Background: Endoscopic therapy has replaced esophagectomy for the management of early Barrett’s neoplasia, allowing for the curative treatment of intramucosal adenocarcinoma, dysplastic Barrett’s esophagus (BE), and the prevention of metachronous recurrences. Summary: Endoscopic therapy relies on the resection of any visible lesion, suspicious of harboring cancer, followed by the eradication of the residual BE, potentially harboring dysplastic foci. Currently, endoscopic mucosal resection (EMR) using the multiband mucosectomy technique is the gold standard for the resection of visible lesions. Endoscopic submucosal dissection (ESD) is feasible with comparable complication rates to EMR, but longer procedural times. It is still limited to EMR failures or suspected submucosal adenocarcinoma. Eradication of residual BE mainly relies on radiofrequency ablation, with over 90% efficacy in expert centers. Despite initial complete eradication of BE, intestinal metaplasia and dysplasia recur in time, justifying prolonged endoscopic surveillance. Key Messages: The first step of the therapeutic endoscopy for BE is a careful diagnostic evaluation, searching for visible(s) lesion(s). EMR is the recommended resection technique for visible lesions. ESD has not demonstrated its superiority on EMR in routine practice. Endoscopic follow-up after Barrett’s eradication therapy is mandatory.

Endoscopic therapy of early Barrett’s neoplasia aims at resecting early adenocarcinoma and preventing the progression of dysplastic Barrett’s esophagus (BE) toward invasive adenocarcinoma. The indications for endoscopic therapy, presented in Table 1, do not include nondysplastic BE, considering the scarcity of the data, and the possible unfavorable risk to benefit ratio [1]. While the indications of endoscopic therapy for visible lesions, high-grade dysplasia (HGD), or early (T1) adenocarcinoma is consensual, the optimal management of low-grade dysplasia (LGD) is still debated. Three randomized trials have addressed the question of endoscopic therapy for LGD, concluding to a probable benefit in terms of neoplastic progression rate (nonstatistically significant in 2/3 studies) [2]. The spontaneous regression of LGD and the morbidity of endoscopic therapy have led to cautious recommendations on the management of patients with LGD [1]. In clinical practice, the indication for endoscopic therapy for confirmed and repeated multifocal LGD is discussed on a case-to-case basis.

Table 1.

Indications of endoscopic therapy for early Barrett’s neoplasia

Indications of endoscopic therapy for early Barrett’s neoplasia
Indications of endoscopic therapy for early Barrett’s neoplasia

The principle of endoscopic therapy is first to resect any visible abnormality, and then to eradicate intestinal metaplasia (IM) in the esophagus [1, 3]. Indeed, the presence of a visible abnormality, either slightly depressed (Paris 0-IIc), flat (Paris 0-IIb), or elevated (Paris 0-IIa), associated or not with modifications of the pit pattern or vascular pattern, is highly predictive of neoplasia, and requires to rule out invasive adenocarcinoma. Logically, endoscopic submucosal dissection (ESD), endoscopic mucosal resection (EMR), and endoscopic mucosal biopsies have decreasing accuracy for the histological diagnosis of BE-associated lesions [4, 5]. In clinical practice, EMR is the most widely accepted resection tool for visible lesions arising in BE. After resection of a dysplastic lesion, the residual BE is considered to harbor other dysplastic foci, with up to 21% metachronous recurrence rate at 5 years [6]. The complete eradication of IM (CE-IM) can be achieved by means of endoscopic resection, mostly in cases of BE tongues. In cases of circumferential BE, owing to a significant risk of esophageal strictures, thermal ablation of the residual BE is preferred [7]. Once CE-IM is achieved, as in 78%–94% of the patients [8, 9], lifelong endoscopic follow-up is recommended with random biopsies of the neosquamous epithelium and the gastric cardia. We will present the state of the art in clinical practice and research in BE endoscopic therapy, and address commonly made mistakes in the management of Barrett’s neoplasia.

Endoscopic Mucosal Resection

Endoscopic Resection-Cap

Historically, esophageal EMR was performed using the endoscopic resection-cap technique, involving a specifically designed oblique distal attachment cap of 12 mm with a distal ridge, allowing to place an asymmetrical snare. After submucosal injection and suctioning of the lesion in the cap, the snare is tightened and the lesion resected. As demonstrated by a randomized controlled trial [10], this technique is associated with higher costs, longer procedural times, and more esophageal perforations, and is currently abandoned for BE.

Multiband Mucosectomy

Multiband mucosectomy (MBM) involves a modified variceal band ligation device and a polypectomy snare (Duette MBM system, Cook, Ireland and Captivator System, Boston Scientific, Natick, MA, USA). After a first diagnostic step – without the cap – and delineation of the lesions, the lesion is sucked in the cap and a band is released as during esophageal varices band ligation. This creates a pseudopolyp, which is resected with a snare. This technique allows performing six consecutive EMR without removing the endoscope and replacing the snare as is the case within endoscopic resection-cap procedure.

Besides the aforementioned randomized controlled trial [10], large MBM resection cohorts involving over 200 procedures confirmed the safety of the technique, with less than 1% esophageal perforations, 1.5%–2% delayed bleeding, and 3%–4% esophageal strictures [11, 12]. As a consequence, MBM has become the preferred endoscopic resection technique for early Barrett’s neoplasia.

The Concept of EMR for Early Barrett’s Neoplasia

Long-term (>5 years) follow-up data show the satisfying oncological results of EMR for early Barrett’s neoplasia, with 96%–97% remission rates of neoplasia after the EMR of HGD or intramucosal (T1a) carcinomas [6, 13]. Although against the principles of oncologic surgery that advise en bloc excision of any neoplasia, piecemeal endoscopic resection, even of intramucosal adenocarcinoma, does not result in a pejorative oncological outcome. This exception to the rule can be explained by the virtual risk of lymph node metastasis in this disease, and the contribution of the ablative therapies such as radiofrequency ablation (RFA) that will follow, allowing to destroy residual dysplastic foci.

Common Mistakes in EMR

Omitting the Specific Technical Aspects of Esophageal EMR. The most important step of the endoscopic procedure is the diagnostic evaluation. The routine use of chromoendoscopy (including virtual chromoendoscopy) during BE endoscopic surveillance is recommended, to improve the detection of neoplastic lesions [14] and to detect residual IM during BE eradication therapy [1, 3, 14]. Chromoendoscopy (particularly virtual chromoendoscopy) is also used to help delineating the neoplastic lesions before resection. Although not recommended in the latest guidelines, the use of a distal attachment cap can help to examine the folds of the gastric cardia. In addition, the cap allows to check that the target lesion is actually suctionnable in the cap and not fixed to the deeper layers of the esophageal wall. During MBM, some specific aspects of the technique, such as avoiding submucosal lifting, cutting below the band, and using pure coagulation current are often overlooked. This can result in major bleeding and small resection specimens with a creation of mucosal bridges. In the case of mucosal bridges between the resections, they should be resected with submucosal lifting and conventional EMR without suction to avoid perforation [15].

Performing Circumferential Endoscopic Resections. Performing complete circumferential EMR is technically feasible and gives the endoscopist the feeling of having “solved the problem” by resecting all IM and early neoplasia in one to three endoscopic treatment sessions. However, this approach is unadvisable and results in 40%–50% stricture rates [16, 17]. Although some small studies have reported a beneficial effect of local or systemic steroid therapy for esophageal stricture prevention, these results have not been confirmed by prospective and controlled studies [18]. Currently, there is no effective stricture prevention technique after extensive esophageal mucosal resection [19]. Similarly, single-session EMR and RFA of the residual BE may result in esophageal perforation by inadvertent ablation of the exposed submucosa and muscularis propria [20].

Performing EMR for all Early Barrett’s Neoplasia. In 2021, the management of early Barrett’s neoplasia is performed in expert centers in which ESD is easily accessible and safe. Considering the poor diagnostic performances of endosonography to stage T1 adenocarcinomas and the uncertainty of the endoscopic prediction for T1a versus T1b lesions, performing ESD of all T1 esophageal adenocarcinomas is conceivable. Indeed, en bloc resection allows an optimal histological analysis and prediction of the risk of lymph node metastasis [5]. In this perspective, the indications for EMR could become restricted to nodular BE, LGD or HGD on BE, or residual BE after initial endoscopic resection, as an alternative to ablative therapies.

Endoscopic Submucosal Dissection

ESD in Barrett’s Esophagus-Related Neoplasia?

ESD has become the standard of care for the resection of esophageal squamous cell neoplasia and gastric adenocarcinoma, considering the virtual local recurrence rate, but also the optimal histological analysis allowed by an en bloc-resected specimen [21]. While an underpowered randomized controlled trial demonstrated the absence of clinical benefit of ESD in the routine management of early Barrett’s neoplasia [22], a number of large retrospective studies confirmed the safety of ESD in this indication with 89%–93% en bloc, 73%–79% R0, and 65%–66% curative resection rates, at the cost of 0%–1.5% perforations, 1.4–2.1% delayed bleeding, and 2.1%–16% stricture rates [23-25]. Thus, the safety profile is similar to EMR, with a possible benefit in terms of histological analysis of esophageal adenocarcinomas [5], but longer procedural times (over 60 mn in most publications). Since the benefit of ESD over EMR mostly relies on the management of high-risk adenocarcinomas (T1b, lymphovascular involvement, poorly differentiated lesions), and these lesions are rare, it is unlikely that prospective comparative evidence will be published demonstrating the superiority of ESD over EMR in early Barrett’s neoplasia. Currently, ESD is therefore restricted to EMR failures (bulky, scarred, and poorly lifting lesions) or lesions >15 mm with a high suspicion of submucosal adenocarcinoma.

Common Mistakes in ESD

Performing ESD for Unselected Lesions. ESD is a powerful treatment tool designed to resect en bloc early digestive cancers. “Just because you can does not mean you should”: a liberal use of ESD for any dysplastic lesion arising on BE could be considered as an overtreatment. Indeed, ESD puts the patient at risk of complications resulting from longer anesthesia time and extensive mucosal resections.

Performing “Small” ESDs. Conversely, once an ESD is planned, the endoscopist should aim for an R0 resection for adenocarcinoma and HGD; therefore, large resection margins, guided by virtual chromoendoscopy and magnification, are advisable.

Endoscopic Ablation

Argon Plasma Coagulation

Argon plasma coagulation (APC) (Erbe, Tübingen, Germany) is a cheap and broadly available technique allowing to ablate flat dysplastic or residual (and potentially dysplastic) BE after endoscopic resection. In a randomized trial involving 63 patients, Manner et al. [26] showed that APC ablation after ER achieved CE-IM in 79% of the patients, and reduced the neoplastic recurrence rate from 37% to 3% at 2 years follow-up. The technique is however limited by its heterogeneity of application (depending on the distance to the mucosa, the ablation settings, the time of application), the long procedural time when ablating circumferential BE segments. As a result, the use of APC is restricted to the ablation of small residual Barrett’s islands or tongues in centers without access to RFA.

Hybrid Argon Plasma Coagulation

A modified APC probe called Hybrid APC allows to inject saline in the submucosal space via an integrated waterjet channel. The aim of the submucosal lifting is to allow high power and more homogeneous ablation in order to improve the outcomes of APC ablation. A 2016 retrospective study reported the results of hybrid APC in BE, reporting more similar efficacy (78% CE-IM after a median 3.5 treatment sessions) than conventional APC, but lower stricture rates (2% vs. 9%) [27]. Recently, a large prospective multicenter study found an 87% rate of CE-IM (71% at 2 years) after a mean of 1.2 endoscopic resections and 2.7 ablation sessions, with a 4% esophageal stricture rate [28]. Considering the availability and ease of use of APC, particularly in the scarred and narrow esophagus, these data could promote the adoption of hybrid APC for the ablation of dysplastic or residual BE.

Radiofrequency Ablation

RFA allows a reproducible and controlled in-depth ablation of BE on the whole surface of a 3 cm, balloon-based over the wire, electrode, or a 20 × 13 mm focal, endoscope-fitting electrode (Barrx 36 Express and Barrx 90, Medtronic, Minneapolis, MN, USA). The technique has been extensively and rigorously studied since the early 2010s, in terms of power settings, short and long-term outcomes [8, 9, 29]. When performed in expert centers, CE-IM is achieved in 94% of the patients, at the cost of 21% adverse events, including 15% esophageal strictures. Following CE-IM, the annual recurrence rate of IM and dysplasia range from 2% to 4% and 1% to 2%, respectively [9, 30]. Of note, this rate excludes recurrent nondysplastic IM at the gastric cardia, of which the clinical significance is debated.

Currently, it is recommended to wash the esophageal mucosa prior to the procedure, and then perform two 10 J/cm2 ablations with a gentle scraping of the mucosal coagulum between the procedures when performing circumferential RFA, and to perform three consecutive 12 J/cm2 ablations, including the esophagogastric junction at least once, when performing focal RFA. Typically, an RFA treatment follows an initial endoscopic resection; it is performed every 3–4 months, under double-dose proton pump inhibitors, and includes one circumferential and two focal RFA treatments.

Cryoablation

Cryoablation of dysplastic or residual BE has been introduced in 2010, but has not gained wide acceptance around the world, considering the outstanding outcomes of RFA. One type of device is liquid nitrogen through the scope spray catheter (TruFreeze, Steris Medical, Mentor, OH, USA) that has been mostly studied in the USA, with suboptimal results in terms of CE-IM (66% after a median of 4 treatment sessions in a recent study involving 62 patients) [31]. Of note, the technique requires the placement of a nasogastric decompression tube to prevent stomach overinsufflation. A second type of device, also based on nitrous oxide spraying, but inside a through the scope balloon that both stabilizes the application and prevents oversinsufflation, has been studied in Europe and in the USA since 2016 [32, 33]. Although the first studies are encouraging, with up to 88% CE-IM in one study involving 41 patients [32], the device itself is still evolving [33], and, the implementation of the Cryoballoon ablation system (Pentax Medical, Redwood City, CA, USA) in the therapeutic armamentarium of BE is still at an early stage.

Common Mistakes on Ablation

Not Performing Ablation. Because of the multifocal nature of dysplasia in BE, metachronous neoplasia occurs in up to 21% of the patients following endoscopic resection of a neoplastic lesion. Therefore, the first mistake of ablation is to forget to ablate the residual BE. When a patient is sent to a referral center for the resection of a visible lesion, both the therapeutic endoscopist and the referring gastroenterologist must make sure that the patient will be scheduled for controls and ablation procedures usually over a whole year following endoscopic resection.

Ablating Visible Lesions. Ablation is meant to treat flat dysplastic BE. This is the case for residual BE and BE with LGD, but very uncommon for BE with HGD, where a visible lesion is almost always detected, requiring initial endoscopic resection. Therefore, the presence of a visible lesion should lead to cancel the ablation procedure, and switch to endoscopic resection. Occasionally, “visible” lesions, characterized by a regular enlarged pit pattern and Paris 0-IIa appearance, usually at the limit of a recent endoscopic resection or in patients with portal hypertension, turn out to be purely inflammatory or hyperplastic and only require postponing the ablation procedure and intensifying the acid suppression therapy (Fig. 1).

Fig. 1.

Endoscopic aspects encountered during endoscopic therapy for early Barrett’s neoplasia. LGD presenting as a Paris 0-IIb lesion mainly visible at 6 o’clock, reddish in white light (a), and with modified pit pattern in narrow-band imaging (b). Early (T1) adenocarcinoma arising in a BE, presenting as a Paris 0-Is lesion at 6 o’clock position with slightly eroded surface, in white light (c) and narrow-band imaging (d). This lesion is a typical indication for en bloc excision by ESD. e, f Examples of “visible,” yet inflammatory and non-neoplastic lesions seen arising in BE during endoscopic therapy. Aspect of recurrent nondysplastic IM at the gastric cardia after initial CE-IM, in white light (g) and narrow-band imaging (h).

Fig. 1.

Endoscopic aspects encountered during endoscopic therapy for early Barrett’s neoplasia. LGD presenting as a Paris 0-IIb lesion mainly visible at 6 o’clock, reddish in white light (a), and with modified pit pattern in narrow-band imaging (b). Early (T1) adenocarcinoma arising in a BE, presenting as a Paris 0-Is lesion at 6 o’clock position with slightly eroded surface, in white light (c) and narrow-band imaging (d). This lesion is a typical indication for en bloc excision by ESD. e, f Examples of “visible,” yet inflammatory and non-neoplastic lesions seen arising in BE during endoscopic therapy. Aspect of recurrent nondysplastic IM at the gastric cardia after initial CE-IM, in white light (g) and narrow-band imaging (h).

Close modal

Performing Unindicated Ablations. Even in expert hands, 6% of the patients do not reach CE-IM after endoscopic resection and ablation [9]. In less experienced centers, this rate reaches 25%–44% [34-36]. First, this underlines the paramount importance of expert centers in the management of early Barrett’s neoplasia. The latest ESGE position statement, suggesting that all cases of dysplasia should be handled in expert centers should help improving this point [3]. Second, performing ablation in a patient with peptic esophagitis or poor healing from the last ablation is doomed to fail, and should be avoided: instead, increasing acid suppression therapy, postponing the ablative procedure, and in some instances performing antireflux surgery based on 24 h ambulatory pH-impedance measurement is advisable. Finally, although ablation spares the patient the morbidity of many endoscopic resection procedures, “escape resection” should be used when ablation fails after repeated procedures. Indeed, the increased risk of neoplastic progression of the patients with poor squamous regeneration after ablation should be kept in mind [37].

Follow-Up of Barrett’s Esophagus

The follow-up of BE appears in Table 1 and will be addressed in a specific chapter of the issue.

Follow-Up after Treatment of Early Barrett’s Neoplasia

The goal of the treatment of early Barrett’s neoplasia is to prevent the occurrence of a T ≥ 2 adenocarcinoma requiring surgery or an advanced adenocarcinoma with fatal outcome. Reaching CE-IM was hoped to be a definitive treatment of BE; however, IM and dysplasia do recur in 2%–4% and 1%–2% per year, respectively [9, 30]. Advanced adenocarcinomas are also observed in 0.4%–0.7% of the patients following initial CE-IM after 3–5 years follow-up. Most dysplastic recurrences are diagnosed in random biopsies of the gastric cardia [9, 38]. In addition, dysplastic recurrences are observed up to 4 years after CE-IM [39].

Current endoscopic surveillance protocol following CE-IM includes a careful endoscopic examination of the neosquamous epithelium and gastric cardia in direct and retroflexed position, and random quadrantic biopsies of the gastric cardia and of the neosquamous epithelium every 1–2 cm to search for buried glands. The surveillance intervals are 3, 6, 12 months, and annually thereafter in case of initial HGD or adenocarcinoma; 1 and 3 years, and every 3 years thereafter in case of initial LGD [1]. Considering the poor diagnostic yield of performing random biopsies of the neosquamous epithelium (1% buried IM with no dysplasia and no neoplastic progression observed in the Dutch registry), these biopsies could be abandoned in the future. Furthermore, considering the median 25–31 months’ time to diagnose recurrent dysplasia, surveillance intervals during the first year following CE-IM might be broadened [9].

Common Mistakes on Follow-Up

Omitting Retroflexion to Examine the Gastric Cardia

While the interest of random biopsies of the gastric cardia is currently debated, a careful inspection of the gastric cardia, in direct and retroflexed position, is paramount to detect neoplastic recurrences that typically occur at this site [40].

Over Interpreting Residual or Recurrent Intestinal Metaplasia at the Gastric Cardia

IM of the gastric cardia is found in up to 20% of patients undergoing upper digestive endoscopy and does not justify surveillance [41]. Following CE-IM for early Barrett’s neoplasia, IM of the gastric cardia is found in 14%–21% of the patients (Fig. 1), however, reproduced in subsequent endoscopies in only a third of the cases [9, 38]. This casts doubt on the clinical relevance of this finding, and should not lead to the diagnosis of recurrent BE or justify therapy in the absence of dysplasia.

The principles of the management of early Barrett’s neoplasia, consisting in a thorough endoscopic assessment, followed by the resection of all visible abnormalities, and the eradication of the residual BE has not changed much for the last decade. However, the endoscopic resection toolbox has incorporated ESD, which might become, as in every other organ of the digestive tract, the treatment of choice of early carcinoma. The long-term follow-up data after CE-IM confirms the durable and excellent results achieved in expert centers, underlining the importance of centralized care for the management of BE; while questioning the clinical and oncological relevance of recurrent IM at the gastric cardia, these data still prompt for prolonged endoscopic surveillance after BE eradication therapy.

The author has no conflicts of interest to declare.

There is no funding source for this work.

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