Summary Barrett's esophagus with high-grade dysplasia (BEHGD) and intramucosal esophageal adenocarcinoma (IMC) can be treated by radiofrequency ablation (RFA) and endoscopic mucosal resection (EMR). Efficacy of RFA and EMR in academic medical centers has been demonstrated in previous studies. However, the clinical effectiveness of this approach in community clinical practice is not fully established. All patients with biopsy-proven BEHGD and IMC (T1a), who were treated endoscopically between 2007 and 2014, were prospectively enrolled. Treatment algorithms were determined by consensus opinion after presentation at gastrointestinal tumor board. Patients underwent EMR and/or RFA until eradication-of-dysplasia and complete remission of intestinal metaplasia (CRIM) was achieved. Patients were then enrolled in an endoscopic surveillance program. A total of 60 patients underwent endoscopic therapy for BEHGD (32) or IMC (28). Median length BE was 4 cm. Forty-six patients had EMR. Median treatment interval was nine months. Median follow-up was 33 months (Interquartile range: 16–50). Fifty-five (92%) patients achieved eradication-of-dysplasia and 52(87%) CRIM. One patient with BEHGD did not achieve any benefit six months into treatment. Nine (15%) patients relapsed after CRIM with nondysplastic-BE (6), BE with low-grade dysplasia (1), and BEHGD (2). After retreatment, eradication-of-intestinal metaplasia was achieved in five patients. BE length was a negative predictor for achieving CRIM (OR 0.81; P = 0.04). There were no procedure-related severe complications. Eleven patients with prior EMR developed symptomatic strictures, which were all successfully dilated. Endoscopic management of BEHGD and IMC can be safely and effectively performed in a community clinical practice similarly to high-volume academic medical centers when performed by advanced endoscopists following multidisciplinary approach. ABBREVIATIONS ABBREVIATIONS BE: Barrett's esophagus BEHGD: Barrett's esophagus with high-grade dysplasia CRIM: complete remission of intestinal metaplasia EMR: endoscopic mucosal resection IMC: intramucosal esophageal adenocarcinoma IQR: interquartile range RFA: radiofrequency ablation SJMHS: St. Joseph Mercy Health System, Ann Arbor, MI INTRODUCTION Dysplastic Barrett's esophagus is a precursor for developing esophageal adenocarcinoma.1 The incidence of this cancer has been rising with early diagnosis approaches.2 Endoscopic therapy has become the standard treatment for patients with Barrett's esophagus with high-grade dysplasia (BEHGD) and/or intramucosal esophageal adenocarcinoma (IMC) (T1N0, AJCC 7th ed.3).4,5 Endoscopic mucosal resection (EMR) for BEHGD or IMC, followed by radiofrequency ablation (RFA) for residual BE metaplasia or dysplasia, has been shown to be a safe and effective treatment modality in multiple studies when performed in high-volume academic medical centers.6–8 In the United States, the vast majority of gastroenterologists practice in the community and are increasingly treating dysplastic BE.9 The clinical effectiveness of treatment of BEHGD and IMC in the community has not been well studied. We sought to assess whether endoscopists practicing in a community clinical practice could treat BEHGD and IMC with high level of clinical success similar to high-volume academic medical centers. PATIENTS AND METHODS Design and practice setting The study was conducted at St. Joseph Mercy Health System (SJMHS) community medical center and Huron Gastroenterology, a private twenty-provider community practice with no academic affiliation, in Ann Arbor, Michigan, USA. All consecutive patients who were endoscopically treated between August 2007 and August 2014 (study endpoint) were prospectively enrolled in a database. All procedures were performed on an outpatient basis by three gastroenterologists. Each had completed an advanced-endoscopy fellowship that included dedicated training in the endoscopic management of dysplastic-BE, and have performed a minimum of 50 EMRs and 50 RFAs. Eligible patients had biopsy-proven dysplastic-BE confirmed by two board-certified gastrointestinal pathologists. All cancer cases were presented at a multidisciplinary gastrointestinal oncology tumor board that included gastroenterologists, oncologists, thoracic surgeons, and pathologists. Treatment recommendations were determined by consensus opinion. The institutional review board at SJMHS approved the study protocol. Inclusion and exclusion criteria Only patients with biopsy-proven BEHGD or IMC (stage T1aN0)3 were included. Imaging including endoscopic ultrasound, CT scan, and PET scan were taken into account when available. Patients with IMC beyond stage T1aN0, histology with lymphovascular invasion, poorly differentiated cancer, or with prior esophagectomy were excluded. Procedures and follow-up protocol Patients underwent a high-definition white light and narrow-band imaging exam. BE-segment length measurement also included Prague classification after 2011, but this was not used in prior years.10 EMR was performed for any visible abnormalities such as nodularity (Fig. 1). This was followed by RFA (using the BARRX system, Medtronic Sunnyvale, CA)11 to ablate any residual dysplastic-BE found during subsequent endoscopy sessions. EMR and/or RFA were performed every 2–3 months until eradication-of-dysplasia and complete remission of intestinal metaplasia (CRIM). This EMR and RFA stepwise approach for treatment of BEHGD and IMC has been detailed in prior studies.7,12,13 Follow-up biopsies were obtained per the Seattle protocol.14 Once the therapeutic end point was achieved, patients were enrolled in surveillance program that involved serial endoscopies every 6–12 months as determined by the performing endoscopist. Patients who did not follow-up and could not be reached were deemed lost-to-follow-up. Each patient was typically started on high-dose proton pump inhibitor twice daily. Fig. 1 View largeDownload slide Therapy protocol patient flow chart. Bx, biopsy; m, month; Pos, positive; Neg, negative. Fig. 1 View largeDownload slide Therapy protocol patient flow chart. Bx, biopsy; m, month; Pos, positive; Neg, negative. Outcome measures Primary outcome measure for this study was eradication-of-dysplasia and CRIM.7 Secondary outcomes were relapse of intestinal metaplasia with and without dysplasia after CRIM and procedure-related complications. Statistical analysis Data were analyzed using the SPSS statistical software package (Chicago, IL). Mean (±SD) was used for continuous variables with normal distribution and median (Interquartile range (IQR): 25%–75%) was used for variables with skewed distributions. We conducted logistic regression analysis to detect predictors of CRIM. P value less than 0.05 was considered a level for relative significance. RESULTS Endoscopic therapy Endoscopic therapy was provided to 60 patients (48 men), mean age of 67 (±10) years with BEHGD (n = 32) or IMC (n = 28) (Table 1). Median BE-segment length was 4 cm (IQR: 2–7). Patients underwent a median of one EMR (IQR: 1–2) and three RFA (IQR: 2–5) procedures. Forty-six (77%) patients underwent primary EMR for raised/nodular dysplasia (Fig. 2) followed by RFA. Eight patients required escape-EMR for nodular relapse after RFA therapy. Median endoscopic treatment interval was nine months (IQR: 4–20). Fig. 2 View largeDownload slide (A) A patient with first diagnosis of BE with IMC (early-esophageal adencocarcinoma or eEAC). (B) Post-EMR. (C) EMR specimen—BEHGD (in rectangle) and IMC (in oval). (D) Post-EMR and RFA at 4-year follow-up. No endoscopic evidence of residual BE. Biopsy specimen is showing CRIM. Fig. 2 View largeDownload slide (A) A patient with first diagnosis of BE with IMC (early-esophageal adencocarcinoma or eEAC). (B) Post-EMR. (C) EMR specimen—BEHGD (in rectangle) and IMC (in oval). (D) Post-EMR and RFA at 4-year follow-up. No endoscopic evidence of residual BE. Biopsy specimen is showing CRIM. Table 1 Demographic characteristics Mean age (±SD), y 67 (10) Men (%) 48 (80) Race/ethnicity (%) Caucasian 54 (90) Hispanic 1 (2) Unknown 5 (8) Primary dysplasia (%) BEHGD 32 (53) IMC 28 (47) Median BE (IQR), cm 4 (2–7) Mean age (±SD), y 67 (10) Men (%) 48 (80) Race/ethnicity (%) Caucasian 54 (90) Hispanic 1 (2) Unknown 5 (8) Primary dysplasia (%) BEHGD 32 (53) IMC 28 (47) Median BE (IQR), cm 4 (2–7) BEHGD, Barrett's esophagus with high-grade dysplasia; IMC, intramucosal adenocarcinoma; IQR, interquartile range; SD, standard deviation of the mean; y, years. View Large Follow-up surveillance Median follow-up duration was 33 months (IQR: 16–50) (Table 2). Overall, fifty-two (87%) patients were able to achieve CRIM and 55 (92%) patients eradication-of-dysplasia. Dysplasia was down-staged in four (7%) patients. One patient failed to regress BEHGD 6 months into therapy after one EMR and three RFA procedures and was planned for further endoscopic therapy (Fig. 1) by the study endpoint. Forty-three (72%) patients maintained CRIM with follow up of median 16 months (IQR: 5–32) (Table 2) and 43% of patients had follow up >12 months (30% with >24 months). Nine (15%) patients relapsed after achieving CRIM (at median 19 months into follow-up, IQR: 11–35). Six patients relapsed with nondysplastic BE, one with BE with low-grade dysplasia, and two BEHGD. None of the patients relapsed with adenocarcinoma. After retreatment, eradication of intestinal metaplasia was again achieved in five patients (Table 2) and nondysplastic BE was maintained in three (one of which was lost-to-follow-up after 30 months). One patient relapsed with BEHGD after long-term remission of intestinal metaplasia for 43 months. He underwent two additional RFA sessions but was subsequently lost-to-follow-up after total of 54 months. Overall, three patients were lost-to-follow-up. Table 2 Outcomes of endoscopic therapy and follow-up duration Final Outcomes by the end of follow-up (%) CRIM 48 (80) Eradication of dysplasia 55 (92) Overall down-staged dysplasia 59 (98) Final biopsy results (%) 48 (80) No intestinal metaplasia 7 (12) NDBE 1 (2) BELGD 4 (7) Median duration of maintained CRIM without relapse (IQR), m 16 (6–32) Median duration of endoscopic treatment interval (IQR), m 9 (4–20) Median overall follow-up duration (IQR), m 33 (16–50) Final Outcomes by the end of follow-up (%) CRIM 48 (80) Eradication of dysplasia 55 (92) Overall down-staged dysplasia 59 (98) Final biopsy results (%) 48 (80) No intestinal metaplasia 7 (12) NDBE 1 (2) BELGD 4 (7) Median duration of maintained CRIM without relapse (IQR), m 16 (6–32) Median duration of endoscopic treatment interval (IQR), m 9 (4–20) Median overall follow-up duration (IQR), m 33 (16–50) BELGD, Barrett's esophagus with low-grade dysplasia; CRIM, complete remission of intestinal metaplasia; m, months; NDBE, nondysplastic Barrett's esophagus. View Large Predictors of success of endoscopic therapy Multivariable analysis demonstrated that BE-segment length was the only significant independent negative predictor of CRIM (Table 3). Patients with long-segment BE were less likely to achieve CRIM (OR 0.81, 95% CI 0.66–0.99, P = 0.04). However, original BE-segment length did not predict relapse after CRIM (OR 0.95, 95% CI 0.78–1.15, P = 0.6). Age, gender, original diagnosis of BEHGD versus IMC, and number of endoscopic treatments, did not independently predict relapse after CRIM. Table 3 Univariable and multivariable logistic regression analysis of predictors of CRIM Variable, No. (%) Univariable analysis Multivariable analysis OR (95% CI) P value OR (95% CI) P value Male vs. Female 0.95 (0.17–5.19) 0.95 0.53 (0.078–3.57) 0.51 Age 0.99 (0.93–1.06) 0.85 1.02 (0.94–1.10) 0.64 Original IMC vs. BEHGD 0.85 (0.22–3.31) 0.81 0.62 (0.12–3.26) 0.57 Total number of EMR and RFAs 0.78 (0.65–0.95) 0.01 1.10 (0.86–1.40) 0.46 Number of RFAs 0.69 (0.53–0.90) <0.01 Number of EMRs 0.89 (0.63–1.26) 0.51 BE-length, cm 0.85 (0.73–1.00) 0.04 0.81 (0.66–0.99) 0.04 Overall follow-up duration 0.98 (0.95–1.02) 0.36 1.00 (0.95–1.04) 0.85 Logistic regression interaction model analysis BE-length and age 1.00 (0.98–1.01) 0.80 BE-length and original dysplasia 0.73 (0.46–1.17) 0.19 BE-length and No. of EMR and RFAs 1.01 (0.96–1.06) 0.78 BE-length and follow-up duration 1.01 (0.99–1.02) 0.31 Variable, No. (%) Univariable analysis Multivariable analysis OR (95% CI) P value OR (95% CI) P value Male vs. Female 0.95 (0.17–5.19) 0.95 0.53 (0.078–3.57) 0.51 Age 0.99 (0.93–1.06) 0.85 1.02 (0.94–1.10) 0.64 Original IMC vs. BEHGD 0.85 (0.22–3.31) 0.81 0.62 (0.12–3.26) 0.57 Total number of EMR and RFAs 0.78 (0.65–0.95) 0.01 1.10 (0.86–1.40) 0.46 Number of RFAs 0.69 (0.53–0.90) <0.01 Number of EMRs 0.89 (0.63–1.26) 0.51 BE-length, cm 0.85 (0.73–1.00) 0.04 0.81 (0.66–0.99) 0.04 Overall follow-up duration 0.98 (0.95–1.02) 0.36 1.00 (0.95–1.04) 0.85 Logistic regression interaction model analysis BE-length and age 1.00 (0.98–1.01) 0.80 BE-length and original dysplasia 0.73 (0.46–1.17) 0.19 BE-length and No. of EMR and RFAs 1.01 (0.96–1.06) 0.78 BE-length and follow-up duration 1.01 (0.99–1.02) 0.31 View Large Complications of endoscopic therapy There were no procedure-related esophageal perforations, severe or delayed hemorrhage, or complications requiring hospitalization. Symptomatic therapy-related esophageal strictures occurred in 11 (18%) patients, all with prior EMR, and were all successfully dilated. Number of RFA or EMR procedures did not predict the development of symptomatic strictures (OR 1.18 and 1.17, P = 0.16 and 0.36, respectively). Immediate post-EMR bleeding requiring endoclips and/or local epinephrine injection occurred in two patients. There was no procedure-related mortality. DISCUSSION This is one of the few prospective studies that assess clinical effectiveness of endoscopic treatment for BEHGD and IMC in a community clinical practice in the United States, performed by advanced endoscopists following multidisciplinary approach. With a median follow-up duration of 2.8 years, eradication-of-dysplasia was achieved in 92% of the patients and CRIM in 87% with EMR and RFA therapy. In patients who maintained CRIM, median follow up was 1.3 years in 72% of the cohort (>1 year in 43% and >2 years in 30%). During surveillance there were nine relapses, two with advanced dysplasia, but none with adenocarcinoma. All were managed with RFA and/or escape-EMR, again achieving eradication of intestinal metaplasia in five patients and three maintained eradication-of-dysplasia. These outcomes were achieved without any major procedure-related morbidity or death. Consistent with the growing body of literature demonstrating the efficacy, long-term durability, and safety of endoscopic therapy for BEHGD and IMC in academic medical centers, this study likewise suggests that clinical effectiveness can also be achieved in the community clinical practice. The rates of eradication-of-dysplasia and CRIM in this study are close to the results reported in the UK RFA Registry and Netherlands cohort study.6,15 They are as high as the EURO-II multicenter study rates of 92% and 87%, respectively (median follow-up duration of almost 4 years).7 The UK and EURO-II studies reported an IMC relapse rate of up to 4–5% after a median of 2.3 years after therapy.7,15 While we did not have IMC relapse in our cohort of patients, we emphasize that compulsive surveillance after treatment is still imperative to decreasing the risk of recurrence.16 One of our patients relapsed with BEHGD after long-term remission of intestinal metaplasia for 43 months, therefore we would advise at least yearly surveillance for those with a history of BEHGD or IMC. In parallel with the UK RFA Registry report,15 our findings show that the maximum BE-segment length was the only significant independent predictor of achieving CRIM (OR 0.81, P = 0.04). The longer the BE-segment, the lower the rate of CRIM. The rate of relapse after CRIM however was not influenced by the length of BE segment. Original grade of Barrett's dysplasia, IMC versus BEHGD, also did not appear to predict CRIM. The rates of symptomatic strictures (18%) necessitating therapy and minor bleeding necessitating endoclips and/or epinephrine injections (3%) were higher compared to the UK RFA Registry and the Amsterdam group study (9–12% and 1%, respectively).15,17 None of our patients, however, required postprocedure inpatient admission while nearly 2% of the patients were admitted after the procedure in one large academic medical center study.18 None of the patients in our study required blood transfusions. Only gastroenterologists with advanced-endoscopy fellowship training (n = 3), performed RFA and EMR procedures. All patients had high-definition endoscopy with narrow-band imaging, and biopsies were obtained following a standard methodology. All biopsies were evaluated by two expert fellowship-trained gastrointestinal pathologists. All cancer cases were presented in a multidisciplinary gastrointestinal oncology tumor board prior to initiating treatment. Oncologists, thoracic surgeons, pathologists, as well as gastroenterologists discussed the cases and treatment algorithms were determined based on consensus opinion. The limitations of this study are the relatively lower volume of patients when compared to tertiary academic centers, and that patients did not have consistent protocol-based follow-up durations and biopsies. Therefore, the rates of CRIM and relapse may be underestimated. Our follow-up duration (median of 2.8 years) was slightly shorter than other high-volume academic center trials, for example the EURO-II (median of almost 4 years),7 which may have had an impact on rates of CRIM maintenance and relapse. We suspect that on further follow up our rates would probably not have significantly changed. Based on our experience, as described in this study, we would recommend a multidisciplinary approach to achieve outcomes comparable to high-volume academic medical centers. This multidisciplinary team approach includes fellowship-trained therapeutic endoscopists with expertise in performing EMR and RFA for management of these cases, gastrointestinal pathologists, thoracic surgeons, and oncologists. Such an approach ensures appropriate patient selection for endoscopic treatment, and referral of more advanced cases for alternative treatment pathways. CONCLUSION This study demonstrates that gastroenterologists in a community clinical practice with advanced-training and expertise in managing advanced-esophageal dysplasia, who work collaboratively with a multidisciplinary gastrointestinal oncology tumor board, can achieve rates of CRIM in patients with BEHGD and IMC comparable to high-volume academic medical centers. Notes Specific author contributions: Study concept: Riad H. Al Natour; Acquisition of data: Riad H. Al Natour; Analysis and interpretation of data: Riad H. Al Natour, Eugene Zolotarevsky; Statistical analysis: Riad H. Al Natour; Drafting and finalizing the manuscript: Riad H. Al Natour; Endoscopic procedures: Andrew Catanzaro, Eugene Zolotarevsky, Naresh T. Gunaratnam; Intellectual manuscript revision: Andrew Catanzaro, Eugene Zolotarevsky, Anthony T. DeBenedet; Study concept and design: Naresh T. Gunaratnam; Interpretation of data: Naresh T. Gunaratnam; Critical and intellectual manuscript revision: Naresh T. Gunaratnam; Overall study supervision: Naresh T. Gunaratnam. SUPPLEMENTARY DATA Supplementary data are available at DOTESO online. Additional Supporting Information may be found in the online version of this article at the publisher's website. Supplement Figure Patient's follow up and outcomes. 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Diseases of the Esophagus – Oxford University Press
Published: Jan 1, 2018
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