with total thoracoscopic ablation. Korean J Thorac Cardiovasc Surg 2014; 47: 1–5.doi:10.5090/kjtcs.2014.47.1.1

http://www.ncbi.nlm.nih.gov/pubmed/24570858

18.

Bisleri

Rosati

Bontempi

et al. Hybrid approach for the treatment of long-standing persistent atrial fibrillation: electrophysiological findings and clinical results. Eur J Cardiothorac Surg 2013; 44: 919–923.doi:10.1093/ejcts/ezt115

http://www.ncbi.nlm.nih.gov/pubmed/23475587

19.

Gaita

Ebrille

Scaglione

et al. Very long-term results of surgical and transcatheter ablation of long-standing persistent atrial fibrillation. Ann Thorac Surg 2013; 96: 1273–1278.doi:10.1016/j.athoracsur.2013.05.054

http://www.ncbi.nlm.nih.gov/pubmed/23915587

20.

Zembala

Filipiak

Kowalski

et al. Minimally invasive hybrid ablation procedure for the treatment of persistent atrial fibrillation: one year results. Kardiol Pol 2012; 70: 819–828.http://www.ncbi.nlm.nih.gov/pubmed/22933215

21.

Richardson

TD.

Shoemaker

MB.

Whalen

et al. Staged versus simultaneous thoracoscopic hybrid ablation for persistent atrial fibrillation does not affect time to recurrence of atrial arrhythmia. J Cardiovasc Electrophysiol 2016; 27: 428–434.doi:10.1111/jce.12906

http://www.ncbi.nlm.nih.gov/pubmed/26725742

22.

Gersak

Pernat

Robic

et al. Low rate of atrial fibrillation recurrence verified by implantable loop recorder monitoring following a convergent epicardial and endocardial ablation of atrial fibrillation. J Cardiovasc Electrophysiol 2012; 23: 1059–1066.doi:10.1111/j.1540-8167.2012.02355.x

http://www.ncbi.nlm.nih.gov/pubmed/22587585

23.

Vroomen

Pison

. Hybrid ablation for atrial fibrillation: a systematic review. J Interv Card Electrophysiol 2016; 47: 265–274.doi:10.1007/s10840-016-0183-9

http://www.ncbi.nlm.nih.gov/pubmed/27613183

24.

Moqadam

SM.

Grewal

Shokoufi

et al. Compression-dependency of soft tissue bioimpedance for in-vivo and in-vitro tissue testing. J Electr Bioimpedance 2015; 6: 22–32.doi:10.5617/jeb.1489

25.

Issa

ZF.

Miller

JM.

Zipes

. Chapter 7 - Ablation Energy Sources. In: Issa

ZF.

Miller

JM.

Zipes

DP.

(eds) Clinical Arrhythmology and Electrophysiology: A Companion to Braunwald’s Heart Disease. Second Edition. Philadelphia: W.B. Saunders, 2012, pp.144–163.

26.

Bhaskaran

Barry

MA.

Pouliopoulos

JIM

et al. Circuit impedance could be a crucial factor influencing radiofrequency ablation efficacy and safety: a myocardial phantom study of the problem and its correction. J Cardiovasc Electrophysiol 2016; 27: 351–357.doi:10.1111/jce.12893

http://www.ncbi.nlm.nih.gov/pubmed/26648095

27.

Zhou

Chen

et al. Left atrial posterior wall isolation reduces the recurrence of atrial fibrillation: a meta-analysis. J Interv Card Electrophysiol 2016; 46: 267–274.doi:10.1007/s10840-016-0124-7

http://www.ncbi.nlm.nih.gov/pubmed/26971331

28.

Kim

J-S.

Shin

SY.

et al. Does isolation of the left atrial posterior wall improve clinical outcomes after radiofrequency catheter ablation for persistent atrial fibrillation? A prospective randomized clinical trial. Int J Cardiol 2015; 181: 277–283.doi:10.1016/j.ijcard.2014.12.035

http://www.ncbi.nlm.nih.gov/pubmed/25535691

29.

Kyrylkova

Kyryachenko

Leid

. Detection of Apoptosis by TUNEL Assay. In: Kioussi

(ed) Odontogenesis: Methods and Protocols. Totowa, NJ: Humana Press, 2012, pp.41–47.

30.

Ansari

Coates

PJ.

Greenstein

et al. In situ end-labelling detects DNA strand breaks in apoptosis and other physiological and pathological states. J Pathol 1993; 170: 1–8.doi:10.1002/path.1711700102

http://www.ncbi.nlm.nih.gov/pubmed/8326456

31.

Nishiyama

Kwak

Takekoshi

et al. In situ nick end-labeling detects necrosis of hippocampal pyramidal cells induced by kainic acid. Neurosci Lett 1996; 212: 139–142.doi:10.1016/0304-3940(96)12794-4

http://www.ncbi.nlm.nih.gov/pubmed/8832658

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