Endoscopic Mucosal Resection (EMR)
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Endoscopic mucosal resection (EMR) is a technique used for the staging and treatment of superficial neoplasms of the gastrointestinal (GI) tract. This technique was first developed in Japan for the treatment of early gastric cancer (EGC) and has since spread in use throughout the world for various indications, including dysplastic Barrett mucosa and sessile colonic neoplasms. The utility of EMR rests in its ability to do the following:
Several variations of EMR are currently used, including injection-assisted, cap-assisted, and ligation-assisted techniques. All adhere to the basic principles of identification and demarcation of the lesion, submucosal injection to lift the lesion, and endoscopic snare resection. By virtue of its overall safety and efficacy in appropriately selected patient populations, EMR has become firmly integrated into the diagnostic and treatment algorithms of superficial GI malignancies.
Several classification systems for the staging of early GI cancers that may aid in the prediction of lymph node metastases have been developed. Much of this work has been pioneered by Japanese gastroenterologists for the staging and treatment of EGC. The Japanese Society of Gastrointestinal Endoscopists (JSGE), working from large databases of early gastric cancer resections, classified lesions according to their endoscopic features and the implied risk of mural invasion. [1]
The subsequent Paris classification, developed in 2002 at an international consensus meeting, echoed the structure of the JSGE system. In this classification, superficial (Type 0) lesions are divided into polypoid (0-I) and nonpolypoid categories (0-II), which are further subcategorized as pedunculated (0-Ip), sessile (0-Is), slightly elevated (0-IIa), flat (0-IIb), slightly depressed (0-IIc), or excavated (0-III). [2] (See the image below.)
In the Vienna classification, lesions are divided into two broad categories, noninvasive (low-grade dysplasia, high-grade dysplasia [HGD]) and invasive (intramucosal cancer, cancer that infiltrates the submucosa). [3]
The mucosal layer is divided into upper, middle, and lower layers: m1 (epithelium), m2 (lamina propria), and m3 (muscularis mucosae). The submucosa is similarly divided into three layers: sm1, sm2, and sm3. Submucosal tumor involvement of 500 μm or less below the muscularis mucosae is characterized as sm1 (superficial) disease, and involvement past 500 μm is categorized as sm2-3 (deep) disease. [2, 4] The sm1 layer is further divided into sublayers a, b, and c on the basis of the lateral spread within the layer. (See the image below.)
High-frequency (≥20 MHz) endoscopic ultrasonography (EUS) produces an image of the mucosal wall comprising nine separate layers differentiated by their echogenicity. By carefully examining the depth of lesion penetration into the mucosal and submucosal layers, one may determine the risk of lymph node metastases with greater precision. [5]
EUS has excellent sensitivity and specificity in accurately diagnosing the tumor depth and lymph node status of esophageal cancer [6] and is considered the most accurate imaging modality currently available. Its accuracy of EUS ranges from 75% to 82% for T1 disease, from 88% to 100% for T4 disease, and from 72% to 80% for lymph node involvement. [7]
A 2017 study examining the accuracy of staging with radiologic and pathologic correlation in patients with esophageal cancer with lymph node metastases who were radiologically staged as N0 reported that whereas EUS, contrast-enhanced computed tomography (CT), and PET/CT were all more likely to understage nodal disease, PET/CT was more likely to do so than EUS was. [8] The accuracy, sensitivity, and specificity of EUS for N0 vs N+ disease were 55.4%, 42.6% and 75%. The majority of lymph nodes (82%) were smaller than 6 mm, making direct visualization challenging with current medical imaging techniques (probably the main reason for the discrepancy between radiologic and pathologic staging).
False-positive EUS images are attributed to peritumoral inflammation, whereas false-negative staging is often due to the microscopic spread of tumor not detectable by EUS. Micrometastases have been found in lymph nodes of early esophageal tumors (as many as 44% in one study [8] ). Because of the limitations of the technology, EUS is subject to significant rates of false positive and negative disease; however, EUS followed by EMR and histopathologic analysis remains the standard of care for early esophageal cancer staging.
EMR may be considered for definitive treatment of superficial premalignant and well-differentiated to moderately differentiated malignant lesions of the GI tract in the absence of lymph node or distant metastases (T1mN0M0). It also plays an integral role in the staging algorithm of early GI cancers by providing a larger resection specimen than standard forceps biopsy, allowing accurate T staging and establishing the presence of lymphovascular involvement. [9] Furthermore, pathologic examination of EMR resection specimens frequently leads to significant alterations in patient management. [10]
Previous criteria from the JSGE include a lesion size smaller than 2 cm and involvement of less than one third of the esophageal circumference. Disease-specific survival rates after EMR are as high as 95%, with a low rate of complications. [11, 12, 13] Staging EMR may be performed on lesions lacking architectural or EUS features suggestive of deep submucosal invasion (see Technical Considerations).
EMR should be used in segments of Barrett esophagus (BE) with mucosal irregularities, including nodularity, ulceration, or flat but irregular mucosal contour. This allows more accurate staging of the lesion, as well as potential therapeutic benefit if a lesion is completely resected. Accurate pathologic staging, the potential for cure, and a favorable safety profile are all reported advantages of EMR in this setting. [14, 15, 16, 17]
As with squamous neoplasms, EMR is considered definitive therapy for cancer if the lesion is well-differentiated to moderately differentiated, is limited to the mucosal layer, is 2 cm or smaller, and has no lymphovascular invasion. If an EMR specimen is a definitively resected Barrett cancer or shows only high-grade dysplasia, endoscopic ablative therapy of the remaining BE should be performed. If the EMR specimen demonstrates neoplasia at the deep margin, residual neoplasia should be assumed, and surgical or systemic therapy (chemotherapy, radiation, or a combination of the two) should be considered. [18]
Investigations have demonstrated the efficacy of EMR applied to the treatment of larger lesions, as well as the complete eradication of BE with favorable results (albeit with potential increases in complications). [19]
As an established alternative to surgery, guidelines for the use of EMR in the treatment of EGC have been published by the JSGE. [20]
Well- or moderately differentiated tubular and papillary adenocarcinomas are classified as differentiated cancers, whereas signet-ring cell carcinomas and poorly differentiated adenocarcinomas are classified as undifferentiated cancers. Indications for endoscopic resection are classified as absolute, expanded, or out of indication and are based on the following:
Absolute indications for endoscopic resection include the following:
Expanded indications include the following:
Endoscopic submucosal dissection (ESD) has been developed as an alternative to EMR. In ESD, the mucosa surrounding the lesion is first raised with saline or another solution and excised with a diathermy knife. This step is followed by dissection of the submucosa beneath the lesion for an en-bloc resection. Factors determining whether EMR or ESD is indicated include the following:
Given the risk of incomplete resection with EMR for lesions with expanded indications, ESD is recommended by the JSGE as the preferred modality. There have been no randomized controlled trials comparing clinical outcomes between gastric EMR and ESD.
In a Japanese retrospective gastric cancer registry of 12,647 patients comparing short- and long-term outcomes of EMR and ESD, 81% of patients underwent ESD and 19% underwent EMR. [21] En-bloc and R0 resections were achieved in 79% and 89% of patients undergoing EMR and ESD, respectively. The total proportion of patients who underwent curative resection was 69%; 44% underwent curative resection for absolute indication lesions, and 25% underwent curative resection for expanded indication lesions.
In this study, the 5-year overall survival rate was 92% in patients with absolute indications and 90% in those with expanded indications after curative resection and 87% in those undergoing noncurative resection. [21] The 5-year disease-specific survival rates were 99.9% for absolute indications and curative resection, 99.7% for expanded indications with curative resection, and 98.7% for noncurative resections.
The standard treatment for expanded indication lesions, however, remains surgery.
EMR has been used in the treatment and staging of ampullary and periampullary adenomas, early carcinomas, and ampullary submucosal lesions. Additional applications include nonampullary adenomas, neuroendocrine tumors, and submucosal lesions. Available evidence suggests that duodenal EMR may be associated with a substantial rate of complications, particularly in the treatment of submucosal lesions (see Complications).
EMR has been applied to the evaluation of submucosal lesions, partly because of the often scant cellularity of fine-needle aspiration (FNA) specimens and the inability to establish the presence of malignancy with such specimens. In a study of gastric submucosal lesions no larger than 2 cm, EMR was shown to be safe and resulted in complete resection in a single session with the injection-assisted or cap-assisted techniques. [22] Definitive histologic diagnosis was obtained in all cases, compared with an accuracy of 45.5% for EUS alone. Because of the risk of bleeding and perforation, treatment should be restricted to lesions arising in the submucosal layer as defined by EUS.
EMR is commonly used for the resection of laterally spreading benign or malignant lesions of the colon, including early-stage colon cancers, flat adenomas, large superficial colorectal tumors, and rectal carcinoids. The “lift-and-cut” technique is most commonly used, as opposed to cap-assisted or ligation-assisted EMR (see Technique). Appropriate indications include the following [23] :
Additional indications also include those patients who refuse surgical intervention or in whom significant comorbidities are prohibitive.
In 2015, the Japan Gastroenterological Endoscopy Society (JGES) published guidelines for colorectal EMR/ESD, including the following recommendations [24] :
Successful removal of larger lesions has been well documented but is associated with higher recurrence rates, highlighting the need for intensive surveillance after EMR (see Monitoring & Follow-up). [25, 26, 27]
For large lesions whose size exceeds half of the circumference of the colorectal lumen, piecemeal EMR should be avoided, and ESD or a surgical resection should be performed. [24]
Contraindications include the presence of or a high index of suspicion for lymph node or distant metastases (see Technical Considerations).
The nonlifting sign, defined as the failure of a lesion to elevate above the surrounding mucosa after submucosal injection underneath the lesion, has been established as a highly accurate and specific predictor of submucosal invasion by colonic lesions. [28] With regard to mucosal lesions with a nonlifting sign and residual or recurrent lesions, ESD often can resect those lesions for which EMR is generally difficult and for which en-bloc resection is desirable. [24]
Biopsy of the lesion before EMR may result in a false-positive result as a consequence of fibrosis at the biopsy site. Because the result of mucosal biopsies is unlikely to alter treatment algorithms, biopsy prior to referral for EMR should be avoided. If biopsy is undertaken, minimization of the time interval between biopsy and EMR may help reduce false-positive results. [29]
The presence of coagulopathy is a relative contraindication, in view of the risk of bleeding. Any contraindication that applies to standard endoscopy (eg, severe cardiopulmonary comorbidities) is also applicable to EMR.
Given the increasing risk of lymph node metastases associated with deeper tumor invasion into the wall, determination of the depth of lesion penetration is an integral step before EMR is considered.
The following two methods can be used to predict the depth of penetration:
Certain lesion characteristics detectable on endoscopy (see Background) have been associated with risk of submucosal invasion, including the following [30] :
For those lesions with submucosal invasion, the risk of lymph node metastases is further modified by the presence or absence of lymphovascular invasion on histologic examination. [32] In one study of HGD and early cancerin BE, lymph node metastases were detected in 0%, 23%, and 69% of lesions within the sm1, sm2, and sm3 layers, respectively. [33]
Several retrospective studies of patients with T1b esophageal adenocarcinoma undergoing esophagectomy have found that 16-18% of patients have lymph node metastasis and 27-34% have lymphovascular invasion. [34] Studies comparing lymph node metastases between sm1 and sm2-3 disease, all retrospective and including small numbers of patients, have shown conflicting results. [35, 36, 37]
Similarly, in a study of more than 3000 patients who had undergone gastrectomy with lymph node dissection for early gastric cancer, no lymph node metastases were seen with well-differentiated to moderately differentiated lesions smaller than 3 cm that were confined to the mucosal or sm1 layers without lymphovascular invasion. [38]
Standard EUS, with a probe frequency of 7.5-12 MHz, is the most commonly used method of determining the presence of lymph node metastases immediately before EMR. Compared with high-frequency EUS, standard EUS provides greater tissue penetration, displaying a five-layer mucosal wall while allowing visualization of locoregional lymph nodes.
In evaluating for lymph node metastases in BE-HGD and early-stage Barrett-associated easophageal adenocarcinoma, EUS demonstrated an accuracy of 93% in an early series. [33] In a second study, EUS identified suspicious lymph node metastases in 28% of patients referred for EMR of BE-HGD and BE-EAC, and FNA confirmed metastases in 71% of these cases. [39]
A subsequent study examined the accuracy of staging with radiologic and pathologic correlation in patients who had esophageal cancer with lymph node metastases and who were radiologically staged as N0. [8] EUS correctly identified N0 vs N+ disease in 55.4% of cases. Its sensitivity for identifying N0 vs N+ disease was 42.6%, and its specificity was 75%.
The impact of the information provided by EUS beyond that of a careful endoscopic examination has been questioned. [40] As a result, the use of EUS before EMR has been somewhat controversial. [41, 42] Nonetheless, EUS remains the most widely accepted method of assessing for the presence of lymph node metastases immediately before EMR.
EMR should be performed by experienced operators in a center of expertise. Appropriate adjuncts to treatment should be readily available in the procedure room (see Periprocedural Care). Additionally, interventional radiology and surgical backup should be available in the event of uncontrolled hemorrhage or perforation.
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Bruce D Greenwald, MD Professor of Medicine, Division of Gastroenterology and Hepatology, University of Maryland School of Medicine
Bruce D Greenwald, MD is a member of the following medical societies: Alpha Omega Alpha, American College of Gastroenterology, American College of Physicians, American Gastroenterological Association, American Society for Gastrointestinal Endoscopy
Disclosure: Nothing to disclose.
Matthew Hudson, MD Fellow, Department of Gastroenterology and Hepatology, University of Maryland Medical System
Disclosure: Nothing to disclose.
Fariha H Ramay, MD, MBA Fellow, Division of Gastroenterology and Hepatology, Department of Medicine, University of Maryland School of Medicine
Fariha H Ramay, MD, MBA is a member of the following medical societies: American Gastroenterological Association, American Society for Gastrointestinal Endoscopy, Phi Beta Kappa
Disclosure: Received research grant from: National Institute of Diabetes and Digestive and Kidney Diseases of the National Institutes of Health under Award Number T32DK067872. .
Mary L Windle, PharmD Adjunct Associate Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference
Disclosure: Nothing to disclose.
Kurt E Roberts, MD Assistant Professor, Section of Surgical Gastroenterology, Department of Surgery, Director, Surgical Endoscopy, Associate Director, Surgical Skills and Simulation Center and Surgical Clerkship, Yale University School of Medicine
Kurt E Roberts, MD is a member of the following medical societies: American College of Surgeons, Society of American Gastrointestinal and Endoscopic Surgeons, Society of Laparoendoscopic Surgeons
Disclosure: Nothing to disclose.
William R Brugge, MD Professor of Medicine, Harvard Medical School; Director, Gastrointestinal Endoscopy Unit, Massachusetts General Hospital
William R Brugge, MD is a member of the following medical societies: American College of Gastroenterology, American College of Physicians, American Federation for Clinical Research, American Gastroenterological Association, American Pancreatic Association, American Society of Gastrointestinal Endoscopy, and Crohns and Colitis Foundation of America
Disclosure: RedPath Grant/research funds Consulting
Rabindra Watson, MD Clinical Instructor, Interventional Endoscopy Services, Division of Gastroenterology, University of California, Los Angeles, David Geffen School of Medicine
Rabindra Watson, MD is a member of the following medical societies: American College of Gastroenterology, American Gastroenterological Association, and American Society of Gastrointestinal Endoscopy
Disclosure: Nothing to disclose.
Acknowledgments
Medscape Reference thanks Dawn Sears, MD, Associate Professor of Internal Medicine, Division of Gastroenterology and Hepatology, Scott and White Memorial Hospital; and Dan C Cohen, MD, Fellow in Gastroenterology, Scott and White Hospital, Texas A&M Health Science Center College of Medicine, for assistance with the video contribution to this article.
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