Pilot series of radiofrequency ablation of Barrett’s esophagus with or without neoplasia

• Introduction
• Patients and methods
• Results
• Discussion
• Acknowledgment
• References

Background and study aims: Radiofrequency ablation is a rapidly evolving therapeutic modality for Barrett’s esophagus. The aim of this ongoing 12-month trial is to assess Barrett’s esophagus eradication after radiofrequency ablation using a balloon-based (HALO-360) and a plate-based (HALO-90) device. We report here our experience with the first 10 patients (out of 40) who have completed 12 months of follow-up.

Patients and methods: Following radiofrequency ablation using the HALO-360 device all patients were maintained on double-dose proton pump inhibitor therapy. Endoscopic evaluation was performed at 3 and 12 months postablation. Patients with residual Barrett’s esophagus at 3 months underwent repeat ablation. Ten patients, seven with nondysplastic Barrett’s esophagus, two with low-grade and one with high-grade dysplasia have completed the study to date.

Results: Complete Barrett’s esophagus eradication was achieved in seven patients, and partial eradication was achieved in three. There were no major complications. One case of buried Barrett’s metaplasia was encountered and successfully re-ablated, with complete Barrett’s esophagus eradication achieved at 12 months.

Conclusions: In this study, Barrett’s eradication rates were comparable to previously published reports. One case of buried Barrett’s metaplasia was identified out of 247 biopsies and was eradicated with repeat ablation.

Introduction

Barrett’s esophagus is encountered in 1.6 % of the general population and in approximately 7 % of patients with gastroesophageal reflux disease symptoms [1] [2]. Barrett’s esophagus is an important risk factor in the development of esophageal adenocarcinoma, now the predominant form of esophageal malignancy in the United States [3]. Esophageal adenocarcinoma carries a poor prognosis and continues to have a 5-year survival rate of less that 15 % [4]. The risk for development of esophageal adenocarcinoma in patients with Barrett’s esophagus is approximately 0.5 % per year. This risk is doubled in patients with Barrett’s and high-grade dysplasia (HGD) [5]. Optimal management of Barrett’s esophagus remains controversial. One rapidly evolving area of treatment is endoscopic ablative techniques. Multipolar electrocoagulation, argon plasma coagulation, photodynamic therapy, and laser ablation have been evaluated as treatment modalities for Barrett’s esophagus and have produced mixed results [6]. Limitations include high rates of complications (perforation and stricture formation), recurrence of Barrett’s disease, difficulty of use, and high costs. Development of postablation buried Barrett’s metaplasia is another potentially serious complication of endoscopic ablative techniques [7] [8] [9] [10]. Buried Barrett’s metaplasia is defined as specialized intestinal epithelium found postablation underneath otherwise normally appearing squamous epithelium [10] [11].

The HALO system (BÂRRX Medical Corp, Sunnyvale, California, USA) is a novel radiofrequency-based ablation device for Barrett’s eradication. Energy delivery is automated and rapid at a predefined depth using balloon-based (HALO-360) and plate-based (HALO-90) devices. The main advantage of this approach is a uniform and circumferential ablation at a defined depth [12] [13] [14]. This study is an ongoing 12-month trial that aims to assess BE eradication following ablation with the HALO system. We report our initial experience with 10 patients who completed a 12-month follow-up.

Patients and methods

From December 2005 to January 2008, all patients at our institution with biopsy-proven Barrett’s esophagus were evaluated for inclusion in the study. Inclusion criteria were histologic diagnosis of Barrett’s esophagus with endoscopic length > 1 cm, age 18 - 85 years, and the ability to provide informed consent. Both short- and long-segment Barrett’s lengths were evaluated. Patients with nondysplastic Barrett’s esophagus and Barrett’s with low-grade dysplasia (LGD) or HGD were included. Exclusion criteria were esophageal strictures, active esophagitis, esophageal varices, esophageal malignancy, prior esophageal surgery, prior ablation or radiation therapy of esophagus, and any comorbid conditions or restrictions that would prevent endoscopy or patient compliance.

Initial endoscopic work up of the patients included visual evaluation and biopsy. Biopsy samples were obtained from four quadrants every 1 cm throughout the Barrett’s lesion using a maximum capacity forceps. All biopsies were reviewed by a senior pathologist with extensive experience in gastrointestinal pathology (SF). All patients with nondysplastic Barrett’s esophagus or Barrett’s with LGD who met inclusion criteria were considered for the study. Patients with Barrett’s esophagus and multifocal HGD were referred for surgical evaluation and thus excluded from the study. Patients with Barrett’s esophagus and HGD who were not surgical candidates were included into the study. All study patients with HGD were then evaluated with endoscopic ultrasound. Those with invasion beyond the mucosa or with regional lymph node involvement were referred to an oncology specialist and excluded from the study. Study patients with localized HGD underwent endoscopic mucosal resection (EMR) at least 1 month prior to radiofrequency ablation. Study patients with multifocal HGD proceeded to radiofrequency ablation without EMR.

Radiofrequency ablation was performed according to a previously described protocol [5]. The initial ablation was performed using the balloon-based radiofrequency electrode HALO-360. Patients with nondysplastic Barrett’s esophagus received two ablations at 10 J/cm², and patients with dysplasia received two ablations at 12 J/cm² during each treatment. Between ablations the balloon electrode was removed and cleaned. The mucosal debris was scrapped off with an Olympus EMR cap. This technique allowed for better visualization and improved contact of the electrode with the surface during the second ablation.

On follow-up ablations the plate-based HALO-90 was used to treat small islands of residual Barrett’s esophagus (< 2 cm). Two ablations at 12 J/cm² were performed during each session with debris and electrode cleaning between the two ablations. Balloon-based radiofrequency electrode was used as described above for large residual Barrett’s esophagus (> 2 cm). All the procedures were performed using a high-definition diagnostic upper endoscope with narrow-band imaging (NBI) capabilities (GIF H-180, Olympus Medical Corp., Tokyo, Japan). NBI was used during initial endoscopic evaluation at the discretion of the performing endoscopist.

Following initial ablation therapy, patients were followed up for 12 months. At 3 months and 12 months postablation, endoscopy with biopsies was performed. NBI was routinely used during all follow-up endoscopies to identify small areas of residual Barrett’s esophagus. Biopsies were taken at four quadrants every 1 cm, starting at 1 cm above the original Barrett’s lesion, included ablation zone with neosquamous epithelium, and ended at 1 cm below the original Barrett’s lesion. Biopsies suspicious for residual disease and/or buried Barrett’s metaplasia were reviewed by two independent gastrointestinal pathologists (SF, WW).

Patients with all biopsies negative for Barrett’s esophagus were deemed to have complete response. Partial response was defined as 50 % - 99 % biopsies negative for Barrett’s esophagus. Patients with residual Barrett’s esophagus (endoscopically visible or on biopsy) underwent repeat ablation as described above. Up to four repeat ablations were allowed with a 3-month healing period in between sessions.

All patients remained on twice-daily proton pump inhibitor therapy for the duration of the study. At the end of 12 months, patients with residual Barrett’s esophagus or Barrett’s with dysplasia were offered endoscopic surveillance or esophageal resection in accordance to the standard of practice.

Primary endpoints at the 12-months evaluation were complete response (all biopsies negative for Barrett’s esophagus), partial response (50 % - 99 % biopsies negative for Barrett’s esophagus), and no response (0 % to less than 50 % biopsies negative for Barrett’s esophagus). Secondary endpoints were complication rates and rates of buried Barrett’s metaplasia.

Results

Ten patients have completed the study with 12 month follow-up. Seven of those patients showed no evidence of residual disease (complete response). Three patients had partial response with only small islands of Barrett’s remaining. Mean Barrett’s length was 4.9 cm, (range, 1 - 11 cm), and mean age was 62 years. For patients with complete response, the average number of ablation sessions was 1.4; for patients with partial response, the average number of sessions was 2.7. In total, 247 postablation biopsies have been reviewed. An overview of the study design is shown in [Fig. 1].

There were no major complications (i. e. perforation or stricture formation). Mild throat and chest pain were the most frequent postablation complaints. These symptoms resolved in most patients by day 4 postablation. In our initial cohort, three patients had Barrett’s with dysplasia (two LGD and one HGD). To date, all three patients showed complete response at the 12-month follow-up. The patient with HGD received two EMRs followed by successful eradication of Barrett’s esophagus using both radiofrequency ablation devices ([Tables 1] and [2]). At the 12-month follow-up evaluation, the patient with HGD was found to have no endoscopic or microscopic evidence of Barrett’s esophagus or HGD.

We encountered one case of buried Barrett’s metaplasia, which was found in a 54-year-old male with an 8-cm nondysplastic circumferential Barrett’s segment with a distal border at the top of gastric folds (at 39 - 40 cm). No squamous islands were seen endoscopically or on biopsies of the distal esophagus containing the Barrett’s mucosa segment ([Fig. 2]). Ablation was delivered at 10 J/cm² in two successive doses to include the entire Barrett’s lesion. Follow-up evaluation at 3 months revealed normally appearing squamous epithelium and no endoscopic evidence of residual disease ([Fig. 3]). Biopsies taken at 39 cm from the incisors immediately above the top of the gastric folds revealed nondysplastic buried Barrett’s metaplasia ([Fig. 4 a, b]). The buried glands were encountered within the distal ablation zone. No other residual disease was seen in the 8-cm-long ablated Barrett’s segment. Per protocol, the patient underwent a second ablation with the HALO-360 device in the area where buried Barrett’s metaplasia was found. Repeat endoscopy at 12 months revealed no endoscopic evidence of residual disease ([Fig. 5]). Repeat biopsies (four quadrant every 1cm) taken from 40 - 30 cm from the incisors revealed no evidence of buried Barrett’s metaplasia ([Fig. 6]).

Discussion

There has been rapid progress in the development of endoscopic therapies for Barrett’s esophagus. Radiofrequency ablation (HALO system) is a novel ablative technique that has recently been gaining momentum. In our study, we evaluate a cohort of patients that included mostly nondysplastic Barrett’s esophagus. Long-term surveillance with proton pump inhibitor therapy is currently the standard of care for nondysplastic Barrett’s. However, prospective data on validity and cost-effectiveness of this approach is limited. Radiofrequency ablation could provide an alternative management strategy. Sharma et al. recently reported 70 % complete eradication rate of nondysplastic Barrett’s at 1 year after HALO ablation [5]. We report a similar rate of Barrett’s eradication in a broad-base community setting at 12-month follow-up. To date, 40 patients have completed initial HALO ablation: 35 nondysplastic Barrett’s, four LGD, and one HGD. To date, 28 patients have completed the 3-month follow-up. At 3 months, 12 (43 %) showed complete response, 14 (50 %) showed partial response, and two (7 %) showed no response. Longer follow-up is needed to confirm lasting Barrett’s eradication after radiofrequency ablation.

Development of postablation buried Barrett’s metaplasia is a particular concern with regard to endoscopic ablative therapies. The incidence of buried Barrett’s metaplasia following ablation with multipolar electrocoagulation, argon plasma coagulation, and photodynamic therapy ranges from 7.4 % to as high as 27.3 % [6] [7] [8] [15] [16] [17] [18] [19]. Etiology, natural history, and true incidence of buried Barrett’s metaplasia have not been well described. The progression of buried Barrett’s metaplasia to adenocarcinoma has been reported [9] [10] [20] [21] [22] [23]. The clinical dilemma posed by buried Barrett’s metaplasia is how to identify it underneath normally appearing neosquamous epithelium and how to prevent cancer development.

We report a case of buried Barrett’s metaplasia encountered after HALO-360 ablation during the 3-month follow-up. In our case, buried Barrett’s metaplasia was found on biopsies taken near the top of the gastric folds within the ablation zone. To our knowledge, buried Barrett’s metaplasia has not been described following HALO radiofrequency ablation. However, in a previously published report [5], biopsies were taken above the top of the gastric folds. We believe that biopsies at and near the top of the gastric folds should be performed following HALO ablation to increase the diagnostic yield. Furthermore, the transition zone between the ablated Barrett’s and adjacent gastric mucosa should be thoroughly treated to fully eradicate metaplasia including potential buried Barrett’s metaplasia. Although pre-ablation biopsies (taken from the area in which buried Barrett’s metaplasia was later found) showed Barrett’s without overlying squamous epithelium, we cannot definitively exclude the possibility of pre-existing buried Barrett’s metaplasia. During the endoscopic follow-up after HALO ablation, close endoscopic inspection is imperative to exclude the presence of small residual islands of Barrett’s esophagus. In case such small islands are overlooked and subsequently biopsied under the presumption that the biopsy was obtained from neosquamous mucosa, tangential cutting of the biopsy may result in the false diagnosis of buried glands. We thoroughly inspected the treatment zone before obtaining biopsies, but were not able to identify a residual Barrett’s island in this case. High-resolution and corresponding NBI images of the area where the biopsies were obtained should be considered mandatory for further studies.

Our data suggest that buried Barrett’s metaplasia after HALO ablation occurs at much lower rates compared with the other ablative techniques. We found one incidence of buried Barrett’s metaplasia out of 247 biopsies (0.4 %; [Table 2]). Such a low rate may be due to the circumferential and more uniform depth of ablation therapy delivered by the HALO device. Nonetheless, the possibility of buried Barrett’s metaplasia dictates thorough surveillance biopsies, in particular at the ablation borders. More importantly, our case illustrates that buried Barrett’s metaplasia can be successfully eradicated with repeated HALO ablation. In conclusion, our data on radiofrequency ablation for Barrett’s esophagus is comparable to the previously published report in achieving very low rates of complications and buried Barrett’s metaplasia.

Acknowledgment

The authors would like to thank Dr. Wilfred M. Weinstein for the histopathologic review.

Competing interests: None

References

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V. E. Eysselein, MD

Harbor-UCLA Medical Center

1000 West Carson Street

Torrance

CA 90509

USA

Fax: +1-310-212-7837

Email: veysselein@labiomed.org

References

• 1 Hirota W K, Loughney T M, Lazas D J. et al . Specialized intestinal metaplasia, dysplasia, and cancer of the esophagus and esophagogastric junction: prevalence and clinical data.  Gastroenterology. 1999;  116 277-285
  CrossrefPubMedSearch in Google Scholar
• 2 Rokainen J, Aro P, Storskrubb T. et al . Prevalence of Barrett’s esophagus in the general population: an endoscopic study.  Gastroenterology. 2005;  129 1825-1831
  CrossrefPubMedSearch in Google Scholar
• 3 Shaheen N J. Advances in Barrett’s esophagus and esophageal adenocarcinoma.  Gastroenterology. 2005;  128 1554-1556
  CrossrefPubMedSearch in Google Scholar
• 4 Sharma P, Faulk G W, Weston A P. et al . Dysplasia and cancer in a large multicenter cohort of patients with Barrett’s esophagus.  Clin Gastroenterol Hepatol. 2006;  4 566-572
  CrossrefPubMedSearch in Google Scholar
• 5 Sharma V K, Wang K, Overholt B. et al . Balloon-based, circumferential, endoscopic radiofrequency ablation of Barrett’s esophagus: 1-year follow-up of 100 patients.  Gastrointest Endosc. 2007;  65 185-195
  CrossrefPubMedSearch in Google Scholar
• 6 Barr H, Stone N, Rembacken B. Endoscopic Therapy for Barrett’s Oesophagus.  Gut. 2005;  54 875-884
  CrossrefPubMedSearch in Google Scholar
• 7 Basu K K, Pick B, Bale R. et al . Efficacy and one year follow up of argon plasma coagulation therapy for ablation of Barrett’s oesophagus: factors determining persistence and recurrence of Barrett’s epithelium.  Gut. 2002;  51 776-780
  CrossrefPubMedSearch in Google Scholar
• 8 Ban S, Mino M, Norman N. et al . Histopathologic aspects of photodynamic therapy for dysplasia and early adenocarcinoma arising in Barrett’s esophagus.  Am J Surg Path. 2004;  28 1466-1473
  CrossrefPubMedSearch in Google Scholar
• 9 Van Laethem J L, Peny M O, Salmon I. et al . Intramucosal adenocarcinoma arising under squamous re-epithelialisation of Barrett’s oesophagus.  Gut. 2000;  46 574-577
  CrossrefPubMedSearch in Google Scholar
• 10 Mino-Kenudso M, Ban S, Ohana M. et al . Buried dysplasia and early adenocarcinoma arising in Barrett esophagus after porfimer-polydynamic therapy.  Am J Surg Pathol. 2007;  3 403-409
  PubMedSearch in Google Scholar
• 11 Biddlestone L R, Barham C P, Wilkinson S P. et al . The histopathology of treated Barrett’s esophagus; squamous reepithelialization after acid suppression and laser photodynamic therapy.  Am J Surg Pathol. 1998;  22 239-245
  CrossrefPubMedSearch in Google Scholar
• 12 Ganz R A, Utley D S, Stern R. et al . Complete ablation of esophageal epithelium with a balloon-based bipolar electrode: a phased evaluation in the porcine and in human esophagus.  Gastrointest Endosc. 2004;  60 1002-1010
  CrossrefPubMedSearch in Google Scholar
• 13 Ganz R A, Batts K. Pilot human study of a balloon-based electrode for ablation of esophageal epithelium: results in subjects prior to planned esophagectomy.  Gastrointest Endosc. 2004;  59 AB252
  PubMedSearch in Google Scholar
• 14 Sharma V K, Overholt B, Wang K. et al . A randomized, multi-center evaluation of ablation of nondysplastic short segment Barrett esophagus using BÂRRX bipolar balloon device: extended follow-up of the Ablation of Intestinal Metaplasia (AIM-I) Trial.  Gastrointest Endosc. 2005;  61 T1391
  PubMedSearch in Google Scholar
• 15 Hornick J, Blount P, Sanchez C. et al . Biologic properties of columnar epithelium underneath reepithelialized squamous mucosa in Barrett’s esophagus.  Am J Surg Pathol. 2005;  29 372-380
  CrossrefPubMedSearch in Google Scholar
• 16 Sharma V K, McLaughlin R, Dean P. et al . Successful ablation of Barrett’s esophagus (BE) with low grade dysplasia (LGD) using BÂRRX bipolar balloon device: preliminary results of the Ablation of Intestinal Metaplasia with LGD (AIM-LGD) Trial.  Gastrointest Endosc. 2005;  61 S1205
  PubMedSearch in Google Scholar
• 17 Barewal H, Ramsey L, Sharma P. et al . Biomarker studies reversed in Barrett’s esophagus.  Am J Gastoenterol. 1999;  94 2829
  PubMedSearch in Google Scholar
• 18 Sampliner R E, Faigel D, Fennerty M B. et al . Effective and safe reversal of nondysplastic Barrett’s esophagus with thermal electrocoagulation combined with high-dose acid inhibition: a multicenter study.  Gastrointest Endosc. 2001;  53 554-558
  CrossrefPubMedSearch in Google Scholar
• 19 Hernandez J C, Tsai F, Reicher S. et al . Frequency of buried Barrett’s metaplasia after BÂRRX ablation for intestinal metaplasia with or without dysplasia.  Gastrointest Endosc. 2007;  65AB 111
  PubMedSearch in Google Scholar
• 20 Barr H. Barrett’s esophagus: treatment with 5-aminolevulinic acid photodynamic therapy.  Gastrointest Endosc Clin N Am. 2000;  10 421-438
  PubMedSearch in Google Scholar
• 21 Weston A, Sharma P, Banerjee S. et al . Visible endoscopic and histologic changes in the cardia, before and after complete Barrett’s esophagus ablation.  Gastrointest Endosc. 2005;  61 515-521
  CrossrefPubMedSearch in Google Scholar
• 22 Overholt B F, Panjehpour M, Haydek J M. Photodynamic therapy for Barrett’s esophagus; follow up in 100 patients.  Gastrointest Endosc. 1999;  49 1-7
  CrossrefPubMedSearch in Google Scholar
• 23 Shand A, Dallal H, Palmer K. et al . Adenocarcinoma arising in columnar lined oesophagus following treatment with argon plasma coagulation.  Gut. 2001;  48 580-581
  CrossrefPubMedSearch in Google Scholar

V. E. Eysselein, MD

Harbor-UCLA Medical Center

1000 West Carson Street

Torrance

CA 90509

USA

Fax: +1-310-212-7837

Email: veysselein@labiomed.org