Cover Story

How to Protect the Esophagus: A Review of Past, Present, and Future Approaches

Linda Moulton, RN, MS; Faculty, Order and Disorder EP Training Program;
Critical Care ED/CCE Consulting; Calistoga, California

Linda Moulton, RN, MS; Faculty, Order and Disorder EP Training Program;
Critical Care ED/CCE Consulting; Calistoga, California

With 5 million new cases of atrial fibrillation (AF) each year, AF is considered the most common sustained arrhythmia in clinical practice worldwide.1 Approximately 50,000 patients undergo a catheter ablation each year in the United States.1 For many operators, the ablation procedure has evolved into isolation of the pulmonary veins plus creation of box lesion lines on the posterior wall of the left atrium (LA). The esophagus is immediately adjacent to the posterior wall, and is therefore vulnerable to thermal injury from these lesion sets (Figure 1). Thus, one of the most worrisome complications of AF ablation has been the development of atrioesophageal lesions post procedure, the rate of which has been reported at between 2-47%.2

Progression to atrioesophageal fistula has been reported in 0.1-0.2%3; these fistulas account for 16% of post-procedure deaths4, with a 55% overall mortality rate.1 Atrioesophageal fistula formation has been reported with radiofrequency (RF), cryoballoon, high-intensity focused ultrasound (HIFU), surgical, laser, and robotic-assisted ablation. The following is a review of the pathophysiology, presentation, diagnosis, treatment, and attempts to prevent this potentially deadly complication.

Pathophysiology and Possible Contributors

It is believed that the esophageal lesions that occur during ablation are produced from thermal injury to the microvasculature. This evolves into progressive inflammation, injury from swallowing and gastric reflux, and progression to perforation and fistula5 with air and food extravasation into the LA. In addition, the vagus nerve and its branches are close to the posterior wall and may be being injured.6 The vagus is involved with motor control of the stomach, and damage to this nerve could contribute to GI reflux and gastric hypermotility.

The LA posterior wall thickness can vary between 1.58 ± 0.22 mm for the mid-posterior wall and 1.74 ± 0.18 mm for the infero-posterior wall.7 Wall thickness could be a factor in lesion development. Also of importance is the distance between the LA posterior wall and esophageal wall, which was <5 mm in 40% of specimens studied by Sanchez-Quintana et al.8 The distance of the esophagus from the left inferior pulmonary vein (LIPV) can be as low as 2.8 ± 2.5 mm.9 LA enlargement could be a factor10; Fakaya et al reported on a case with a dilated esophagus.11 A correlation between smaller body mass index (BMI) and a shorter esophagus to LA distance (AED) has been reported.12 Ito et al found that fistulas were closely associated with a contrast computed tomography distance between the esophagus and posterior LA of <2.9 mm.13 Sarairah et al performed pre-procedural MRI to evaluate the esophageal lumen in 95 patients who underwent cryoablation for AF; intraprocedural esophageal luminal temperature and balloon temperatures were recorded and a 24-hour post upper endoscopy was performed.14 They found 21 esophageal thermal injuries (20 mild, and 1 severe); GI reflux was associated with increased risk, while a wider esophageal lumen and esophageal wall thickness were protective.14

The esophagus may also shift position during the ablation procedure and become more of a direct target. A recently published study by Stauber et al looked at esophageal position, temperature, and endoscopy follow-up of 645 AF ablation patients.15 They found lesion development was most dependent on esophageal position and temperature, but not with BMI. However, esophageal temperature and position had no effect on arrhythmia recurrence. Of the 15 patients in which an endoscopically detected esophageal lesion was found, the median esophageal temperature was 41.8°C.15 The highest temperatures were recorded when the esophageal position was behind the left pulmonary veins to left ostial position, and the right ostial to right pulmonary vein regions, and not midline.

General anesthesia has been implicated as a contributor to esophageal lesions. Di Biase et al reported on a study of 50 patients undergoing RF ablation for atrial fibrillation randomized to general anesthesia versus conscious sedation.16 Capsule endoscopy was performed post procedure. The general anesthesia group had a 48% lesion rate, while the conscious sedation group was 4%. The authors attributed the difference to reduced motility and peristalsis during general anesthesia, exposing the same area of the esophageal tissue to RF injury. They believed that with conscious sedation, pain from RF could trigger active peristalsis and swallowing, leading to cooler and more inconsistent heat transfer, and thus be more protective.16

Atrioesophageal fistula formation after cryoballoon ablation is rare and is most commonly identified near the LIPV.17 It is thought that a more posteriorly directed force is required when ablating this area, so the distance is lessened.17 A study from Japan found that use of the second-generation cryoballoon increased the incidence of silent periesophageal nerve injury, even after short freeze times.18 It was thought that cases where temperature probes were used had an increased risk of lesion formation. The risk of silent gastric hypomotility was more than that reported with RF. The distance between the right inferior pulmonary vein (RIPV) and the esophagus was the sole independent predictor of gastric hypomotility. They speculated that the esophagus was wedged between the balloon anteriorly and the thoracic spinal column or aorta posteriorly in that ablation site.18

Yarlagadda et al proposed the novel Kansas City classification system for esophageal lesions (Table 1).19 They conducted a retrospective analysis of 30 studies in which patients underwent endoscopy within 1 week post procedure. They categorized the findings into 3 main types of lesions: type 1 (erythema); type 2a (superficial ulcers); type 2b (deep ulcer); type 3a (perforation without communication with atria); and type 3b (perforation with atrio-esophageal fistula). They then proceeded to look at treatment outcomes.

Symptoms

Patients present with symptoms of esophageal injury anywhere between 0-60 days post ablation.1 Reported symptoms include fever, septic shock, hypotension, rigors, focal neurology, seizures, confusion, loss of consciousness, hematemesis, melena, dysphagia, nausea, vomiting, chest pain, dyspnea, and palpitations. Barbhaiya et al found that gastroparesis and esophageal injury diagnosed in the first 5 days after ablation usually resolved spontaneously, but that symptoms occurring more than 5 days after the procedure signaled a more severe situation.20

Diagnosis

Use of post-procedure endoscopy has been suggested to identify high-risk patients. Halbfass et al3 found asymptomatic esophageal lesions detected by endoscopy in ≤40% post ablation; 18% of asymptomatic patients had lesions detected endoscopically, and one-third of these were categorized as ulcers. However, endoscopy should be avoided once a fistula is suspected. Esophagogastroduodenoscopy (EGD) in this setting has caused deterioration and some reported deaths.1 For a suspected fistula, contrast-enhanced computed tomography is recommended.1

Treatment

Yarlagadda et al reviewed the outcomes of patients included in each group of the Kansas City classification.19 All type 1 and most of the type 2 lesions were resolved with conservative management. Of the type 2b lesions, six progressed to perforation (5 to type 3a, and 1 to type 3b). Of the 5 in the type 3a group, 1 was fatal; the type 3b was also fatal. The authors suggested that if a fistula is suspected, a CT of the chest with oral and IV contrast should be performed. If perforation or fistula is seen on CT, this should be considered a surgical emergency. Treatments ranged from stent to omental/muscle wrap to esophagectomy, depending on the clinical situation. If the CT is negative, the patient should be followed closely. EGD was found to cause further damage in high-grade lesions.

In the study by Zhang et al21, management was guided by the Kansas City scoring criteria. Group 1 received a semi-solid diet with administration of proton pump inhibitors (PPIs). Group 2 received IV PPIs and fasted until repeat endoscopic ultrasonography showed resolution or improvement to type 1. If recovery exceeded 7 days, a jejunal feeding tube was placed. Lesions were classified as type 3 if contrast-enhanced CT showed extravasation of air or oral contrast media from the esophagus to mediastinum, pericardium, or LA. If a type 3 was determined, pericardiocentesis and drainage, intubation, nutritional support, and surgical repair were initiated. Other authors have reported use of an autologous pericardial patch22, vascular omental wrap23, and latissimus dorsi muscle interposition flap to wrap the esophagus.24 The use of stents remains controversial.1,3,21

Prevention

A variety of preventive measures have been tried or have evolved in an attempt to prevent esophageal injury. Some of these will be reviewed in addition to some specific recommendations for energy delivery modes other than radiofrequency.

The use of irrigated catheters has been suggested due to the ability to more quickly produce a deeper lesion and not transmit as much heat to the esophagus.26 Low-flow irrigation has also been tried.27

Attempts at decreasing energy delivery near the esophagus to 25-30W, ablating for shortened durations (such as <20-30 sec), and applying less contact force have been recommended. Borne et al28, using bovine myocardium, tested delivery of different powers and time intervals, and analyzed depth and volumes of the lesions created. Variable power and durations led to different lesion types that could be a guide to lesion creation more appropriate for individual substrates. Shallower lesions may be safer near the esophagus. The Ablation Index (AI) was developed as a quality marker of energy delivery incorporating contact force, time, and power into a weighted formula that predicts lesion size and outcomes.29 Additionally, Taghji et al30 reported on the CLOSE protocol, in which 130 patients with paroxysmal AF received encircling PV lesions with contact force contiguous radiofrequency targeting an inter-lesion distance ≤6 mm and an AI ≥400 at the posterior wall and ≥550 at the anterior wall. No fistulas were reported in follow-up.

Contact force recommendations have varied. Contact force >15g at 50W is more likely to cause lesions. Keeping the level <10-15g with lower power is seen as more protective.31,32

High power short duration (HPSD) lesion formation is believed to be a shift to resistive heating rather than conductive tissue heating, thus decreasing lesion depth and limiting collateral tissue damage.33 In CLOSE-PVI, esophageal and periesophageal injury were evaluated with endoscopy 9 ± 4 days post procedure after the use of HPSD, investigating incidences of esophageal temperature rises. Esophageal erythema/erosion was found in 1 out of 85 patients (1.2%) and no ulceration was reported.34 However, Baher et al35 compared HPSD to lower power longer duration (LPLD) and found similar esophageal outcomes between groups, and 2.5-year rhythm recurrence rates were similar.

Thermal insulation of the esophagus has been tried as a method to prevent lesion formation. A device used to induce hypothermia has found its way into the electrophysiology lab. The ensoETM device (Attune Medical) is used to induce hypothermia, usually with the goal of brain protection. It has a dual-lumen silicone tube to circulate cold distilled water. Temperature control is maintained via the Blanketrol III mobile console (Gentherm Medical). Temperature can be maintained between 4-42° C. In the electrophysiology lab, the idea is to cool the esophagus during the ablation procedure to prevent thermal injury. Pre-clinical studies were performed and the results of the IMPACT study were recently reported.36-38 This was a 1:1 randomization with a 38°C ablation cutoff. The group with the cooling device had esophageal temperature maintained at 4°C. Endoscopy was performed within 7 days post procedure. In the control group, thermal injury occurred in 12 out of 60 patients. The group receiving esophageal protection had thermal injury in 2 out of 60 cases. A recent meta-analysis of 9 studies using the cooling system confirmed that severity of lesions was reduced.39

The use of a high-resolution infrared thermography to measure peak esophageal temperature has been reported on in a couple of studies.40,41 The research, supported in part by grants from Securus Medical, concludes that infrared thermography seems to accurately predict peak esophageal temperature during ablation. The esophageal temperature is continuously monitored in the system by attaching the esophageal catheter to an external infrared detector. Infrared energy is collected from 360 degrees over a 6 cm length of esophagus. More than 7680 temperature measurements are collected per second. The data is displayed quickly and accurately. In these studies, the peak esophageal temperature predicted post ablation endoscopy results. Temperatures of 50°C predicted endoscopically detected lesions. Temperatures below 50°C produced no lesions.

Mechanical deflection of the esophagus was attempted at least as early as 2012.42 Initial efforts involved an off-the-shelf metal stylet and tube. Deviation >20 mm from the PV ablation line prevented esophageal heating, but was difficult to achieve.43 There was also trauma due to the instrumentation in many patients.42,43 A couple of products have been developed for this purpose since then. One is the DV8 Retractor (Manual Surgical Sciences), a polyurethane balloon wrapped with a silicone sleeve that is used to move the esophagus. The device has a port to inject contrast to opacify and delineate the esophageal lumen. There is a second port for inflation. As the balloon is inflated, it takes a predefined deflection shape. In order to move it to each side, it is deflated, rotated, and then re-inflated. Bhardwaj et al44 studied the safety and feasibility of the device. They were able to safely move the esophagus from the site of energy delivery during ablation. Two patients had oropharyngeal bleeding, which was treated. A lower temperature rise was recorded with luminal esophageal temperature (LET) monitoring, and the mean esophageal movement achieved was 18.4 ± 8.7 mm. The other esophageal deviation device is the EsoSure Esophageal Retractor (Northeast Scientific). This is a temperature-programmed stylet that can change shape at body temperature. Parikh et al studied the safety and efficacy of the EsoSure in 209 patients.45 The device was used when LET rise occurred and if the esophagus was in the ablation line. There were no complications and only transient sore throats.

LET monitoring has been used to monitor esophageal temperature during ablation for a number of years. The information from these devices has given physicians the ability to know when the esophageal temperature exceeds a safe level. However, LET monitoring has not been entirely without issues. In a major review of LET studies, Assis et al reported cut-off ranges from 38.5-42°C in various protocols.46 A high incidence of ulcer formation was found in each and some with deeper lesions. They questioned whether inside temperature adequately reflects what is happening on the outer esophagus. There also seem to be problems with malalignment of probes to the LA posterior wall. Halbfas et al3 believe there are problems with thermal latency and incomplete temperature surveillance coverage of the esophagus, which are drawbacks for use of LET monitoring. Two studies suggested that temperature probes have become a risk factor if they have uncoated stainless-steel thermocouples, causing an inductive heating process, and therefore, an increased risk of esophageal damage.3,47 However, Perez et al developed a computational model to assess the electrical and thermal effects of three different esophageal temperature probes.48 One had a single sensor, one had a multisensor with a metallic surface, and one had a multisensor without a metallic surface. They found that the temperature rise in the esophageal wall and the probes was produced by thermal conduction, and was not related to an interaction between the ablation catheter and probe of an electrical and/or thermal nature, or “antenna” effect. Finally, a study by Turagam et al evaluated 22 commercial esophageal temperature probes.49 They found variations in transient thermal response, such that there may be an underestimation of LET. The CIRCA S-CATH Esophageal Temperature Probe (10 French) (CIRCA Scientific) had the lowest mean thermal time and the fastest time to peak temperature in their study.

Gastric acid suppression for 6 weeks post procedure has been recommended for lesion prophylaxis. This would include histamine-2 receptor blockers (eg, ranitidine, famotidine, or cimetidine) or PPIs (pantoprazole, omeprazole, and lansoprazole) to decrease acid reflux. No randomized trials have been conducted to study these approaches.

Specific Prevention Measures for Non-RF Techniques

The issue with cryoablation is to make sure the esophageal tissue is not damaged from excessive freezing. Recommendations include limiting freeze time to 180-second dosing, but also needing to look at the cumulative dose.32 Temperature cutoff recommendations have varied from 10-15°C.51-53 A study from Deiss et al with 29 patients using the second-generation cryoballoon found that after termination of cryofreezing, the temperature may decline an additional 6.4°C, suggesting that cut-offs should consider this.50

A method of monitoring for esophageal damage during laser catheter ablation is taking a different direction.54 Use of the SensoLas light sensor (SLLS; LasCor GmbH) plus focused local atrial electrograms has been tried in an in vitro porcine model and in vivo canine model. The sensor is passed into the esophagus through a transparent esophageal probe. The SLLS captures information about the photons scattering through the atrial and esophageal walls, sends this via an optical fiber to a diode, and creates a power display on a monitor. The laser application is stopped automatically as power reaches a preset upper limit. Bipolar local electrograms are simultaneously recorded from the laser catheter to monitor for the reduction/loss of electrical potentials.

Something a Little Different

What if the posterior wall was not ablated? The question of whether or not the posterior wall lesion set makes a difference in outcomes was explored by Lee et al.55 They randomized a group of 217 persistent AF patients to a procedure with or without inclusion of posterior wall isolation to determine if the wall isolation actually led to improved rhythm outcomes. Inclusion of the posterior wall did not improve rhythm outcome or influence the type of atrial arrhythmia recurrence at 16.2±8.8 months follow-up. The 1-year recurrence rate was substantial regardless of the approach, and the difference was not significant. More such randomized trials could prove interesting.

A couple of entirely different ablation approaches are also looking promising: electroporation and radiotherapy. Electroporation involves the changing of the membrane of a cell through the use of an electrical field.56 Application of this technique for treatment of arrhythmias is called pulsed field ablation. The technique is nonthermal and tissue selective. Myocardial cells have a lower threshold for cell damage, so they are more sensitive to the electrical field. However, the nerves and esophagus are spared.57-59

Radiotherapy or radioablation borrows the knowledge gleaned from the oncology realm, where the ability to target very specific areas for treatment has been developed. In the case of AF, a computer program identifies the area that would normally be ablated and radiation is delivered, avoiding the esophageal region.60-63 This technique also looks really exciting.

Discharge

The importance of providing explicit discharge information about symptoms of esophageal lesions to the patient, family, and primary care provider cannot be emphasized enough. A list of reasons to contact a physician should include the development of chest pain, fever, dysphagia, hematemesis, melena, neurologic symptoms, and dyspnea (Table 3). In addition, emergency room staff should be educated about the importance of these symptoms for the post-ablation patients who may seek their care.

We know quite a bit about the fate of the esophagus during AF ablation and have some great potential approaches to provide protection, but there are still many questions. The science is evolving. 

Disclosures: The author has no conflicts of interest to report regarding the content herein. 

References
  1. Han HC, Ha FJ, Sanders P, et al. Atrioesophageal fistula: clinical presentation, procedural characteristics, diagnostic investigations, and treatment outcomes. Circ Arrhythm Electrophysiol. 2017;10(11):e005579.
  2. de Oliveira B, Oyama H, Hardy C, et al. Comparative study of strategies to prevent esophageal and periesophageal injury during atrial fibrillation ablation. J Cardiovasc Electrophysiol. 2020;31(4):924-933.
  3. Halbfass P, Pavlov B, Muller P, et al. Progression from esophageal thermal asymptomatic lesion to perforation complicating atrial fibrillation ablation: A single-center registry. Circ Arrhythm Electrophysiol. 2017;10(8):e005233.
  4. Nair KKM, Shurrab M, Skanes A, et al. The prevalence and risk factors for atrioesophageal fistula after percutaneous radiofrequency catheter ablation for atrial fibrillation: the Canadian experience. J Interv Card Electrophysiol. 2014;39(2):139-144.
  5. Grubina R, Cha Y, Bell MR, Sinak LJ, Asirvatham SJ. Pneumopericardium following radiofrequency ablation for atrial fibrillation: Insights into the natural history of atrial esophageal fistula formation. J Cardiovasc Electrophysiol. 2010;21:1046-1049.
  6. Bunch TJ, Ellenbogen KA, Packer DL, Asirvatham SJ. Vagus nerve injury after posterior atrial radiofrequency ablation. Heart Rhythm. 2008;5:1327-1330.
  7. Hayashi H, Hayashi M, Mujauchi Y, et al. Left atrial wall thickness and outcomes of catheter ablation for atrial fibrillation in patients with hypertrophic cardiomyopathy. J Interv Card Electrophysiol. 2014;40(2):153-160.
  8. Sanchez-Quintana D, Cabrera JA, Climent V, Farre J, de Mendoca MC, Ho SY. Anatomic relations between the esophagus and left atrium and relevance for ablation of atrial fibrillation. Circulation. 2005;112(10):1400-1405.
  9. Tsao HM, Wu MH, Higa S, et al. Anatomic relationship of the esophagus and left atrium: implication for catheter ablation of atrial fibrillation. Chest. 2005;128(4):2581-2587.
  10. Martinek M, Meyer C, Hassanein S, et al. Identification of a high-risk population for esophageal injury during radiofrequency catheter ablation of atrial fibrillation: procedural and anatomical considerations. Heart Rhythm. 2010;7(9):1224-1230.
  11. Fukaya H, Niwano S, Ogiso S, et al. Steerable esophageal thermometer for atrial fibrillation in a patient with esophageal achalasia: a case report. Clin Case Rep. 2018;6(5):839-842.
  12. Yamasaki H, Tada H, Sekiguchi Y, et al. Prevalence and characteristics of asymptomatic excessive transmural injury after radiofrequency catheter ablation of atrial fibrillation. Heart Rhythm. 2011;8:826-832.
  13. Ito M, Yamabe H, Koyama J, et al. Analysis for the primary predictive factor for the incidence of esophageal injury after ablation of atrial fibrillation. J Cardiol. 2018;72:480-487.
  14. Sarairah SY, Woodbury B, Methachittiphan N, Tregoning DM, Sridhar AR, Akoum N. Esophageal thermal injury following cryoballoon ablation for atrial fibrillation. JACC Clin Electrophysiol. 2020;6:262-268.
  15. Stauber A, Kornej J, Bollman A, Hindricks G, Sommer P. Relevance of esophageal position and temperature on thermal injuries and rhythm outcome in atrial fibrillation ablations. Pacing Clin Electrophysiol. 2020;43:194-200.
  16. Di Biase L, Saenz LC, Burkhardt DJ, et al. Esophageal capsule endoscopy after radiofrequency catheter ablation of atrial fibrillation: documented higher risk of luminal esophageal damage with general anesthesia as compared with conscious sedation. Circ Arrhythm Electrophysiol. 2009;2:108-112.
  17. John RM, Kapur S, Ellenbogen KA, Koneru JN. Atrioesophageal fistula formation with cryoballoon ablation is most commonly related to the left inferior pulmonary vein. Heart Rhythm. 2017;14:184-189.
  18. Miyazaki S, Nakamura H, Taniguchi H, et al. Gastric hypomotility after second-generation cryoballoon ablation — unrecognized silent nerve injury after cryoballoon ablation. Heart Rhythm. 2017;14:670-677.
  19. Yarlagadda B, Deneke T, Turagam M, et al. Temporal relationship between esophageal injury type and progression in patients undergoing atrial fibrillation catheter ablation. Heart Rhythm. 2019;16:204-212.
  20. Barbhaiya CR, Kumar S, Guo T, et al. Global survey of esophageal injury in atrial fibrillation ablation: characteristics and outcomes of esophageal perforation and fistula. JACC Clin Electrophysiol. 2016;2(2):143-150.
  21. Zhang P, Zhang Y, Ye Q, et al. Characteristics of atrial fibrillation patients suffering esophageal injury caused by ablation for atrial fibrillation. Sci Rep. 2020;10(1):2751.
  22. Singh R, Landa EJ, Machado C. Atrial-esophageal fistula after catheter ablation: diagnosing and managing a rare complication of a common procedure. Am J Case Rep. 2019;20:557-561.
  23. Badertscher P, Delko T, Oertli D, et al. Surgical repair of an esophageal perforation after radiofrequency catheter ablation for atrial fibrillation. Indian Pacing Electrophysiol J. 2019;19(3):110-113.
  24. Yousuf T, Keshmiri H, Buliva Z, et al. Management of atrial-esophageal fistula following left atrial ablation. Cardiol Res. 2016;7(1):36-45.
  25. Barbhaiya C, Kogan E, Jankelson L, et al. Esophageal temperature dynamics during high-power short-duration posterior wall ablation. Heart Rhythm. 2020;17(5 Pt A):721-727.
  26. Ghia KK, Chugh A, Good E, et al. A nationwide survey on the prevalence of atrioesophageal fistula after left atrial radiofrequency catheter ablation. J Interv Card Electrophysiol. 2009;24(1):33-36.
  27. Kumar S, Romero J, Stevenson WG, et al. Impact of lowering irrigation flow rate on atrial lesion formation in thin atrial tissue: preliminary observations from experimental and clinical studies. JACC Clin Electrophysiol. 2017;3(10):1114-1125.
  28. Borne RT, Sauer WH, Zipse MM, Zheng L, Tzou W, Nguyen DT. Longer duration versus increasing power during radiofrequency ablation yields different ablation lesion characteristics. JACC Clin Electrophysiol. 2018;4:902-908.
  29. Das M, Loveday JJ, Wynn GJ, et al. Ablation index, a novel marker of ablation lesion quality: prediction of pulmonary vein reconnection at repeat electrophysiology study and regional differences in target values. Europace. 2017;19:775-783.
  30. Taghji P, El Haddad M, Phlips T, et al. Evaluation of a strategy aiming to enclose the pulmonary veins with contiguous and optimized radiofrequency lesions in paroxysmal atrial fibrillation: a pilot study. JACC Clin Electrophysiol. 2018;4:99-108. 
  31. Chelu MG, Morris AK, Kholmovski EG, et al. Durable lesion formation while avoiding esophageal injury during ablation of atrial fibrillation: lessons learned from late gadolinium MR imaging. J Cardiovasc Electrophysiol. 2018;29:385-392.
  32. Williams AA, Al-Zubaidi M, Su W, et al. Abstract 16411: incidence of atrial-esophageal fistula in cryoballoon ablation for atrial fibrillation is dose dependent. Circulation. 2016;134:A16411.
  33. Bhaskaran A, Chik W, Pouliopoulos J, et al. Five seconds of 50-60 W radiofrequency atrial ablations were transmural and safe: an in vitro mechanistic assessment and force-controlled in vivo validation. Europace. 2017;19:874-880.
  34. Wolf M, El Haddad M, DeWilde V, et al. Endoscopic evaluation of the esophagus after catheter ablation of atrial fibrillation using contiguous and optimized radiofrequency applications. Heart Rhythm. 2019;16(7):1013-1020.
  35. Baher A, Kheirkhahon M, Rechenmacher SJ, et al. High-power radiofrequency catheter ablation of atrial fibrillation: using late gadolinium enhancement magnetic resonance imaging as a novel index of esophageal injury. JACC Clin Electrophysiol. 2018;4(12):1583-1594.
  36. Montoya MM, Mickelsen S, Clark B, et al. Protecting the esophagus from thermal injury during radiofrequency ablation with an esophageal cooling device. J Atr Fibrillation. 2019;11(5):2110. 
  37. Knight B. Grilling a burger in the winter. EP Lab Digest. 2020;20(6):6.
  38. Gallagher M, Leung L, Bajpal A, et al. Improving esophageal protection during AF ablation with ablation index technology: outcomes from the IMPACT study. Late-breaking clinical trials: all about AFib. Heart Rhythm. 2020;17(7):1208.
  39. Leung LW, Gallagher MW, Santangeli P, et al. Esophageal cooling for protection during left atrial ablation: a systematic review and meta-analysis. J Interv Card Electrophysiol. 2019 Nov 22. Online ahead of print.
  40. Deneke T, Nentwich K, Berkovitz H, et al. High-resolution infrared thermal imaging of the esophagus during atrial fibrillation ablation as a predictor of endoscopically detected thermal lesions: results from the HEAT-AF study. Circ Arrhythm Electrophysiol. 2018;11(11):e006681. 
  41. Daly MG, Melton I, Roper G, Lim G, Crozier IG. High-resolution infrared thermography of esophageal temperature during radiofrequency ablation of atrial fibrillation. Circ Arrhythm Electrophysiol. 2018;11(2):e005667. 
  42. Koruth JS, Reddy VY, Miller MA, et al. Mechanical esophageal displacement during catheter ablation for atrial fibrillation. J Cardiovasc Electrophysiol. 2012:23(2):147-154.
  43. Palaniswamy C, Koruth J, Mittnacht A, et al. The extent of mechanical esophageal deviation to avoid esophageal heating during catheter ablation of atrial fibrillation. JACC Clin Electrophysiol. 2017;3(10):1146-1154.
  44. Bhardwaj R, Naniwadekar A, Whang W, et al. Esophageal deviation during atrial fibrillation ablation: clinical experience with a dedicated esophageal balloon retractor. JACC Clin Electrophysiol. 2018;4(8):1020-1030.
  45. Parikh V, Swarup V, Hantla J, et al. Feasibility, safety, and efficacy of a novel preshaped nitinol esophageal deviator to successfully deflect the esophagus and ablate left atrium without esophageal temperature rise during atrial fibrillation ablation: the DEFLECT GUT study. Heart Rhythm. 2018;15:1321-1327.
  46. Assis FR, Shah R, Narasimhan B, et al. Esophageal injury associated with catheter ablation for atrial fibrillation: determinants of risk and protective strategies. J Cardiovasc Electrophysiol. 2020;31(6):1364-1376.
  47. Müller P, Dietrich JW, Halbfass P, et al. Higher incidence of esophageal lesions after ablation of atrial fibrillation related to the use of esophageal temperature probes. Heart Rhythm. 2015;12(7):1464-1469.
  48. Perez J, D’Avila A, Aryana A, Berjano E. Electrical and thermal effects of esophageal temperature probes on radiofrequency catheter ablation of atrial fibrillation: results from a computational modeling study. J Cardiovasc Electrophysiol. 2015;26(5):556-564.
  49. Turagam MK, Miller S, Sharma SP, et al. Differences in transient thermal response of commercial esophageal temperature probes: insights from an experimental study. JACC Clin Electrophysiol. 2019;5(11):1280-1288.
  50. Deiss S, Metzner A, Ouyang F, et al. Incidence of significant delayed esophageal temperature drop after cryoballoon-based pulmonary vein isolation. J Cardiovasc Electrophysiol. 2016;27(8):913-917.
  51. Metzner A, Burchard A, Wohlmuth P, et al. Increased incidence of esophageal thermal lesions using the second-generation 28-mm cryoballoon. Circ Arrhythm Electrophysiol. 2013;6(4):769-775.
  52. Fürnkranz A, Bordignon S, Schmidt B, et al. Luminal esophageal temperature predicts esophageal lesions after second-generation cryoablation pulmonary vein isolation. Heart Rhythm. 2013;10(6):789-793.
  53. Fürnkranz A, Bordignon S, Böhmig M, et al. Reduced incidence of esophageal lesions by luminal esophageal temperature-guided second-generation cryoballoon ablation. Heart Rhythm. 2015;12(2):268-274.
  54. Weber H, Schaur P, Sagerer-Gerhardt M. Use of light sensor and focused local atrial electrogram recordings for the monitoring of thermal injury to the esophagus and lungs during laser catheter ablation of the posterior atrial walls: preclinical in vitro porcine and in vito canine experimental studies. J Innov Card Rhythm Manag. 2019;10(7):3723-3731.
  55. Lee JM, Shim J, Park J, et al. The electrical isolation of the left atrial posterior wall in catheter ablation of persistent atrial fibrillation. JACC Clin Electrophysiol. 2019;5:1253-1261.
  56. Ivey J, Latouche EL, Richards ML, et al. Enhancing irreversible electroporation by manipulating cellular biophysics with a molecular adjuvant. Biophys J. 2017;113(2):472-480.
  57. Koruth J, Kuroki K, Kawamura I, et al. Pulsed field ablation versus radiofrequency ablation: esophageal injury in a novel porcine model. Circ Arrhythm Electrophysiol. 2020;13(3):e008303.
  58. Koruth J, Kuroki K, Iwasawa J, et al. Preclinical evaluation of pulsed field ablation: electrophysiological and histological assessment of thoracic vein isolation. Circ Arrhythm Electrophysiol. 2019;12(12):e007781. 
  59. Reddy VY, Neuzil P, Koruth JS, et al. Pulsed field ablation for pulmonary vein isolation in atrial fibrillation. J Am Coll Cardiol. 2019;74(3):315-326.
  60. Zei P, Soltys S. Ablative radiotherapy as a noninvasive alternative to catheter ablation for cardiac arrhythmias. Curr Cardiol Rep. 2017;19(9):79.
  61. Zei P, Wong D, Gardner E, Fogarty T, Maguire P. Safety and efficacy of stereotactic radio ablation targeting pulmonary vein tissues in an experimental model. Heart Rhythm. 2018;15(9):1420-1427.
  62. Kim E, Davogustto G, Stevenson WG, John RM. Non-invasive cardiac radiation for ablation of ventricular tachycardia: a new therapeutic paradigm in electrophysiology. Arrhythm Electrophysiol Rev. 2018;7(1):8-10.
  63. Robinson C, Samson PP, Moore KMS, et al. Phase I/II trial of electrophysiology-guided noninvasive cardiac radioablation for ventricular tachycardia. Circulation. 2019;139(3):313-321.
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