Endoscopic submucosal dissection for esophageal cancer: an overview of current indications and challenges to adoption in the United States

Introduction

Endoscopic submucosal dissection (ESD) has emerged as a groundbreaking technique in the management of early-stage esophageal cancer, providing a minimally invasive alternative to traditional surgical approaches like esophagectomy. Developed in Japan in the late 1990s, ESD represented a significant advancement over existing techniques such as endoscopic mucosal resection (EMR), which often led to piecemeal resection and higher rates of local recurrence (1). ESD was driven by the need for more precise and complete removal of early-stage gastrointestinal tumors, particularly in East Asia, where the incidence of gastric and esophageal cancers is notably high (2). ESD’s ability to achieve en bloc resection of the entire lesion is crucial for accurate histopathological assessment and significantly reduces the risk of recurrence, positioning it as a superior method compared to conventional EMR (2).

The technique’s adoption outside of Japan, particularly in Western countries, has been slower due to several factors. These include the steep learning curve associated with the procedure, the technical challenges posed by the esophagus’s unique anatomy, and differences in cancer epidemiology between Eastern and Western populations (3). Western endoscopists often face significant barriers to mastering this technique, including limited access to hands-on training and mentorship from experienced practitioners (4).

Furthermore, the anatomical characteristics of the esophagus, such as its narrow lumen, thin muscle layer, and proximity to critical structures like the aorta and trachea, present unique challenges during ESD. The lack of a serosal layer also increases the risk of perforation, making the procedure technically demanding and requiring a high level of precision (5). These challenges are compounded by the need to control physiological movements caused by respiration and cardiac pulsations, which can further complicate the procedure.

Despite these hurdles, ESD has been increasingly recognized for its potential to achieve curative outcomes in early-stage esophageal cancer (6). The procedure’s ability to achieve high en bloc resection rates, along with its potential to minimize the need for more invasive surgical interventions, underscores its importance in the evolving landscape of esophageal cancer treatment. However, the successful implementation of ESD in Western clinical practice will require ongoing efforts to overcome these technical challenges and improve training opportunities for endoscopists. In this review, we aim to comprehensively review the current indications and practice of ESD and barriers to further adoption of the procedure especially in the United States (US).

Epidemiology of esophageal cancer

Esophageal cancer is a major global health burden, ranking as the seventh leading cause of cancer-related mortality worldwide, with significant variations in incidence and histological subtypes across different regions (7,8). The two main histological types of esophageal cancer are squamous cell carcinoma (SCC) and adenocarcinoma, each with distinct epidemiological patterns that influence the application and outcomes of treatment modalities like ESD.

Global incidence and histological distribution

In Eastern Asia, particularly in China and Japan, esophageal SCC is the predominant histological subtype, accounting for approximately 90% of all esophageal cancers (9). In 2020, the estimated age-standardized incidence rate (ASIR) in China was 13.8/100,000 and 7.2/100,000 in Japan (10). Also, Asia accounts for 74.9% of the incidence and 74.0% of the mortality of esophageal cancer worldwide (11). The high prevalence of SCC in these populations has driven the widespread adoption of ESD, which has been particularly effective in treating early-stage SCC. Studies from Japan have demonstrated en bloc resection rates of 94.9% and curative resection rates of 88.3% for esophageal SCC treated with ESD, with local recurrence rates as low as 1.7% (12).

In contrast, Western countries have a higher incidence of esophageal adenocarcinoma (EAC), which is closely associated with Barrett’s esophagus. This condition, characterized by the metaplasia of the normal squamous epithelium to columnar epithelium in the distal esophagus, significantly increases the risk of developing adenocarcinoma (13). The prevalence of Barrett’s esophagus varies based on the study population and design, but a recent study estimated the burden of a screen-eligible population for Barrett’s esophagus ranges from 19.7 million to 120.1 million, representing 8.4% to 51.5% of noninstitutionalized-US-adult population (14). Given this epidemiological context, the application of ESD in Western countries has largely focused on the resection of dysplastic lesions and early adenocarcinoma associated with Barrett’s esophagus (15).

Diagnosis of esophageal cancer and Indications for ESD

Diagnosis of esophageal cancer requires histopathological confirmation through EGD with biopsy. Assessment of tumor sublocation and local extent, presence, and extent of Barrett’s esophagus through endoscopy also assist in the diagnosis (16). Endoscopic ultrasound (EUS) is the preferred method for assessing locoregional staging and for guiding treatment plans, with a sensitivity of 80%, especially in patients without distant metastases, and also outperforms fluorodeoxyglucose-positron emission tomography (FDG-PET) scan in the detection of locoregional spread or primary tumor and regional lymph node metastasis (17,18). A computed tomography (CT) scan or FDG-PET scan should also be conducted to evaluate the presence of distant metastases and assist in determining the staging and appropriate treatment strategy and also a more specific in diagnosis of lymph node metastases compared to EUS (16,19).

When the diagnosis of esophageal cancer is confirmed with the absence of distant metastases, locoregional treatment modalities are considered. A meta-analysis of 15 nonrandomized studies demonstrated that ESD had a better en bloc and curative resection rate and local recurrence compared with EMR for esophageal, gastric, and colorectal neoplasms (20). ESD is a minimally invasive procedure that would benefit older adults or those with multiple comorbidities. A recent retrospective cohort study reported a 5-year overall and disease-survival rate of 78.0% and 98.0% respectively in older adults same or above 65 years of age who received ESD for esophageal squamous cell carcinoma with age and performance status being poor prognostic factors (21). Given its superiority in achieving en bloc and curative resection compared to EMR, along with its minimally invasive nature, ESD is indicated for early-stage dysplasia or cancer that would benefit from thorough tumor staging and curative resection. The indications for ESD based on the international society guidelines (22-25) are summarized in Table 1.

Absolute indications for ESD

Early Barrett’s cancer limited to the mucosa (i.e., T1m1-m3) or visible Barrett’s lesions with high-grade dysplasia (HGD) or suspicious dysplasia or cancer

Given the minimal risk of lymph node metastasis (<2%) associated with this condition, Barrett’s lesion with or high-suspicion of HGD or Barrett’s cancer is an absolute indication for ESD that allows curative resection and accurate pathologic staging (26).

SCC limited to epithelial (m1)/lamina propria mucosae (m2)

Given the minimal risk of lymph node metastasis associated with m1/m2 lesions, endoscopic resection (ER) is curative in this case, making early-stage SCC or esophageal squamous dysplasia an absolute indication for ESD (27,28). However, with invasion into muscularis mucosa (m3) or submucosa (sm1), the risk of lymph node ranges between 5–15% (26). Squamous cancer has a higher lymph node metastatic rate than its Barrett’s counterpart and this is reflected in a tighter cutoff value for superficial submucosal invasion in the former (200 µm for squamous sm vs. 500 µm for Barrett’s sm) (26).

Relative indications for ESD

Clinical T1a-mm/T1b-sm1 (invading submucosa ≤200 µm) squamous cancer non-circumferential lesion, without any other histologic risk factors for lymph node metastasis (i.e., good to moderate differentiation, no presence of lymphovascular invasion, and radical vertical resection margin).

Clinical T1b-sm1, submucosal (invasion ≤500 µm) Barrett’s cancer, without any other histologic risk factors for lymph node metastasis (i.e., good to moderate differentiation, no presence of lymphovascular invasion, absence of tumor budding, and radical resection).

Given a much lower risk of lymph node metastasis than previously assumed (0–2%), endoscopic therapy followed by strict endoscopic follow-up is now considered a valid relative indication for the above conditions (26).

For muscularis mucosae or submucosa 1 (m3/sm1) cancer lesions, ER is weakly recommended as initial treatment as the preoperative diagnosis of cancer invasion depth for m3/sm1 cancer using other diagnostic tests such as magnifying narrow band-imaging (NBI) and EUS is not accurate enough. This makes a diagnostic rather than a therapeutic ESD the initial management step for clinical m3/sm1 cancer.

In esophageal cancer with a larger lateral extent, the effectiveness of ESD must be balanced with an increased risk of postoperative esophageal stricture with extensive esophageal ER. These strictures not only affect the quality of life negatively but also delay chemoradiotherapy. A long diameter of the same or more than 50 mm is considered a risk for post-operative stenosis (29). The risk for postoperative esophageal stricture can be as high as 70% in semi-circumferential lesions and 100% in whole circumferential lesions, without any prophylaxis (30). The risk is significantly reduced in non-circumferential lesions combined with prophylaxis, therefore making ESD a suitable intervention for non-circumferential lesions (30).

Procedural techniques

ESD is performed in a step-by-step process, with various tools available to aid the endoscopist in resecting a mucosal neoplastic lesion through the following steps: (I) peripheral marking of the lesion with cautery; (II) a lifting agent is injected into the submucosa around the lesion; (III) the mucosa is incised and circumferentially cut around the lesion using an electrosurgical knife; (IV) the submucosa beneath the lesion is injected and dissected with an electrosurgical knife until the specimen is fully removed (31). Any bleeding during the mucosal incision or submucosal dissection is controlled using a water jet for washing and hemostatic forceps or an electrosurgical knife for coagulation of the vessels (31). One option is to use a traction device with a clip and thread during ESD for superficial esophageal squamous cell carcinoma, as it significantly shortens the procedure time without increasing risk (25,32).

Tunneling ESD, also called endoscopic submucosal tunnel dissection (ESTD), is a technique recommended for esophageal lesions involving more than two-thirds of the esophageal circumference (33). It is a technique that creates a submucosal tunnel between the mucosa and muscularis propria layer to dissect the esophageal superficial neoplasms and is a safe and effective way to dissect large lesions (34). A recent multicenter trial showed that tunneling ESD resulted in shorter procedure time, especially for lesions more than half of the circumference of the esophagus, and had less frequent muscular injury and improved healing of the mucosal defect compared to the conventional method (35).

Several cases of endoscopic full-thickness resection (EFTR) for a submucosal tumor in the esophagus have been reported (36,37) EFTR originates from techniques used by ESD and can be performed either by exposed EFTR and nontunneled exposed EFTR (38). Tunneled exposed EFTR, or submucosal tunnel endoscopic resection (STER), is a method that includes dissection through the muscularis propria circumferentially around the lesion. It is feasible for submucosal tumors same or less than 4 cm in diameter and enables access to the distal esophagus and gastric cardia (39). It was able to achieve en bloc resection in 90.6% of 124 esophageal cases, 43 esophagogastric junction cases, and 13 cases in the stomach and the patients were free from local recurrence or distant metastasis during the study period of a median of 36 months (15). Due to its invasiveness, it also accompanies the risk of gas dissection causing pneumothorax, pneumomediastinum, subcutaneous emphysema, or pneumoperitoneum although the majority resolves with conservative management (15). Since EFTR is a variation of ESD or peroral endoscopic myotomy (POEM), we anticipate that the procedure is not particularly challenging regarding technique for endoscopists who are already proficient in ESD or POEM (30). We anticipate that this technique would enable local complete resection for even T1b or T2 malignancy, further expanding the implication of ESD (30).

Technical challenges of ESD

ESD is a procedure that is technically challenging and requires extensive training. It is more complex for esophageal cancer due to the narrow lumen of the esophagus making it difficult to use gravity traction, has a thin muscular layer and no serous membrane, is located in the posterior mediastinum and is compressed by the aorta, vertebral body, and trachea, and is easily affected by heartbeat, respiratory movement, and contraction of the internal ring muscle (30). Most Western gastroenterologists and surgeons are not familiar with the skills and equipment required for ESD, and it takes a significant amount of time and practice to perform it confidently and independently (4). A study from a high-volume referral center in the US showed that proficiency benchmarks of en bloc resection >90%, R0 resection >80%, and resection speed >9 cm²/h were achieved after around 250 cases, which is a prominent number compared to the suggested 30–40 ESDs based on high-volume Japanese centers (4,40,41). Several reasons contribute to this longer learning curve in Western society, such as less prevalent gastric lesions which are thought to be technically easier cases of ESD to start with, limited tutoring or supervision from an expert, and a higher proportion of previously manipulated lesions (3,4,42). An alternative to the limited cases of gastric cancer in Western society could be rectal lesions, as rectal cancer is more prevalent in the West, and as there has been a significant increasing trend in minimally invasive surgery and ESD, with a recent study demonstrating ESD had lesser adverse events and shorter hospital stay in early rectal cancer compared to transanal endoscopic microsurgery (43,44). Furthermore, adenocarcinoma lesions more prevalent in Western countries tend to be larger and more difficult to resect en bloc, and Western patients often present with more advanced disease at diagnosis, which complicates the use of ESD as a first-line treatment (45).

In addition, ESD is a time-consuming procedure. In a study on 201 early esophageal cancer cases in China, the median procedure time was 66.9 min [interquartile range (IQR), 10–190 min], with a median of 112 min (IQR, 10.0–190.0 min) when the tumor size was the same or more than 4.0 cm performed by endoscopists with more than 15 years of experience (46). The mean procedural time was longer in a study based on 16 French endoscopy centers with a mean time of 117.3 (median: 105) min with a statistically significant difference based on the size of the lesion (mean: 92.7 min in lesions <20 mm vs. mean: 124.6 min in lesions >20 mm) (47). In a meta-analysis of 776 ESD-treated lesions on esophageal dysplasia or esophageal squamous cell carcinoma, demonstrated a median of the mean operation time of 90.9 min (range, 49.7–180 min) (48). Whereas ESD for BE with HGD and early EAC demonstrated a median duration of 88 min, ranging from 34 to 358 min (49). ESD has a longer operation time, typically 3–4 times longer, compared to EMR for superficial esophageal carcinoma, regardless of the tumor type and in all tumor sizes (less than 10, 10–20, and more than 20 mm) (26,50).

Complications of ESD

Major complications of ESD are bleeding, intraoperative perforation, and stenosis. Perforation and perforation-related disorders were observed in 3.3% out of the 12,899 esophageal ESD procedures in Japan. A subsequent meta-analysis of 15 studies on ESD for esophageal neoplasia demonstrated pooled estimates of bleeding and perforation as 2.1% and 5.0% respectively, with one case of perforation requiring urgent operation (48). The pooled estimate of stenosis was 11.6% and there was no case of mortality, either directly or indirectly related to ESD, reported in any of the studies (48).

Post-ESD bleeding after esophageal ESD is considered rare, especially in comparison to gastric ESD (51,52). Pharmacological measures to reduce post-procedural bleeding have been investigated including proton pump inhibitors (PPIs) and vonoprazan, a potassium-competitive acid blocker. Vonoprazan has shown better efficacy compared to PPI in multiple studies regarding post-procedure bleeding and ulcer shrinkage rate for post-ESD ulcers (53,54).

A recent retrospective cohort study suggested that there was no significant difference between the no acid suppression or PPI or vonoprazan group in regards to delayed bleeding after ESD (55). The discussion on PPI and vonoprazan to prevent post-ESD bleeding remains an area of debate with further studies needed. The reported incidence of strictures following esophageal ESD is 0.7% for lesions covering less than half of the circumference, 27.6% for those covering more than half, and 94.1% for lesions covering more than three-quarters (56). Circumferential extension and depth of invasion exceeding lamina propria of esophageal mucosa have been reported to be associated with esophageal strictures, especially when the resection major axis length was more than 50 mm (29,56,57). Stenosis prophylaxis using steroid injection or oral steroid therapy has been studied. Oral prednisolone started at 30 mg daily and tapered for a total of 3-week duration showed that the stricture rate after esophageal ESD was significantly lower in the oral prednisolone group than in the ESD alone group (17.6% vs. 68.7%) and a more significant reduction in endoscopic balloon dilatation (EBD) sessions (median: 4.6 vs. 8.1) (58). An alternative method for steroid injection is triamcinolone injection immediately after ESD with or without a subsequent oral steroid regimen (59). It remains controversial in the superiority of the steroid administration route especially due to the systemic adverse effects of oral steroids accompanied with long-term administration (60). A clinical trial in Japan (JCOG 1217) is currently investigating the outcomes including stricture-free survival of submucosal triamcinolone injections vs. oral prednisolone treatment in preventing post-ESD esophageal stenosis (61).

Perforation in esophageal ESD is reported in 1.5–5.0% of esophageal ESD cases and may lead to mediastinal emphysema and/or mediastinitis (33,62). To avoid intraoperative perforation, it is essential to obtain a good visual field, and using a traction method such as the clip-with-line, S-O clip method, or modified external forceps method can be utilized (63-65). Most periprocedural perforations are closed with clips but can be treated with endoscopic suturing, stent placement, over-the-scope (OTS) clip, clipping, or endoscopic vacuum therapy when the perforation is larger (33,66). Delayed perforation is extremely rare but more serious, and can occur due to tissue necrosis and degeneration caused by heat damage in the deeper layers of the gastrointestinal wall, often resulting from excessive energy use during ESD (67). Only a few case reports are reported, including a case after resection of 4/5 of the esophageal circumference along a 12-cm segment of Barrett’s esophagus with multifocal HGD treated with two self-expandable metal stents (67,68).

Barriers to ESD in the US

Despite the superiority in en bloc resection rate and local recurrence rate over EMR in early esophageal cancer, the adoption of ESD in the US has been slow and mostly limited to tertiary centers (69). The technical complexity, prolonged procedural time, and limited training opportunities are all contributing factors. In addition, one of the major barriers to performing ESD in the US is the lack of financial reimbursement (69-71). The current Medicare physician payment is determined by decisions from the Centers for Medicare & Medicaid Services based on the relative value units (RVU) associated with the individual Current Procedural Terminology (CPT) code based on the work RVU, practice expense RVU, and malpractice RVU (72). As of now, there is no unique CPT code for ESD and physicians bill an unlisted procedure code (i.e., unlisted procedure, esophagus) (73). Listed CPT codes for endoscopic procedures for the esophagus are POEM or esophagoscopy with EMR, and EGD with EMR (73). Without a unique CPT code, the provider must require approval and authorization from the insurance carrier by submitting documentation of the need for an ESD and alternatives. Based on an analysis of two advanced endoscopists who performed ESD-related procedures in their private practice, the unlisted CPT code was initially denied in 35% of the cases, and 8.33% of the cases were ultimately denied and unpaid (70). ESD is a cost-effective procedure, with a cost-effectiveness analysis demonstrating that at a 50% chance or higher, ESD was a more cost-effective option than piecemeal EMR at willingness-to-pay values of ≥3,795–4,744 USD for avoiding recurrence and ≥90,143–99,631 USD for avoiding surgery (74). Curative endoscopic resection with ESD should be the preferred alternative to surgery for T1 esophageal cancer.

Conclusions

ESD is beneficial in that it allows minimally invasive resection of the malignancy while having a high en bloc resection rate and low local recurrence rate. We anticipate that the indications will be broadened for more advanced lesions such as T1b or T2 cancer with advancements in techniques such as a modified ESD, or EFTR and devices. However, despite these advancements, ESD remains a challenging procedure with limited opportunities for training especially in Western countries. The primary obstacles to broader implementation include insufficient coding and reimbursement relative to the cost, the lengthy procedural time, the technical complexity, and the specific techniques required for additional interventions depending on the location, number, size, and depth of the esophageal malignancy.

Acknowledgments

Funding: None.

Footnote

Peer Review File: Available at https://aoe.amegroups.com/article/view/10.21037/aoe-24-24/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://aoe.amegroups.com/article/view/10.21037/aoe-24-24/coif). R.E.K. is a consultant for Cook Medical and Apollo Endosurgery of Boston Scientific. The other authors have no 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.

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