Endoscopic resection and ablation of neoplastic lesions of the esophagus: clinical application and techniques

Introduction

Esophageal cancer is the eighth most common cause of cancer and sixth most common cause of cancer-related mortality in the world, with only 10–30% 5-year survival rate (1). Esophageal cancer can be divided into two histological subtypes: Esophageal adenocarcinoma (EAC) and squamous cell carcinoma (SCC), with different risk factors associated with each subtype (2). The age-standardized incidence rate per 100,000 individuals of EAC and SCC In North America is estimated to be 1.9% and 0.9%, respectively (2). EAC is by far the most common subtype in the Western world, with SCC being the most common cancer worldwide. The risk factors for EAC are white race, male gender, presence of gastroesophageal reflux disease, obesity, and Barrett’s esophagus (BE) (1,2). This article will provide a practical approach to indications, effectiveness, and adverse events of endoscopic eradication therapy (EET), including resection and ablative therapies for BE related dysplasia and neoplasia.

BE

BE is an acquired condition characterized by replacing esophageal squamous epithelium with columnar epithelium, or intestinal metaplasia.; and is a precursor of most EAC in the Western world. The annual incidence risk of progression of non-dysplastic BE, low-grade dysplasia (LGD), and high-grade dysplasia (HGD) was reported to be 0.3%, 0.54%, and 1.73%, respectively (3,4). EET removes any dysplastic and nondysplastic BE. This often requires endoscopic resection (ER) of nodular, dysplastic BE, followed by ablation of smooth, nondysplastic BE to achieve complete remission of dysplasia (CRD) and complete remission of intestinal metaplasia (CRIM). A high-quality endoscopic examination with a high-definition white light endoscope and virtual chromoendoscopy such as Narrow Band Imaging (Olympus), Blue Light Imaging (Fuji), or i-Scan (Pentax) should be performed to identify any visible lesions (5). Using a clear cap attachment to the endoscope to facilitate close inspection of the mucosa (6). BE should be described using the Prague classification, and any mucosal irregularities (“nodular BE”) should be defined according to the Paris classification (5). Biopsies should be obtained according to the Seattle protocol, which requires biopsy samples every 1 to 2 cm in 4 quadrants for salmon-colored mucosa >1 cm proximal to the esophagogastric junction.

ER

Endoscopic ultrasound (EUS) offers limited evaluation of early esophageal cancer, limited to the mucosa/or submucosa. ER, when feasible, is both therapeutic and diagnostic due to the ability to provide histopathologic T staging. If possible, nodular mucosa should be resected endoscopically (7,8). In the case of carcinoma, ER can assist with accurate T staging, margin status, tumor differentiation, and lymphovascular invasion. ER of EAC is considered curative when all of the following criteria are met: lateral and deep margins (<500 µm below the muscularis mucosa for esophageal tumors) are negative (R0 resection), well (G1) or moderately (G2) differentiated, absence of lymphovascular invasion, with the lack of deep invasion into the submucosa (<500 microns) (9,10).

The two ER techniques used in the esophagus are endoscopic mucosal resection (EMR) and endoscopic submucosal dissection (ESD).

EMR

EMR involves lifting the lesion followed by snare resection. There are two commonly used EMR techniques in the esophagus: band ligation EMR and cap-assisted EMR.

Band ligation EMR

This technique involves a banding device mounted on an upper endoscope similar to esophageal varices banding. The lesion is suctioned into the device; the band is deployed over the lesion, followed by electrocautery snare resection above or below the cap. This technique does not involve submucosal injection, as band ligation leads to mucosa retraction from the muscularis propria layer. This technique is commonly used due to lower cost and shorter procedure time.

Cap-assisted EMR

This technique involves clear cap-mounted endoscopy after submucosal injection followed by a crescent-shaped electrocautery snare passing through the biopsy channel. The lesion is suctioned into the cap, and the snare is closed for resection of the lesion.

Efficacy and safety

The effectiveness of EMR, low risk of adverse events, and technical ease have been established by multiple studies, leading to its widespread acceptance as a primary resection modality. Randomized trials comparing both EMR techniques have shown similar resection and safety outcomes, but band assisted EMR was found to have shortened procedure time and lower costs (11,12). A study of 1,000 patients on outcomes of EMR for BE-related mucosal adenocarcinoma reported an initial response rate of 96.3%. Recurrence was reported in 14.5% of cases retreated with EMR resulting in a long-term complete remission rate of 93.8% (13). In another study, the local recurrence rate of neoplasia after complete ER was reported to be 6.4% over a mean follow-up of 5 years (14). On multivariable analysis, the length of Barrett’s was associated with recurrence (14). In a meta-analysis comparing complete ER of BE and targeted EMR of suspected dysplastic lesions followed by radiofrequency ablation (RFA) of nondysplastic, smooth BE reported similar rates of complete eradication of neoplasia (94.9% vs. 93.4%) but complete ER was associated with higher rates of strictures [odds ratio (OR), 4.73], perforation (OR, 7.00) and bleeding (OR, 6.88) (15). The common complications after EMR are bleeding (1%), perforation (0.2% to 1.3%), and stricture formation (10%) (15,16).

EMR, however, has several limitations despite its excellent safety and efficacy profile. Lesions greater than 1.5 cm in size that cannot be removed en-bloc and piecemeal resection is associated with higher recurrence rates (13). Therefore, patient selection remains essential to obtaining the best oncologic outcome and decreasing the recurrence rate.

ESD

ESD was initially developed in Japan for resection of gastric neoplasia, and then the technique was extended to treat esophageal, colonic, and duodenal neoplasia. ESD allows for en-bloc resection despite their size or associated fibrosis. For Barrett’s related neoplasia, ESD can be considered for visible lesions greater than 1.5 cm in size, poorly lifting lesions, or those suspected of submucosal involvement. ESD also allows for en-bloc resection of tumors and precise histopathologic analysis.

The American Gastroenterological Association and European Society of Gastrointestinal Endoscopists propose ESD for curative resection of lesions with invasion up to the submucosa (vertical margin ≤500 µm, sm1), well or moderately differentiated tumors without lymphovascular invasion as these tumors have low risk of lymph node metastasis and tumors >15 mm in size (9,10).

Technique

The steps of ESD include marking the periphery, submucosal injection with viscous solution, making a mucosal incision around the lesion, and dissecting through the submucosa beneath the lesion using an electrocautery knife, which allows the lesion to be removed in one en-bloc piece. The main challenge with ESD is the technical difficulty and time it takes to perform the procedure, which has limited its use in the West.

However, procedural and device innovation is now making ESD easier and safer. Adequate visualization during ESD can be maintained by applying traction on the lesion. Yoshida and colleagues showed in a randomized multicenter trial that clip line traction assisted ESD resulted in significantly shorter procedure time than conventional ESD (44.5 vs. 60.5 minutes, respectively; P<0.001) (17). Traction wire assisted ESD has been shown to have significantly lower procedure time than conventional ESD. In a multicenter study, traction wire ESD was shown to have shorter submucosal dissection (7.0±1.9 vs. 18.3±3.4 minutes; P<0.001) and total ESD time (21.5±4.1 vs. 29.5±7.7 minutes; P=0.049 with en-bloc and R0 resection rates of 98.1% and 98.03%, respectively (18).

Precise dissection is achieved by electrosurgical knife during ESD. The insulated tip (IT) knife is mounted by a ceramic ball at the end, which protects the muscle layer from injury during ESD. Recently, the IT knife tunneling technique has been shown to have R0 resection rates of 88.1%, en-bloc resection of 97.6%, and no perforations (19).

Efficacy and safety

Esophageal ESD for Barrett’s related neoplasia has shown high rates of en-bloc resection (80–100%) with low rates of complications. An initial multicenter study on the role of ESD for early neoplastic BE, ESD had en-bloc and complete resection rates of 96% and 70%, respectively (20). The authors reported one perforation and three bleeding events post-ESD, all managed endoscopically. Since then, data from the West has become more encouraging and reassuring. Another European study reported en-bloc, R0 resection, and adverse events rates of 90.8%, 79%, and 3.5%, respectively after esophageal ESD (21). A pooled meta-analysis of ESD for early BE-related neoplasia, including studies from east and west, reported high rates of en-bloc (92.9%), R0 (74.5%), and curative resection rates (64.9%) (22). Rates of perforation, bleeding, and stricture formation were 1.5%, 1.7%, and 11.6%, respectively (22). The majority of perforation and bleeding complications can be managed endoscopically. The major long-term adverse event after ESD is stricture formation, which is reported to occur in 12–17% of cases (23). Stricture formation is more common when >2/3 the circumference of the esophageal mucosal is resected, and almost always occurs when complete circumferential resections are performed.

A few strategies have been proposed to decrease stricture formation with variable benefits, the most common being injection of steroids into the remain submucosa after ESD and/or local steroids (24-26). The other methods include balloon dilation, stent placement, or local botulinum toxin injection (27,28). Tissue shielding agents such as carboxy-methyl cellulose are under investigation (29-31). In the United States, swallowed topical steroids (fluticasone) are used for post-ESD stricture prophylaxis.

EMR vs. ESD for Barrett’s-associated neoplasia

Limited data compares EMR and ESD for Barrett’s related neoplasia from the Western world. Only one small, randomized trial compares EMR and ESD from Germany (32). The authors reported significantly higher rates of en-bloc (100% vs. 15%) and R0 resection (58.8% vs. 11%) along with higher rates of perforation but no difference in complete remission (93.7% vs. 94.1%) at 3 months with ESD as compared to EMR. This study was limited by a small sample size and a very short follow-up of 3 months to assess recurrence (32). In the case of piecemeal resection, local recurrence was reported to be significantly lower with ESD than with EMR (33). Recently, a multicenter study of 243 patients from the United States comparing ESD vs. EMR showed a significantly higher rate of en-bloc (ESD 89% vs. EMR 43%; P=0.001) and R0 resection (ESD 73% vs. EMR 56%; P=0.01). In addition, ESD was associated with significantly lower rates of recurrence (3.5% vs. 31.4%, P<0.05) after a median follow-up of 15.5 months as compared to EMR, and both modalities had similar rates of adverse events (34). Patients undergoing ESD had significantly higher rates of CRD compared to cap assisted EMR (85.6% vs. 75.8%, P<0.01) but similar rates of CRIM after 2 years of follow-up (35). ESD is not only done for curative resection but can also be performed as a staging procedure with curative intent, especially for T1b lesions. Current literature suggests existing strategies, including EUS and biopsy, have poor diagnostic accuracy (30–50%) in discriminating between T1a and T1b (36). Esophagectomy is the recommended management for good operative candidates for T1b cancers due to the risk of nodal metastases. However, in patients who are not ideal candidates for esophagectomy, EET may be considered. In a multicenter study of pathologic diagnosis of T1b lesion after ESD, EUS under staged disease as Tis/T1a in 50% of cases. In contrast, EUS appropriately staged disease as T1b in only 50% of patients who underwent EUS before ESD. Among the patients who underwent surveillance (N=49), recurrence was noted in 20.4%, and 79.6% of patients remained cancer-free after a median follow-up of 20 months. No recurrences were seen in patients with T1b esophageal cancer within curative criteria. Among the patients with recurrence, five developed metastatic disease, and five had local recurrence (37). Demonstrating that caution must be used in patient with ESD of deep submucosal esophageal cancers outside of curative criteria. ESD helps accurately stage esophageal cancer and determine the need for further adjuvant therapy and surgery for patients with non-curative resection. Patient selection, accurate staging, and available expertise are key to achieving optimal outcomes after ER.

Endoscopic ablation of neoplastic lesions of the esophagus

Endoscopic ablative therapies use heat [delivered by laser, electrocoagulation, argon plasma coagulation (APC), or radiofrequency energy], cold (cryotherapy, delivered by spraying cold carbon dioxide gas), or photochemical energy [photodynamic therapy (PDT)]. Endoscopic ablative therapies aim to eradicate BE and flat dysplasia after resection of any raised lesion or mucosal abnormalities.

RFA

RFA is the most common and widely approved ablative technique. It uses a balloon-based array of spaced electrodes to deliver microwave energy to ablate the esophageal mucosa. It was designed to inflict uniform, circumferential thermal injury, where a generator can control the power, density, and duration of the energy applied. The RFA technique delivers energy deep enough to destroy abnormal epithelium with low risk for complications such as esophageal bleeding, and perforation. The balloon RFA catheters can ablate circumferential areas of BE. In contrast, the smaller focal catheter ablation devices are used to ablate short segments of Barrett metaplasia or residual foci of metaplasia. RFA is contraindicated in nodular BE. RFA can be combined with EMR or ESD to treat residual areas of BE.

In the European Surveillance versus Radiofrequency Ablation (SURF) trial, 136 patients with BE with LGD (confirmed by expert pathologists) were randomized to either RFA or endoscopic surveillance. RFA reduced the risk of progression to HGD or adenocarcinoma by 25.0% [1.5% for ablation vs. 26.5% for control; 95% confidence interval (CI): 14.1% to 35.9%; P<0.001]. RFA reduced the risk of progression to adenocarcinoma by 74% (1.5% for ablation vs. 8.8% for control; 95% CI: 0% to 14.7%; P=0.03) (38). In a multicenter, randomized, sham-controlled trial of RFA (The Ablation of Intestinal Metaplasia Dysplasia Trial), patients were randomized to receive either RFA or a sham endoscopic procedure. At 1 year, CRIM was found in 77.4% of all patients in the ablation group, compared with 2.3% in the control group (P<0.001) (39). Complete eradication of dysplasia was higher in both the HGD group (81.0% vs. 19.0%) and the LGD group (90.5% vs. 22.7%) when compared to the control group (P<0.001). The ablation group recorded fewer cancers (1.2% vs. 9.3%, P=0.45) and less progression in the degree of neoplasia (3.6% vs. 16.3%, P=0.03) at 1 year (39). At a long-term follow-up of 10 years, 4.1% of patients reported EAC after RFA (40). ER is necessary to achieve CRIM for visible lesions. RFA can be performed either alone or after ER. Based on a systematic review and pooled analysis of 20 cohort studies, RFA following ER was deemed effective for patients with HGD/EAC (15). The rate of adverse events after RFA is reported to be 5.6%, 1%, 0.6%, and <0.5% for strictures, bleeding, perforation, and pain, respectively (41). The authors also reported a 25% increase in AE rate with each 1 cm increase in median BE length. When comparing stepwise complete ER of BE and targeted EMR of suspected dysplastic lesions followed by RFA, the complete eradication of neoplasia rates are similar, but the stepwise complete ER arm had higher rates of adverse events (15).

Cryotherapy

Endoscopic cryotherapy causes rapid tissue freezing and thawing, leading to cell membrane disruption, local vasculature thrombosis leading to cellular ischemia and reperfusion injury, and cell apoptosis. Compressed carbon dioxide or liquid nitrous oxide are the common cryogens. Liquid nitrogen cryospray and nitrous oxide-based cryoballoon ablation (CBA) therapies are the main cryoablation techniques. The main difference between the two techniques is the cryogen’s delivery method. In the liquid-nitrogen cryospray technique, the nitrous oxide gas is delivered in a no-contact fashion and simultaneously suctioned. In the newer generation CBA technique, nitrous oxide is contained within a balloon and applied directly to a mucosal surface. The efficacy of cryotherapy in eradicating intestinal metaplasia and dysplasia ranges from 60% to 85% based on the grade of dysplasia and the cryoablation technique (42,43). Cryoablation may have a role in the treatment of persistent BE after RFA ablation. In a systematic review and meta-analysis, liquid nitrogen cryoablation was able to achieve CRIM in 45.9% who did not respond to initial RFA treatment (44). A recent propensity score matched cohort study comparing CBA and RFA found comparable chance of achieving CRIM and CRD with both modalities, but higher stricture rates in the cryoballoon group (45).

Hybrid APC

APC uses a contact-free endoscopic ablation technique that utilizes a jet of ionized Argon gas to generate thermal energy to ablate tissue to a consistent depth to minimize submucosal injury and the risk of stricture formation or bleeding (46). A novel hybrid APC method was developed due to the higher rate of AEs associated with APC. First, the mucosa is raised with a high-pressure water jet to create a submucosal, and then ablation is performed. The submucosal cushion acts as a thermal insulation barrier, which allows energy to dissipate to the required depth without significant damage to the submucosa. There are no prospective trials comparing hybrid APC with other modalities. The CRIM of hybrid APC is 81.8% compared to other modalities (47). However, the long-term efficacy is unclear, and the rate of AEs is higher than other modalities (48). A study of 154 patients reported a CRIM rate of 87.2% with 6.1% adverse events rate. On a 2-year follow-up of the 129 successfully treated cases, 65.9% showed sustained CRIM with neoplasia recurrence in 3 cases (48).

PDT

PDT relies on photosensitizers to induce cell death when exposed to certain wavelengths. It was one of the first ablative techniques used for BE, with 52% eradication of intestinal metaplasia, but it has a very high stricture rate of 36% at five five-year follow-ups (49). There are significant drawbacks to PDT. These include the need for IV administration agents and extended periods of photosensitization. RFA has largely replaced PDT due to its higher cost, side effect profile, and cumbersome setup (50).

Follow-up and surveillance

Follow-up after EET is of paramount importance to prevent recurrence and progression. The recommended interval depends on baseline histology. Patients undergoing EMR with HGD and intramucosal carcinoma are recommended to have follow-up endoscopy at 3, 6, and 12 months after CRIM and annually after that. Patients with LGD who undergo EET are advised to have surveillance at 1 and 3 years. Studies have suggested higher recurrence rates in the first year, with a constant lower rate thereafter (51,52). In the recent American Gastroenterological Association clinical practice update, we gave expert opinion guidance for surveillance after ESD resection (9). For patients who had ESD resection of T1a EAC, ablation therapy to achieve CRIM was recommended. After CRIM was achieved endoscopic surveillance should be performed every 6 months for the first 2 years then yearly. For patients who had ESD resection of T1b EAC within curative criteria, closer surveillance is recommended, as well as consideration of EUS and annual CT scans to assess for lymph nodes during surveillance.

Summary and conclusions

Endoscopic therapy caused a paradigm change in the management of early Barrett’s related neoplasia, allowing most patients to avoid the significant morbidity and mortality associated with surgery. Now, advances in ESD will enable us to remove larger and bulker lesions en-bloc, which was previously impossible with EMR. Device and procedure innovation makes ESD easier and safer to perform so that more patients can benefit from these procedures. Future studies are needed to understand the role of ER in more advanced T1b tumors and to help understand which lesions benefit from ESD vs. EMR.

BE-associated neoplasia remains an essential cause of EAC in the West, and EET is the cornerstone in eradicating BE. The latest technological advancements in ablation and resection techniques have improved outcomes. Multidisciplinary discussion and available institutional expertise remain the most critical factors in achieving the best outcomes in this patient population.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editor (Terry L. Jue) for the series “A U. S. Perspective on Endoscopic Resection of Neoplastic Lesions of the Gastrointestinal Tract” published in Annals of Laparoscopic and Endoscopic Surgery. The article has undergone external peer review.

Peer Review File: Available at https://ales.amegroups.com/article/view/10.21037/ales-23-33/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://ales.amegroups.com/article/view/10.21037/ales-23-33/coif). The series “A U. S. Perspective on Endoscopic Resection of Neoplastic Lesions of the Gastrointestinal Tract” was commissioned by the editorial office without any funding or sponsorship. A.B. and his institution received consulting fees from Medtronic, Boston Scientific and Steris and received royalties from Medtronic. He also holds patents from Medtronic. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Morgan E, Soerjomataram I, Rumgay H, et al. The Global Landscape of Esophageal Squamous Cell Carcinoma and Esophageal Adenocarcinoma Incidence and Mortality in 2020 and Projections to 2040: New Estimates From GLOBOCAN 2020. Gastroenterology 2022;163:649-658.e2. [Crossref] [PubMed]
2. Rumgay H, Arnold M, Laversanne M, et al. International Trends in Esophageal Squamous Cell Carcinoma and Adenocarcinoma Incidence. Am J Gastroenterol 2021;116:1072-6. [Crossref] [PubMed]
3. Singh S, Manickam P, Amin AV, et al. Incidence of esophageal adenocarcinoma in Barrett’s esophagus with low-grade dysplasia: a systematic review and meta-analysis. Gastrointest Endosc 2014;79:897-909.e4; quiz 983.e1, 983.e3.
4. Sharma P. Barrett Esophagus: A Review. JAMA 2022;328:663-71. [Crossref] [PubMed]
5. Shaheen NJ, Falk GW, Iyer PG, et al. Diagnosis and Management of Barrett’s Esophagus: An Updated ACG Guideline. Am J Gastroenterol 2022;117:559-87. [Crossref] [PubMed]
6. Chen BL, Xing XB, Wang JH, et al. Improved biopsy accuracy in Barrett’s esophagus with a transparent cap. World J Gastroenterol 2014;20:4718-22. [Crossref] [PubMed]
7. Wani S, Mathur SC, Curvers WL, et al. Greater interobserver agreement by endoscopic mucosal resection than biopsy samples in Barrett’s dysplasia. Clin Gastroenterol Hepatol 2010;8:783-8. [Crossref] [PubMed]
8. Vantanasiri K, Iyer PG. State-of-the-art management of dysplastic Barrett’s esophagus. Gastroenterol Rep (Oxf) 2022;10:goac068. [Crossref] [PubMed]
9. Wang AY, Hwang JH, Bhatt A, et al. AGA Clinical Practice Update on Surveillance After Pathologically Curative Endoscopic Submucosal Dissection of Early Gastrointestinal Neoplasia in the United States Gastroenterology 2021;161:2030-2040.e1. Commentary. [Crossref] [PubMed]
10. Pimentel-Nunes P, Libânio D, Bastiaansen BAJ, et al. Endoscopic submucosal dissection for superficial gastrointestinal lesions: European Society of Gastrointestinal Endoscopy (ESGE) Guideline - Update 2022. Endoscopy 2022;54:591-622. [Crossref] [PubMed]
11. May A, Gossner L, Behrens A, et al. A prospective randomized trial of two different endoscopic resection techniques for early stage cancer of the esophagus. Gastrointest Endosc 2003;58:167-75. [Crossref] [PubMed]
12. Pouw RE, van Vilsteren FG, Peters FP, et al. Randomized trial on endoscopic resection-cap versus multiband mucosectomy for piecemeal endoscopic resection of early Barrett’s neoplasia. Gastrointest Endosc 2011;74:35-43. [Crossref] [PubMed]
13. Pech O, May A, Manner H, et al. Long-term efficacy and safety of endoscopic resection for patients with mucosal adenocarcinoma of the esophagus. Gastroenterology 2014;146:652-660.e1. [Crossref] [PubMed]
14. Anders M, Bähr C, El-Masry MA, et al. Long-term recurrence of neoplasia and Barrett’s epithelium after complete endoscopic resection. Gut 2014;63:1535-43. [Crossref] [PubMed]
15. Desai M, Saligram S, Gupta N, et al. Efficacy and safety outcomes of multimodal endoscopic eradication therapy in Barrett’s esophagus-related neoplasia: a systematic review and pooled analysis. Gastrointest Endosc 2017;85:482-495.e4. [Crossref] [PubMed]
16. Bhatt A, Kamath S, Murthy SC, et al. Multidisciplinary Evaluation and Management of Early Stage Esophageal Cancer. Surg Oncol Clin N Am 2020;29:613-30. [Crossref] [PubMed]
17. Yoshida M, Takizawa K, Nonaka S, et al. Conventional versus traction-assisted endoscopic submucosal dissection for large esophageal cancers: a multicenter, randomized controlled trial (with video). Gastrointest Endosc 2020;91:55-65.e2. [Crossref] [PubMed]
18. Joseph A, Kahaleh M, Li AA, et al. Initial Multicenter Experience of Traction Wire Endoscopic Submucosal Dissection. Techniques and Innovations in Gastrointestinal Endoscopy 2023;25:2109. [Crossref]
19. Mehta NA, Abe S, Vargo JJ, et al. Insulated-tip Knife Tunneling and C-shaped Incision for Esophageal Endoscopic Submucosal Dissection: An Initial Western Experience. Techniques and Innovations in Gastrointestinal Endoscopy 2021;23:152-8. [Crossref]
20. Yang D, Coman RM, Kahaleh M, et al. Endoscopic submucosal dissection for Barrett’s early neoplasia: a multicenter study in the United States. Gastrointest Endosc 2017;86:600-7. [Crossref] [PubMed]
21. Subramaniam S, Chedgy F, Longcroft-Wheaton G, et al. Complex early Barrett’s neoplasia at 3 Western centers: European Barrett’s Endoscopic Submucosal Dissection Trial (E-BEST). Gastrointest Endosc 2017;86:608-18. [Crossref] [PubMed]
22. Yang D, Zou F, Xiong S, et al. Endoscopic submucosal dissection for early Barrett’s neoplasia: a meta-analysis. Gastrointest Endosc 2018;87:1383-93. [Crossref] [PubMed]
23. Kim JS, Kim BW, Shin IS. Efficacy and safety of endoscopic submucosal dissection for superficial squamous esophageal neoplasia: a meta-analysis. Dig Dis Sci 2014;59:1862-9. [Crossref] [PubMed]
24. Bahin FF, Jayanna M, Williams SJ, et al. Efficacy of viscous budesonide slurry for prevention of esophageal stricture formation after complete endoscopic mucosal resection of short-segment Barrett’s neoplasia. Endoscopy 2016;48:71-4. [PubMed]
25. Hashimoto S, Kobayashi M, Takeuchi M, et al. The efficacy of endoscopic triamcinolone injection for the prevention of esophageal stricture after endoscopic submucosal dissection. Gastrointest Endosc 2011;74:1389-93. [Crossref] [PubMed]
26. Mejía Pérez LK, Abe S, Siva R, et al. Esophageal ESD. In: Wagh MS, Wani SB, editors. Gastrointestinal Interventional Endoscopy: Advanced Techniques. Cham: Springer International Publishing; 2020. p. 83-95.
27. Ezoe Y, Muto M, Horimatsu T, et al. Efficacy of preventive endoscopic balloon dilation for esophageal stricture after endoscopic resection. J Clin Gastroenterol 2011;45:222-7. [Crossref] [PubMed]
28. Wen J, Lu Z, Linghu E, et al. Prevention of esophageal strictures after endoscopic submucosal dissection with the injection of botulinum toxin type A. Gastrointest Endosc 2016;84:606-13. [Crossref] [PubMed]
29. Lua GW, Tang J, Liu F, et al. Prevention of Esophageal Strictures After Endoscopic Submucosal Dissection: A Promising Therapy Using Carboxymethyl Cellulose Sheets. Dig Dis Sci 2016;61:1763-9. [Crossref] [PubMed]
30. Ohki T, Yamato M, Ota M, et al. Application of regenerative medical technology using tissue-engineered cell sheets for endoscopic submucosal dissection of esophageal neoplasms. Dig Endosc 2015;27:182-8. [Crossref] [PubMed]
31. Sakaguchi Y, Tsuji Y, Ono S, et al. Polyglycolic acid sheets with fibrin glue can prevent esophageal stricture after endoscopic submucosal dissection. Endoscopy 2015;47:336-40. [PubMed]
32. Terheggen G, Horn EM, Vieth M, et al. A randomised trial of endoscopic submucosal dissection versus endoscopic mucosal resection for early Barrett’s neoplasia. Gut 2017;66:783-93. [Crossref] [PubMed]
33. Sgourakis G, Gockel I, Lang H. Endoscopic and surgical resection of T1a/T1b esophageal neoplasms: a systematic review. World J Gastroenterol 2013;19:1424-37. [Crossref] [PubMed]
34. Mejia Perez LK, Yang D, Draganov PV, et al. Endoscopic submucosal dissection vs. endoscopic mucosal resection for early Barrett’s neoplasia in the West: a retrospective study. Endoscopy 2022;54:439-46. [Crossref] [PubMed]
35. Codipilly DC, Dhaliwal L, Oberoi M, et al. Comparative Outcomes of Cap Assisted Endoscopic Resection and Endoscopic Submucosal Dissection in Dysplastic Barrett’s Esophagus. Clin Gastroenterol Hepatol 2022;20:65-73.e1. [Crossref] [PubMed]
36. Liu K, Aadam AA. T1b esophageal cancer: Is it time for endoscopic submucosal dissection to enter the stage? Gastrointest Endosc 2022;96:454-6. [Crossref] [PubMed]
37. Joseph A, Draganov PV, Maluf-Filho F, et al. Outcomes for endoscopic submucosal dissection of pathologically staged T1b esophageal cancer: a multicenter study. Gastrointest Endosc 2022;96:445-53. [Crossref] [PubMed]
38. Phoa KN, van Vilsteren FG, Weusten BL, et al. Radiofrequency ablation vs endoscopic surveillance for patients with Barrett esophagus and low-grade dysplasia: a randomized clinical trial. JAMA 2014;311:1209-17. [Crossref] [PubMed]
39. Shaheen NJ, Sharma P, Overholt BF, et al. Radiofrequency ablation in Barrett’s esophagus with dysplasia. N Engl J Med 2009;360:2277-88. [Crossref] [PubMed]
40. Wolfson P, Ho KMA, Wilson A, et al. Endoscopic eradication therapy for Barrett’s esophagus-related neoplasia: a final 10-year report from the UK National HALO Radiofrequency Ablation Registry. Gastrointest Endosc 2022;96:223-33. [Crossref] [PubMed]
41. Qumseya BJ, Wani S, Desai M, et al. Adverse Events After Radiofrequency Ablation in Patients With Barrett’s Esophagus: A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol 2016;14:1086-1095.e6. [Crossref] [PubMed]
42. Canto MI, Trindade AJ, Abrams J, et al. Multifocal Cryoballoon Ablation for Eradication of Barrett’s Esophagus-Related Neoplasia: A Prospective Multicenter Clinical Trial. Am J Gastroenterol 2020;115:1879-90. [Crossref] [PubMed]
43. Westerveld DR, Nguyen K, Banerjee D, et al. Safety and effectiveness of balloon cryoablation for treatment of Barrett’s associated neoplasia: systematic review and meta-analysis. Endosc Int Open 2020;8:E172-8. [Crossref] [PubMed]
44. Visrodia K, Zakko L, Singh S, et al. Cryotherapy for persistent Barrett’s esophagus after radiofrequency ablation: a systematic review and meta-analysis. Gastrointest Endosc 2018;87:1396-1404.e1. [Crossref] [PubMed]
45. Agarwal S, Alshelleh M, Scott J, et al. Comparative outcomes of radiofrequency ablation and cryoballoon ablation in dysplastic Barrett’s esophagus: a propensity score-matched cohort study. Gastrointest Endosc 2022;95:422-431.e2. [Crossref] [PubMed]
46. Manner H, May A, Miehlke S, et al. Ablation of nonneoplastic Barrett’s mucosa using argon plasma coagulation with concomitant esomeprazole therapy (APBANEX): a prospective multicenter evaluation. Am J Gastroenterol 2006;101:1762-9. [Crossref] [PubMed]
47. Shimizu T, Samarasena JB, Fortinsky KJ, et al. Benefit, tolerance, and safety of hybrid argon plasma coagulation for treatment of Barrett’s esophagus: US pilot study. Endosc Int Open 2021;9:E1870-6. [Crossref] [PubMed]
48. Knabe M, Beyna T, Rösch T, et al. Hybrid APC in Combination With Resection for the Endoscopic Treatment of Neoplastic Barrett’s Esophagus: A Prospective, Multicenter Study. Am J Gastroenterol 2022;117:110-9. [Crossref] [PubMed]
49. Overholt BF, Wang KK, Burdick JS, et al. Five-year efficacy and safety of photodynamic therapy with Photofrin in Barrett’s high-grade dysplasia. Gastrointest Endosc 2007;66:460-8. [Crossref] [PubMed]
50. Ertan A, Zaheer I, Correa AM, et al. Photodynamic therapy vs radiofrequency ablation for Barrett’s dysplasia: efficacy, safety and cost-comparison. World J Gastroenterol 2013;19:7106-13. [Crossref] [PubMed]
51. Sawas T, Iyer PG, Alsawas M, et al. Higher Rate of Barrett’s Detection in the First Year After Successful Endoscopic Therapy: Meta-analysis. Am J Gastroenterol 2018;113:959-71. [Crossref] [PubMed]
52. van Munster S, Nieuwenhuis E, Weusten BLAM, et al. Long-term outcomes after endoscopic treatment for Barrett’s neoplasia with radiofrequency ablation ± endoscopic resection: results from the national Dutch database in a 10-year period. Gut 2022;71:265-76. [Crossref] [PubMed]