AGA Institute Clinical Practice Update: Endoscopic Submucosal Dissection in the United States

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Clinical Practice of Endoscopic Submucosal Dissection in the United States Peter V. Draganov,* Andrew Y. Wang,‡ Mohamed O. Othman,§ and Norio Fukamik *Division of Gastroenterology, Hepatology and Nutrition, University of Florida, Gainesville, Florida; ‡Division of Gastroenterology and Hepatology, University of Virginia, Charlottesville, Virginia; §Section of Gastroenterology and Hepatology, Baylor College of Medicine, Houston, Texas; kDivision of Gastroenterology and Hepatology, Mayo Clinic Arizona, Scottsdale, Arizona Endoscopic submucosal dissection (ESD) is an established endoscopic resection method in Asian countries, which is increasingly practiced in Europe and by early adopters in the United States for removal of early cancers and large lesions from the luminal gastrointestinal tract. The intent of this expert review is to provide an update regarding the clinical practice of ESD with a particular focus on its use in the United States. This review is framed around the 16 best practice advice points agreed upon by the authors, which reflect landmark and recent published articles in this field. This expert review also reflects our experience as advanced endoscopists with extensive experience in performing and teaching others to perform ESD in the United States. Best Practice Advice 1: Endoscopic submucosal dissection should be recognized as a mature endoscopic technique that enables complete removal of lesions that are too large for en bloc endoscopic mucosal resection or are at increased risk of containing cancer. Best Practice Advice 2: The safety and feasibility of endoscopic submucosal dissection for early gastric cancer is well established. The absolute indications for curative endoscopic resection include moderately and welldifferentiated, nonulcerated, mucosal lesions that are £2 cm in size. Best Practice Advice 3: Other relative (expanded) indications for gastric endoscopic submucosal dissection include moderately and well-differentiated superficial cancers that are >2 cm, lesions £3 cm with ulceration or that contain early submucosal invasion, and poorly differentiated superficial cancers £2 cm in size. The risk of lymph node metastasis when endoscopic submucosal dissection is performed for these indications is higher than when it is performed for absolute indications but remains acceptably low. Best Practice Advice 4: Endoscopic submucosal dissection may be considered in selected patients with Barrett’s esophagus with the following features: large or bulky area of nodularity, lesions with a high likelihood of superficial submucosal invasion, recurrent dysplasia, endoscopic mucosal resection specimen showing invasive carcinoma

with positive margins, equivocal preprocedural histology, and intramucosal carcinoma. Best Practice Advice 5: Endoscopic submucosal dissection is the primary modality for treatment of squamous cell dysplasia and cancer confined to the superficial esophageal mucosa. Any degree of submucosal invasion caries an increased risk of lymph node metastasis and alternative/ additional therapy should be considered. Best Practice Advice 6: Duodenal endoscopic submucosal dissection is associated with an increased risk of intraprocedural perforation and delayed adverse events. Duodenal endoscopic submucosal dissection should be limited to endoscopists with extensive experience in performing endoscopic submucosal dissection in other locations. It is strongly suggested that endoscopists in the United States refrain from performing duodenal endoscopic submucosal dissection during the early phase of their endoscopic submucosal dissection practice. Best Practice Advice 7: All colorectal lesions should be evaluated for suitability for endoscopic resection. Accumulating evidence has shown that the majority of colorectal neoplasms without signs of deep submucosal invasion or advanced cancer can be treated by advanced endoscopic resection techniques. Best Practice Advice 8: Colorectal neoplasms containing dysplasia confined to the mucosa have no risk for lymph node metastasis and endoscopic resection should be considered as the criterion standard. Best Practice Advice 9: Large (>2 cm) colorectal lesions frequently (>43%) require piecemeal removal when endoscopic mucosal resection is used, which is associated with increased (up to 20%) rates of recurrent neoplasia. Endoscopic submucosal dissection enables higher rates of en bloc resection and lower recurrence rates for these lesions. Patients with large complex colorectal polyps should be referred to a high-volume, specialized center for endoscopic removal by endoscopic mucosal resection or endoscopic submucosal dissection. Best Practice Advice 10: Endoscopic resection for colorectal lesions offers significant cost benefit compared with surgery, and case-based endoscopic submucosal

Abbreviations used in this paper: BE, Barrett’s esophagus; EGC, early gastric cancer; EMR, endoscopic mucosal resection; ER, endoscopic resection; ESD, endoscopic submucosal dissection; GI, gastrointestinal; JGCA, Japanese Gastric Cancer Association; LNM, lymph node metastasis; NCCN, National Comprehensive Cancer Network; R0, marginnegative (resection); SCC, squamous cell carcinoma.

© 2018 by the AGA Institute 1542-3565/$36.00 https://doi.org/10.1016/j.cgh.2018.07.041

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dissection selection for high-risk lesions could offer cost savings. Best Practice Advice 11: Endoscopists in the United States embarking on performing endoscopic submucosal dissection should be familiar with currently available endoscopic tissue closure devices. Both clip closure and endoscopic suturing techniques have been shown to be effective in managing intraprocedural perforation. Complete closure of a post–endoscopic submucosal dissection site may be considered in certain circumstances based on patient factors, procedural factors, and the location of the lesion. Best Practice Advice 12: Careful coagulation of exposed blood vessels in the resection site may reduce the risk of delayed bleeding after endoscopic submucosal dissection. The use of low-voltage coagulation current is recommended for this technique. Best Practice Advice 13: Endoscopists should affix the endoscopic submucosal dissection specimen to a flat surface (eg, pin the specimen to cork board) and immerse it in formalin. An expert gastrointestinal pathologist should evaluate the specimen for margin involvement, degree of differentiation, presence or absence of lymphovascular invasion, depth of submucosal invasion (if present), and tumor budding. Best Practice Advice 14: Acquiring high-level competency in endoscopic submucosal dissection is achievable in the United States. Alternative educational models should be used in the United States because of the limited number of experts and the differing prevalence of gastrointestinal luminal diseases as compared with Asia. Best Practice Advice 15: The endoscopic submucosal dissection educational model most suited for the current US environment is a stepwise approach consisting of didactic self-study, attending training courses with increasing levels of complexity, self-practice on animal models, and observation of live cases performed by experts. Endoscopists should perform their initial endoscopic submucosal dissections on patients with lesions that have well-established indications for endoscopic submucosal dissection and are of the lowest technical complexity. Best Practice Advice 16: Endoscopists in the United States who perform endoluminal resection should educate referring physicians to avoid practices that may induce submucosal fibrosis hampering future endoscopic mucosal resection or endoscopic submucosal dissection. These practices include tattooing in close proximity to or beneath a lesion for marking and partial snare resection of a portion of a lesion for histopathology. Keywords: Endoscopic Submucosal Dissection; ESD; United States; Esophagus; Gastric; Colon; Rectum; Training; Clinical Practice; Cancer; Dysplasia; Training; Pathology.

ndoscopic resection (ER) is a well-established and minimally invasive treatment for premalignant and early malignant gastrointestinal (GI) lesions that can be highly effective when performed by experienced endoscopists for appropriate indications. ER has evolved over the years from snare polypectomy to endoscopic mucosal resection (EMR) and now to endoscopic

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submucosal dissection (ESD). For colorectal lesions without invasive cancer, ER now is considered first-line therapy. Careful endoscopic examination using highdefinition imaging enables the identification of superficial neoplasia or early luminal malignancies that when enhanced further by using dye-based or optical chromoendoscopy confers a high level of diagnostic accuracy. Standardized classifications based on lesion morphology and/or surface characteristics include the Paris classification,1,2 pit pattern using optical magnification,3 and various narrow-band imaging classifications.4,5 These validated methods are important and necessary components for evaluating luminal GI lesions to determine their suitability for endoscopic treatment and can help to plan the optimal resection strategy. Because all forms of EMR use a snare for ER, the size of a specimen that can be removed safely en bloc generally is limited to 1.5 to 2 cm. Larger lesions then must be removed in a piecemeal fashion. This size limitation of EMR for en bloc, margin-negative (R0) resection leads to an undesirable increased rate of residual or recurrent neoplasia.6,7 ESD is a natural extension of EMR that was developed to overcome these limitations. Developed in the mid-to-late 1990s, ESD is an innovative but technically demanding technique that offers an impressive capability to resect large and irregular tumors with a high en bloc, R0, resection rate. Over the years, the steps of ESD have been refined with the development of various injectable lifting solutions, adaptive electrosurgical generators, and dedicated endoscopic resection tools (knives and scissors). As a result, ESD has become the standard method for ER of larger superficial lesions in the luminal GI tract in Japan and in nearby Asian countries. Despite its obvious benefits, the adoption of ESD in Western countries has been slow. Several major reasons for this delay are highlighted in Table 1. However, over the past decade, experience with ESD has accumulated in the West, beginning in Europe and then spreading to the United States, mainly at tertiary referral centers, and safety and efficacy data have been published from centers outside of Asia.8–13 A comparable armamentarium of ESD devices and injectable solutions now are commercially available in the West and in the United States. Furthermore, refinements in ESD technique, such as use of the tunnel method, pocket method, and devices for traction,14–16 now are being used to enable more effective, faster, and safer ESD. With low thresholds for performing endoscopy for upper GI symptoms and the promotion of screening colonoscopy for colon cancer prevention, more precancerous lesions and early cancers are being detected that may be amenable to ER by ESD. The intent of this clinical update is to review the current practice of ESD, with particular focus on the emerging role and integration of ESD in the United States.

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Table 1. Factors Impeding ESD Training in the United States Underestimating the need and benefit from ESD Reluctance to accept the need and benefit from ESD in the United States where gastric cancer is relatively uncommon Bias of medical and surgical oncologists toward surgical resection Established patient-referral patterns among endoscopists geared toward sending patients with more complex superficial luminal lesions to surgery Bias of advanced endoscopist toward EMR Procedure-related factors Steep learning curve for ESD ESD requires a higher level of expertise to endoscopically evaluate and select appropriate lesions Requires in-depth understanding of electrosurgical principals Time-consuming procedure Higher rate of adverse events compared with EMR Slow release of ESD tools in the United States Scarcity of scopes with optical magnification Limited options for chromoendoscopy in the United States Lack of proper reimbursement Training-related factors Lack of ESD experts Lack of ESD training canters Lack of easier-to-remove gastric lesions to gain experience early in the learning curve Western pathologists are unaccustomed to evaluating ESD specimens Reprinted with permission and adapted from Wang and Draganov.68

Gastric Endoscopic Submucosal Dissection Early gastric cancer (EGC) is a well-established indication for ESD, including for patients in the United States and the West.13 In fact, the role of ESD for treating patients with selected superficial gastric cancer is discussed in a US National Comprehensive Cancer Network (NCCN) guideline on gastric cancer.17 The low risk of lymph node metastasis (LNM) coupled with a high survival rate has made EGC an optimal indication for this technique.18 According to the Japanese Gastric Cancer Association (JGCA), differentiated adenocarcinomas that are limited to the mucosa (T1a), have a size of 2 cm or smaller, and are without ulceration possess an extremely low risk of LNM and comprise the standard (absolute) indication for gastric ESD.19 In 2000, Gotoda et al20 published a landmark study that included 5265 patients who underwent gastrectomy with lymph node dissection for EGC. These investigators were able to characterize certain groups of EGCs that fell outside the absolute criteria but also were associated with a negligible risk of LNM, making them suitable expanded targets for ESD (Table 2).20 Similar results have been reported in subsequent studies,21–23 which informed the development of the JGCA’s gastric cancer treatment guidelines.19 In a recent meta-analysis of 9798 patients, the incidence of LNM was 0.2% for those who met the absolute criteria of JGCA guidelines compared with 0.7% for

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patients who met the expanded criteria. On careful examination of the 4 categories of the expanded criteria, undifferentiated mucosal lesions and submucosal lesions had a significantly higher incidence of LNM (2.6% and 2.5%, respectively) compared with absolute-criteria lesions.24 As such, the use of ESD for these more concerning expanded-criteria subcategories should be balanced with the risk of performing surgical resection given the increased risk of LNM. It is worth noting that the risk of LNM in Western populations may be different than in Asian populations, and there are limited data regarding the incidence of LNM in the United States. Pokala et al25 reported on the incidence and predictors of LNM for early stage (T1) gastric adenocarcinomas in the United States from a cohort of 1577 patients derived from the Surveillance, Epidemiology and End Results database. The rates of LNM for well-differentiated or moderately differentiated (low grade, G1, and G2) T1a adenocarcinomas were 1.7% for tumors smaller than 2 cm and less than 4.5% for tumors smaller than 4 cm, but 20% for tumors 4 cm or larger in size. However, rates of LNM for low-grade T1b adenocarcinomas began at 8.4% for tumors smaller than 1 cm and increased dramatically in conjunction with increasing size.25 In the United States, ESD should be considered firstline therapy for visible, endoscopically resectable, superficial gastric neoplasia (Supplementary Video 1, Supplementary Figure 1). Indistinct lesion margins, the relative thickness of the gastric wall compared with other luminal organs, and the precision enabled by ESD make it superior to EMR for resecting lesions larger than 1 cm in size.26

Esophageal Endoscopic Submucosal Dissection Barrett’s Esophagus Current guidelines support ER of visible abnormalities arising from Barrett’s esophagus (BE).27,28 Both EMR and ESD can be applied, but EMR is considered the first-line therapy for BE.27,28 Although extensive data have accumulated regarding the safety and feasibility of ESD for BE including a recent meta-analysis,9,10,29,30 high-quality studies comparing EMR directly with ESD are scarce. In a published randomized controlled study, Q9 in a small group of patients (n ¼ 40) with high-grade dysplasia or early adenocarcinoma and lesion size of 3 cm or smaller, ESD provided higher R0 and curative resection rates.31 Over short-term follow-up evaluation (3 mo) there was no difference in complete remission. However, the outcomes of long-term recurrence or recurrence-free survival were not evaluated by the investigators because of the need for very large patient numbers to address these outcome measures.31 In BE, an ER is considered curative if the lateral and deep resection margins are negative, combined with

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Table 2. Suggested Indications for ESD in the United States Organ Esophagus Squamous cell carcinoma

Barrett’s esophagus

Stomach

Colon and rectum

Indications for ESD HGD to well (G1) to moderately (G2) differentiated Paris 0–II lesions Absolute indications: m1–m2 involvement with two thirds or less of the esophageal circumference Expanded indications: m3 or sm <200 mm involvement, any size, clinically N0 HGD to moderately (G1 or G2) differentiated T1a (m1–m3) lesions 15 mm (not amenable to en bloc resection by EMR) Patients with Barrett’s esophagus and the following features: Large or bulky area of nodularity Equivocal preprocedure histology Intramucosal carcinoma Suspected superficial submucosal invasion Recurrent dysplasia EMR specimen showing invasive carcinoma with positive margins Absolute indications: Mucosal adenocarcinoma (and lesions with HGD), intestinal type, G1 or G2 differentiation, size 2 cm, no ulceration Expanded indications: Adenocarcinoma, intestinal type, G1 or G2 differentiation, any size, without ulceration Adenocarcinoma, intestinal type, G1 or G2 differentiation, sm-invasive (<500 mm) Adenocarcinoma, intestinal type, G1 or G2 differentiation, 3 cm, with ulceration Adenocarcinoma, diffuse type, G3 or G4 differentiation, size 2 cm, without ulceration En bloc resection for lesions at risk for submucosally invasive cancer: Type V Kudo pit pattern Depressed component (Paris 0–IIc) Complex morphology (0–Is or 0–IIaþIs) Rectosigmoid location Nongranular LST (adenomas), 20 mm in size Granular LST (adenomas), 30 mm in size Residual or recurrent colorectal adenomas

References 28,69–72

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19,72,74

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HGD, high-grade dysplasia; LST, laterally spreading tumor. Reprinted with permission and adapted from Wang and Draganov.68

well-differentiated to moderately differentiated histology, no lymphovascular invasion, and no submucosal or only superficial (<500 mm) submucosal invasion.9,26,28,30 On the other hand, specimens with positive deep margins, those that infiltrate deep into the submucosa (>500 mm), or possess poorly differentiated histology or lymphovascular invasion, are at high-risk for LNM.27 Therefore, optimal lesion characterization and selection before endoscopic intervention is of utmost importance. Unfortunately, preprocedural evaluation with highdefinition white-light endoscopy, image-enhanced endoscopy, and targeted biopsies have limitations, and significant discrepancies between preresection and postresection histology have been observed repeatedly in 30% to 60% of cases.9,29,32 As compared with EMR, ESD allows for more accurate histopathologic evaluation33 and consequently can be considered in cases in which there is an increased possibility of an unrecognized invasive component (eg, large bulky lesions, intramucosal carcinoma on preprocedural biopsy, or equivocal preprocedural histology).28 Furthermore, EMR may not be technically feasible in some cases in which ESD can be applied (eg, for nonlifting or recurrent lesions).34 Finally, the

current guidelines recommend that if the EMR specimens show neoplasia at a deep margin, extant residual neoplasia should be assumed, and surgical, systemic, or additional endoscopic therapies should be considered.27 ESD seems to be the best-suited endoscopic modality to provide such additional therapy. Table 2 shows the suggested ESD indications for BE in the United States.

Squamous Cell Carcinoma of the Esophagus When compared with BE-related neoplasia, esophageal squamous cell carcinoma (SCC) has a higher propensity for LNM at earlier stages, and thus accurate histopathologic evaluation is of even greater importance. Therefore, the aim of ER in esophageal SCC always should be to provide en bloc removal with ESD as a firstline therapy28,34 because ESD has been shown repeatedly to be superior to EMR in providing higher en bloc, R0, curative resection with an associated lower rate of recurrence.35 European guidelines provide a useful framework for evaluating the curability of ER for esophageal SCC, and the need for additional therapy based on histopathologic findings (Table 2).28,34

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Duodenal Endoscopic Submucosal Dissection The role of ESD in the resection of superficial neoplasia in the duodenum is constrained because of high rates of complications.36 The duodenal wall is highly vascular, has a thin muscularis propria, and is exposed to gastric acid, bile, and pancreatic juice. As a result, duodenal ESD is associated with high rates of immediate and delayed bleeding, as well as perforation. Duodenal ESD should be limited to endoscopists with extensive experience in performing ESD.

Colorectal Endoscopic Submucosal Dissection Colonoscopy and ER of colorectal neoplasia have led to reductions in the incidence of and mortality from colorectal cancer.37 ER is effective therapy for large and complex premalignant polyps and is more cost effective than surgery.38–40 However, there is an increasing rate of surgery being performed for patients with nonmalignant colorectal polyps in the United States.41 It is important to realize that the colorectal mucosa does not possess lymphatic drainage.26 Accordingly, in situ or intramucosal colorectal cancer should be considered equivalent to high-grade dysplasia,42,43 because any dysplasia confined to the mucosa carries no risk for LNM.26 As a result, ER (EMR, or in some instances ESD) for dysplasia confined to the colorectal mucosa is the most appropriate first-line therapy and should be offered instead of surgery. The first attempt at ER was associated with the highest rate of success.44 Therefore, large, complex, superficial colorectal neoplasms should be referred to high-volume referral centers with expertise in ER. Attempting EMR to see if it might be possible without a high-level of confidence that complete ER is achievable should be avoided. It is debated as to which factors make some large colorectal lesions more suitable for ESD instead of piecemeal EMR. Nakajima et al45 found that for colorectal lesions 2 cm or larger in size, en bloc resection by EMR was impossible in more than 43% of cases. Piecemeal resection results in significantly higher rates of neoplastic recurrence compared with en bloc resection (10%–20% compared with 1%–2% by ESD; odds ratio, 8.2).7,12,40,46 By enabling en bloc resection of larger colorectal lesions, ESD offers high rates of curative resection, and the intact specimen produced by ESD allows for more accurate pathologic and oncologic assessment.7,12,40 In the case of selected early colorectal cancers (with <1000 mm of submucosal invasion and favorable histologic features), en bloc, R0 resection by ESD may obviate the need for additional surgery.

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In a Japanese multicenter study of colorectal polyps 2 cm and larger, 9.9% of lesions removed by ER were staged as T1, after excluding lesions with features of deeply invasive cancer.47 Of these T1 carcinomas, twothirds were confined to the superficial submucosa (<1000 mm) and potentially curable by ESD.47 In a large Australian study, ESD was modeled to be a costeffective modality if applied selectively for colorectal lesions with low-risk submucosally invasive (T1) cancer.48 The rationale for this being that ESD could lower overall cost by reducing the number of surgical resections and by potentially eliminating short-term surveillance, thereby reducing the total number of surveillance colonoscopies. US NCCN guidelines recommend that patients with colon or rectal polyps containing invasive cancer removed endoscopically with a “fragmented specimen or margin[s] [that] cannot be assessed” undergo additional surgical resection.42,43 Therefore, recognizing features that suggest a colorectal polyp might harbor invasive cancer is critical. Examination of data from the Australian Colonic Endoscopic Resection study found that for colorectal lesions 20 mm and larger, a type V Kudo pit pattern, depressed component (Paris 0–IIc), complex morphology (0–Is or 0–IIaþIs), rectosigmoid location, nongranular surface morphology, and increasing size were associated with submucosal invasive cancer, making these features important discriminators for lesions that might benefit from ESD over piecemeal EMR.49 The European Society of Gastrointestinal Endoscopy guideline states that ESD can be considered for removal of colorectal lesions with high suspicion of limited submucosal invasion, particularly for those greater than 20 mm, or those that otherwise cannot optimally and radically be removed by snare-based techniques.28 The Japan Gastroenterological Endoscopy Society guideline recommends colorectal ESD for lesions for which en bloc resection with snare-based EMR would be difficult, for mucosal tumors with submucosal fibrosis, for locally residual or recurrent early carcinomas after ER, and for sporadic lesions in conditions of chronic inflammation.50 In fact, an American Society for Gastrointestinal Endoscopy guideline on the role of endoscopy in inflammatory bowel disease advocated en bloc resection by EMR or ESD of raised, endoscopically visible, dysplastic lesions in regions of chronic active colitis that might be prone to fibrosis.51 Given the limited number of reports on the topic of ESD for inflammatory bowel disease–associated dysplasia,52 additional investigation into this practice would be valuable. It is important to emphasize that EMR by various modalities remains an effective means of providing curative resection for superficial colorectal neoplasia.53–55 High-quality EMR remains an essential skill for advanced ER and likely will be the procedure of choice for ER of noninvasive colorectal neoplasia in most

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settings in the United States. However, where regional expertise in colorectal ESD is available, ESD should be considered for complex lesions for which ER by snarebased methods (EMR) would be difficult, to provide en bloc resection for accurate pathologic assessment for lesions with risk factors for early submucosal invasion, and for residual or recurrent colorectal adenomas (Table 2, Supplementary Video 2).

After Endoscopic Submucosal Dissection Coagulation and Closure

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Careful inspection and coagulation of exposed nonbleeding visible vessels (with little or no overlying submucosa) in the post-ESD site has been recommended to prevent delayed bleeding in the upper GI tract,56 but the effectiveness of this method after large colorectal resections is equivocal.57,58 When using this technique, low-voltage (“soft”) coagulation current has been recommended58 to reduce the risk of perforation and the possibility of pain from postpolypectomy burn syndrome.57 Given the increased risk of bleeding and/or perforation during and after ESD, endoscopists should be familiar with the different closure devices and techniques available for post-ESD defect closure. Generally, standard endoclips are successful at closing most perforations that occur during ESD because, typically, these will be small.59,60 Adjunctive methods have been developed that enable endoclips to close large defects after EMR and ESD.61,62 In addition, over-the-scope clip systems potentially can close large luminal defects that approach 2 cm in size. Endoscopic suturing is another method to close a post-ESD resection bed or perforation. In a comparative study of 21 patients with iatrogenic colonic perforations (11 from ESD and 7 from EMR) closed with endoclips or an endoscopic suturing device, all 5 patients who underwent clip closure had worsening abdominal pain, and 4 of them required laparoscopic surgery. Only 2 of 16 patients in the endoscopic suturing group had worsening abdominal pain. However, this study was limited by its small number of patients.63

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Specialized Pathology Accurate histopathologic evaluation is the cornerstone of post-ER management. One of the main advantages of ESD over EMR is that en bloc resection facilitates accurate histopathologic evaluation. To avoid edge curling, the ESD specimen should be affixed to a flat surface (Figure 1, Supplementary Figure 1) using pins or needles, which has been shown to increase the ability of the pathologist to evaluate all important components including vertical and horizontal margin involvement, degree of differentiation, presence/absence of lymphovascular invasion, depth of submucosal invasion (if present), and tumor budding.28,33 The interobserver and intra-observer variability of pathologic evaluation of dysplastic lesions and early cancers throughout the GI tract has been documented repeatedly. Therefore, all ESD specimens should be evaluated by an expert GI pathologist, and evaluation by a second expert GI pathologist should be given strong consideration.

Endoscopic Submucosal Dissection Education and Practice in the United States In Japan, ESD is taught using the traditional master–apprentice model. The trainee is taken systematically through a path of cognitive training at case conferences, observing and assisting in ESD procedures, performing supervised ESD in patients commencing with smaller lesions in the distal stomach and gradually progressing to more difficult cases. Importantly, colorectal ESD usually is reserved for trainees who have extensive experience in gastric ESD. This model has proven to yield highly competent endoscopists, but, unfortunately, it is not applicable in the United States because of multiple limitations (Table 1). At present, there is no standardized approach for ESD training in the United States, although a commonly followed pathway has emerged.64 The usual starting point is to attend an ESD course or series of courses that provide increasingly more in-depth exposure. This is

Figure 1. Importance of post-ESD specimen management for accurate histopathologic assessment. (A) Placing EMR specimens in formalin without pinning the specimen results in curled edges and distortion of the muscularis mucosae. (B) ESD specimens should be affixed to a flat surface with pins before tissue fixation, which results in a proper specimen orientation with straight edges and a nondistorted muscularis mucosae layer.

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supplemented with self-study and self-guided practice on animal models. A visit to a high-volume center in Asia often is pursued and appears to be a valuable component of ESD training because it has been shown to enhance the learning curve.65 Because early gastric cancer is uncommon in the United States, suitable lesions on which to start performing ESD in patients typically are located in the rectum. It has been shown that colorectal ESD can be performed safely and effectively by an endoscopist with no previous experience with gastric ESD.66 Adequate lesion selection during the trainee’s early cases remains of paramount importance because the goal is to enhance the training experience further without increasing the risk or rate of adverse events. The European Society of Gastrointestinal Endoscopy guideline28 provides a useful framework for the indications for ESD in a Western setting.34 Most importantly, a guiding principle should be that our patients’ interests and welfare stand above all else, and that patients must not be used as an opportunity for practice or skills acquisition. A crucial component for the appropriate and responsible training and practice of ESD in the United States will be the development of benchmarks and quality metrics. Such benchmarks for en bloc, R0, and curative resection rates, along with acceptable rates of adverse events, have been developed in Asia, but may not be directly applicable in the United States. It is our experience that endoscopists offering ESD in the United States will be called upon (and will face significant pressure) to perform ESDs for indications that are well outside of what is endorsed by guidelines. This usually is driven by patients’ poor health status, which makes them poor candidates for other therapies, such as surgery. Nevertheless, endoscopists strongly should consider performing their initial ESDs on patients who are at least fair surgical candidates and have lesions with wellestablished indications that are of the lowest technical complexity.

Education of Referring Physicians The success of ESD is dependent on the degree of fibrosis. Fibrotic lesions have lower en bloc resection rates and higher bleeding and perforation rates.67 Endoscopists should refrain from practices that increase the risk of submucosal fibrosis. These practices include ink or tattoo injection for marking immediately under or close by a lesion, extensive biopsies, or partial snare polypectomy.

The Way Forward for Endoscopic Submucosal Dissection in the United States ESD is a mature endoscopic procedure developed in Japan that has spread to the West and now actively is

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practiced in the United States. Use of this innovative procedure has been included in NCCN guidelines for the treatment of superficial GI malignancies.17 As of 2016, there were more than 2500 publications related to ESD in PubMed.68 As of 2018, clinicians in the United States have access to a wide array of ESD devices. Because of its long and successful track record, the clinical use of ESD should not be confined to the realm of research protocols. However, endoscopists wishing to perform ESD will require specialized training and, similar to complex EMR, this procedure should be performed at referral centers with properly trained ancillary staff and surgical back-up. Although some insurers have begun preapproving and covering their members who might benefit from ESD, the hurdles preventing other patients from being covered for this innovative and potentially cost-saving procedure should be removed. The current significant interest and investment on the part of medical device companies, as well as by clinical investigators and practicing clinicians, suggests that the field and discipline of ESD is poised to make significant strides, particularly in the United States, in the years to come.

Supplementary Material Note: To access the supplementary material accompanying this article, visit the online version of Clinical Gastroenterology and Hepatology at www.cghjournal.org, and at https://doi.org/10.1016/j.cgh.2018.07.041.

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74. Gotoda T. Endoscopic resection of early gastric cancer. Gastric 1045 Cancer 2007;10:1–11. 1046 75. Sakamoto T, Mori G, Yamada M, et al. Endoscopic submucosal 1047 dissection for colorectal neoplasms: a review. World J Gastro1048 enterol 2014;20:16153–16158. 1049 1050 1051 Reprint requests Address requests for reprints to: Andrew Y. Wang, MD, AGAF, FACG, FASGE, 1052 Section of Interventional Endoscopy, Division of Gastroenterology and Hep1053 atology, Box 800708, University of Virginia Health System, Charlottesville, 1054 Q2 Virginia 22908. e-mail: [email protected]; fax: (434) 244-7590. 1055 1056 1057 1058 1059 1060 1061 1062 1063 1064 1065 1066 1067 1068 1069 1070 1071 1072 1073 1074 1075 1076 1077 1078 1079 1080 1081 1082 1083 1084 1085 1086 1087 1088 1089 1090 1091 1092 1093 1094 1095 1096 1097 1098 1099 1100 1101 1102

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Acknowledgments The authors acknowledge Ms Stephanie Stanford, Coordinator of Guideline Development for the American Gastroenterological Association, for her assistance with coordinating this project. Conflicts of interest These authors disclose the following: Peter Draganov is a consultant for Olympus America, Cook Medical, and Boston Scientific Corporation; Andrew Wang has received research support from Cook Medical on the topic of metal biliary stents; Mohamed Othman is a consultant for Olympus America, Boston Scientific Corporation, and Aries Pharmaceutical, and has received an investigator-initiated grant from AbbVie on the topic of exocrine pancreatic insufficiency; and Norio Fukami is a consultant for Boston Scientific Corporation and Olympus America.

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Supplementary Figure 1. Gastric ESD assisted by using endoscopic traction. A 79-year-old Korean man was referred for ESD of a 4-cm, Paris 0–IIaþIIc lesion with high-grade dysplasia arising from a background of gastric intestinal metaplasia that was located in the incisura and involved the lesser curve of the stomach. The lesion had been biopsied by the referring physician and tattooed. (A) Narrow-band imaging (Olympus America, Center Valley, PA) showed an irregular vascular pattern with amorphous areas suggestive of high-grade dysplasia. Superficial ulcerations corresponded to areas previously sampled with cold forceps biopsies. (B) The borders of the lesion were marked, which is required for gastric ESD because the borders can become indistinct after submucosal injection. Additional peripheral marks can be added to pathologically orient the specimen after resection. (C) Six percent hetastarch in 0.9% sodium chloride tinted with methylene blue was injected dynamically to lift the lesion, and ESD was begun from the distal margin using a DualKnife (Olympus America). (D) Because of submucosal fibrosis from the prior tattoo and biopsies, 1 endoclip tied with dental floss was affixed to the distal lip of the partially resected lesion and a second endoclip was used to hold the thread against the opposite gastric wall to provide (E) pulley-type traction. (F) ESD was completed, and fibrotic tattooed submucosa was seen along the left side of the resection base. (G) En bloc resection was achieved and the specimen was pinned to Styrofoam. Pathology showed multifocal high-grade dysplasia, but no invasive cancer. (H) Follow-up endoscopy 3 months later showed a healed scar with some residual inflammation on NBI, and surveillance biopsies confirmed no residual dysplasia.

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