Endoscopic Mucosal Resection (EMR)
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. 
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).  (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). 
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. 
EUS has excellent sensitivity and specificity in accurately diagnosing the tumor depth and lymph node status of esophageal cancer  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. 
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.  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  ). 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.  Furthermore, pathologic examination of EMR resection specimens frequently leads to significant alterations in patient management. 
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. 
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). 
As an established alternative to surgery, guidelines for the use of EMR in the treatment of EGC have been published by the JSGE. 
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.  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.  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.  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  :
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  :
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. 
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.  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. 
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. 
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:
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.  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. 
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.  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. 
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.  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. 
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.  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.  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.
The general rules for The gastric cancer study in surgery. Jpn J Surg. 1973 Mar. 3(1):61-71. [Medline].
The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc. 2003 Dec. 58(6 Suppl):S3-43. [Medline].
Willis J, Riddell RH. Biology versus terminology: East meets West in surgical pathology. Gastrointest Endosc. 2003 Mar. 57(3):369-76. [Medline].
Tian J, Prasad GA, Lutzke LS, Lewis JT, Wang KK. Outcomes of T1b esophageal adenocarcinoma patients. Gastrointest Endosc. 2011 Dec. 74 (6):1201-6. [Medline].
Akahoshi K, Chijiwa Y, Hamada S, Sasaki I, Nawata H, Kabemura T. Pretreatment staging of endoscopically early gastric cancer with a 15 MHz ultrasound catheter probe. Gastrointest Endosc. 1998 Nov. 48(5):470-6. [Medline].
Napier KJ, Scheerer M, Misra S. Esophageal cancer: A Review of epidemiology, pathogenesis, staging workup and treatment modalities. World J Gastrointest Oncol. 2014 May 15. 6 (5):112-20. [Medline]. [Full Text].
Souquet JC, Napoléon B, Pujol B, Keriven O, Ponchon T, Descos F, et al. Endoscopic ultrasonography in the preoperative staging of esophageal cancer. Endoscopy. 1994 Nov. 26 (9):764-6. [Medline].
Foley KG, Christian A, Fielding P, Lewis WG, Roberts SA. Accuracy of contemporary oesophageal cancer lymph node staging with radiological-pathological correlation. Clin Radiol. 2017 Mar 28. [Medline].
Larghi A, Lightdale CJ, Memeo L, Bhagat G, Okpara N, Rotterdam H. EUS followed by EMR for staging of high-grade dysplasia and early cancer in Barrett’s esophagus. Gastrointest Endosc. 2005 Jul. 62(1):16-23. [Medline].
Moss A, Bourke MJ, Hourigan LF, Gupta S, Williams SJ, Tran K. Endoscopic resection for Barrett’s high-grade dysplasia and early esophageal adenocarcinoma: an essential staging procedure with long-term therapeutic benefit. Am J Gastroenterol. 2010 Jun. 105(6):1276-83. [Medline].
Inoue H, Fukami N, Yoshida T, Kudo SE. Endoscopic mucosal resection for esophageal and gastric cancers. J Gastroenterol Hepatol. 2002 Apr. 17(4):382-8. [Medline].
Ciocirlan M, Lapalus MG, Hervieu V, Souquet JC, Napoléon B, Scoazec JY. Endoscopic mucosal resection for squamous premalignant and early malignant lesions of the esophagus. Endoscopy. 2007 Jan. 39(1):24-9. [Medline].
Ell C, May A, Gossner L, Pech O, Günter E, Mayer G, et al. Endoscopic mucosal resection of early cancer and high-grade dysplasia in Barrett’s esophagus. Gastroenterology. 2000 Apr. 118(4):670-7. [Medline].
Nijhawan PK, Wang KK. Endoscopic mucosal resection for lesions with endoscopic features suggestive of malignancy and high-grade dysplasia within Barrett’s esophagus. Gastrointest Endosc. 2000 Sep. 52(3):328-32. [Medline].
Vieth M, Ell C, Gossner L, May A, Stolte M. Histological analysis of endoscopic resection specimens from 326 patients with Barrett’s esophagus and early neoplasia. Endoscopy. 2004 Sep. 36(9):776-81. [Medline].
Yamashita DT, Li C, Bethune D, Henteleff H, Ellsmere J. Endoscopic mucosal resection for high-grade dysplasia and intramucosal carcinoma: a Canadian experience. Can J Surg. 2017 Apr. 60 (2):129-133. [Medline]. [Full Text].
[Guideline] Shaheen NJ, Falk GW, Iyer PG, Gerson LB, American College of Gastroenterology. ACG Clinical Guideline: Diagnosis and Management of Barrett’s Esophagus. Am J Gastroenterol. 2016 Jan. 111 (1):30-50; quiz 51. [Medline].
Chennat J, Konda VJ, Ross AS, de Tejada AH, Noffsinger A, Hart J. Complete Barrett’s eradication endoscopic mucosal resection: an effective treatment modality for high-grade dysplasia and intramucosal carcinoma–an American single-center experience. Am J Gastroenterol. 2009 Nov. 104(11):2684-92. [Medline].
Tanabe S, Hirabayashi S, Oda I, Ono H, Nashimoto A, Isobe Y, et al. Gastric cancer treated by endoscopic submucosal dissection or endoscopic mucosal resection in Japan from 2004 through 2006: JGCA nationwide registry conducted in 2013. Gastric Cancer. 2017 Feb 15. [Medline].
Yokota T, Sugihara K, Yoshida S. Endoscopic mucosal resection for colorectal neoplastic lesions. Dis Colon Rectum. 1994 Nov. 37(11):1108-11. [Medline].
[Guideline] Tanaka S, Kashida H, Saito Y, Yahagi N, Yamano H, Saito S, et al. JGES guidelines for colorectal endoscopic submucosal dissection/endoscopic mucosal resection. Dig Endosc. 2015 May. 27 (4):417-34. [Medline].
Conio M, Repici A, Demarquay JF, Blanchi S, Dumas R, Filiberti R. EMR of large sessile colorectal polyps. Gastrointest Endosc. 2004 Aug. 60(2):234-41. [Medline].
Carvalho R, Areia M, Brito D, Saraiva S, Alves S, Cadime AT. Endoscopic mucosal resection of large colorectal polyps: prospective evaluation of recurrence and complications. Acta Gastroenterol Belg. 2013 Jun. 76(2):225-30. [Medline].
Kim MS, Kim NK, Park JH. Intramural recurrence without mucosal lesions after an endoscopic mucosal resection for early colorectal cancer. Ann Coloproctol. 2013 Jun. 29(3):126-9. [Medline]. [Full Text].
Uno Y, Munakata A. The non-lifting sign of invasive colon cancer. Gastrointest Endosc. 1994 Jul-Aug. 40(4):485-9. [Medline].
Han KS, Sohn DK, Choi DH, Hong CW, Chang HJ, Lim SB. Prolongation of the period between biopsy and EMR can influence the nonlifting sign in endoscopically resectable colorectal cancers. Gastrointest Endosc. 2008 Jan. 67(1):97-102. [Medline].
Kojima T, Parra-Blanco A, Takahashi H, Fujita R. Outcome of endoscopic mucosal resection for early gastric cancer: review of the Japanese literature. Gastrointest Endosc. 1998 Nov. 48(5):550-4; discussion 554-5. [Medline].
Barbour AP, Jones M, Brown I, Gotley DC, Martin I, Thomas J, et al. Risk stratification for early esophageal adenocarcinoma: analysis of lymphatic spread and prognostic factors. Ann Surg Oncol. 2010 Sep. 17 (9):2494-502. [Medline].
Tajima Y, Nakanishi Y, Ochiai A, Tachimori Y, Kato H, Watanabe H, et al. Histopathologic findings predicting lymph node metastasis and prognosis of patients with superficial esophageal carcinoma: analysis of 240 surgically resected tumors. Cancer. 2000 Mar 15. 88(6):1285-93. [Medline].
Buskens CJ, Westerterp M, Lagarde SM, Bergman JJ, ten Kate FJ, van Lanschot JJ. Prediction of appropriateness of local endoscopic treatment for high-grade dysplasia and early adenocarcinoma by EUS and histopathologic features. Gastrointest Endosc. 2004 Nov. 60(5):703-10. [Medline].
Badreddine RJ, Prasad GA, Lewis JT, Lutzke LS, Borkenhagen LS, Dunagan KT, et al. Depth of submucosal invasion does not predict lymph node metastasis and survival of patients with esophageal carcinoma. Clin Gastroenterol Hepatol. 2010 Mar. 8 (3):248-53. [Medline]. [Full Text].
Lorenz D, Origer J, Pauthner M, Graupe F, Fisseler-Eckhoff A, Stolte M, et al. Prognostic risk factors of early esophageal adenocarcinomas. Ann Surg. 2014 Mar. 259 (3):469-76. [Medline].
Sepesi B, Watson TJ, Zhou D, Polomsky M, Litle VR, Jones CE, et al. Are endoscopic therapies appropriate for superficial submucosal esophageal adenocarcinoma? An analysis of esophagectomy specimens. J Am Coll Surg. 2010 Apr. 210 (4):418-27. [Medline].
Westerterp M, Koppert LB, Buskens CJ, Tilanus HW, ten Kate FJ, Bergman JJ, et al. Outcome of surgical treatment for early adenocarcinoma of the esophagus or gastro-esophageal junction. Virchows Arch. 2005 May. 446 (5):497-504. [Medline].
Gotoda T, Yanagisawa A, Sasako M, Ono H, Nakanishi Y, Shimoda T. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer. 2000 Dec. 3(4):219-225. [Medline].
Shami VM, Villaverde A, Stearns L, Chi KD, Kinney TP, Rogers GB. Clinical impact of conventional endosonography and endoscopic ultrasound-guided fine-needle aspiration in the assessment of patients with Barrett’s esophagus and high-grade dysplasia or intramucosal carcinoma. Endoscopy. February 2006. 38(2):157-61. [Medline].
Hizawa K, Iwai K, Esaki M, Matsumoto T, Suekane H, Iida M. Is endoscopic ultrasonography indispensable in assessing the appropriateness of endoscopic resection for gastric cancer?. Endoscopy. 2002 Dec. 34(12):973-8. [Medline].
May A, Günter E, Roth F, Gossner L, Stolte M, Vieth M. Accuracy of staging in early oesophageal cancer using high resolution endoscopy and high resolution endosonography: a comparative, prospective, and blinded trial. Gut. 2004 May. 53(5):634-40. [Medline].
Yanai H, Noguchi T, Mizumachi S, Tokiyama H, Nakamura H, Tada M, et al. A blind comparison of the effectiveness of endoscopic ultrasonography and endoscopy in staging early gastric cancer. Gut. 1999 Mar. 44(3):361-5. [Medline]. [Full Text].
Hamada T, Kondo K, Itagaki Y, Nishida J. [Endoscopic mucosal resection for early gastric cancer]. Nippon Rinsho. 1996 May. 54(5):1292-7. [Medline].
Yoshida M, Hanashi T, Momma K, Yamada Y, Sakaki N, Koike M, et al. [Endoscopic mucosal resection for radical treatment of esophageal cancer]. Gan To Kagaku Ryoho. 1995 Jun. 22(7):847-54. [Medline].
Nomura T, Boku N, Ohtsu A, Muto M, Matsumoto S, Tajiri H, et al. Recurrence after endoscopic mucosal resection for superficial esophageal cancer. Endoscopy. 2000 Apr. 32(4):277-80. [Medline].
Lopes CV, Hela M, Pesenti C, Bories E, Caillol F, Monges G. Circumferential endoscopic resection of Barrett’s esophagus with high-grade dysplasia or early adenocarcinoma. Surg Endosc. 2007 May. 21(5):820-4. [Medline].
Conio M, Repici A, Cestari R, Blanchi S, Lapertosa G, Missale G. Endoscopic mucosal resection for high-grade dysplasia and intramucosal carcinoma in Barrett’s esophagus: an Italian experience. World J Gastroenterol. 2005 Nov 14. 11(42):6650-5. [Medline].
Ell C, May A, Pech O, Gossner L, Guenter E, Behrens A, et al. Curative endoscopic resection of early esophageal adenocarcinomas (Barrett’s cancer). Gastrointest Endosc. 2007 Jan. 65(1):3-10. [Medline].
Pech O, Behrens A, May A, Nachbar L, Gossner L, Rabenstein T, et al. Long-term results and risk factor analysis for recurrence after curative endoscopic therapy in 349 patients with high-grade intraepithelial neoplasia and mucosal adenocarcinoma in Barrett’s oesophagus. Gut. 2008 Sep. 57(9):1200-6. [Medline].
Prasad GA, Wu TT, Wigle DA, Buttar NS, Wongkeesong LM, Dunagan KT. Endoscopic and surgical treatment of mucosal (T1a) esophageal adenocarcinoma in Barrett’s esophagus. Gastroenterology. 2009 Sep. 137(3):815-23. [Medline].
Tomizawa Y, Iyer PG, Wong Kee Song LM, Buttar NS, Lutzke LS, Wang KK. Safety of endoscopic mucosal resection for Barrett’s esophagus. Am J Gastroenterol. 2013 Sep. 108 (9):1440-7; quiz 1448. [Medline].
[Guideline] Hirota WK, Zuckerman MJ, Adler DG, Davila RE, Egan J, Leighton JA. ASGE guideline: the role of endoscopy in the surveillance of premalignant conditions of the upper GI tract. Gastrointest Endosc. 2006 Apr. 63(4):570-80. [Medline].
[Guideline] ASGE Standards of Practice Committee, Evans JA, Early DS, Fukami N, et al. The role of endoscopy in Barrett’s esophagus and other premalignant conditions of the esophagus. Gastrointest Endosc. 2012 Dec. 76 (6):1087-94. [Medline].
[Guideline] American Gastroenterological Association Medical Position Statement on the Management of Barrett’s Esophagus. Gastroenterology. 2011 Mar. 140(3):1084-91. [Medline].
Takekoshi T, Baba Y, Ota H, Kato Y, Yanagisawa A, Takagi K. Endoscopic resection of early gastric carcinoma: results of a retrospective analysis of 308 cases. Endoscopy. 1994 May. 26(4):352-8. [Medline].
Inoue H, Fukami N, Yoshida T, Kudo SE. Endoscopic mucosal resection for esophageal and gastric cancers. J Gastroenterol Hepatol. 2002 Apr. 17 (4):382-8. [Medline].
Mizumoto S, Misumi A, Harada K, Arima K, Hirata T, Yoshinaka I, et al. [Evaluation of endoscopic mucosal resection (EMR) as a curative therapy against early gastric cancer]. Nippon Geka Gakkai Zasshi. 1992 Sep. 93(9):1071-4. [Medline].
Arima N, Adachi K, Katsube T, Amano K, Ishihara S, Watanabe M. Predictive factors for metachronous recurrence of early gastric cancer after endoscopic treatment. J Clin Gastroenterol. 1999 Jul. 29(1):44-7. [Medline].
Irani S, Arai A, Ayub K, Biehl T, Brandabur JJ, Dorer R. Papillectomy for ampullary neoplasm: results of a single referral center over a 10-year period. Gastrointest Endosc. 2009 Nov. 70(5):923-32. [Medline].
Ahmad NA, Kochman ML, Long WB, Furth EE, Ginsberg GG. Efficacy, safety, and clinical outcomes of endoscopic mucosal resection: a study of 101 cases. Gastrointest Endosc. 2002 Mar. 55(3):390-6. [Medline].
Oka S, Tanaka S, Nagata S, Hiyama T, Ito M, Kitadai Y. Clinicopathologic features and endoscopic resection of early primary nonampullary duodenal carcinoma. J Clin Gastroenterol. 2003 Nov-Dec. 37(5):381-6. [Medline].
Wehrmann T, Martchenko K, Nakamura M, Riphaus A, Stergiou N. Endoscopic resection of submucosal esophageal tumors: a prospective case series. Endoscopy. 2004 Sep. 36(9):802-7. [Medline].
Rösch T, Sarbia M, Schumacher B, Deinert K, Frimberger E, Toermer T. Attempted endoscopic en bloc resection of mucosal and submucosal tumors using insulated-tip knives: a pilot series. Endoscopy. 2004 Sep. 36(9):788-801. [Medline].
Tung SY, Wu CS, Wu MC, Su MY. Endoscopic treatment of colorectal polyps and early cancer. Dig Dis Sci. 2001 Jun. 46(6):1152-6. [Medline].
Zlatanic J, Waye JD, Kim PS, Baiocco PJ, Gleim GW. Large sessile colonic adenomas: use of argon plasma coagulator to supplement piecemeal snare polypectomy. Gastrointest Endosc. 1999 Jun. 49(6):731-5. [Medline].
Brooker JC, Saunders BP, Shah SG, Thapar CJ, Suzuki N, Williams CB. Treatment with argon plasma coagulation reduces recurrence after piecemeal resection of large sessile colonic polyps: a randomized trial and recommendations. Gastrointest Endosc. 2002 Mar. 55(3):371-5. [Medline].
Regula J, Wronska E, Polkowski M, Nasierowska-Guttmejer A, Pachlewski J, Rupinski M, et al. Argon plasma coagulation after piecemeal polypectomy of sessile colorectal adenomas: long-term follow-up study. Endoscopy. 2003 Mar. 35(3):212-8. [Medline].
Kim TJ, Kim ER, Hong SN, Kim YH, Chang DK. Current practices in endoscopic submucosal dissection for colorectal neoplasms: a survey of indications among Korean endoscopists. Intest Res. 2017 Apr. 15 (2):228-235. [Medline]. [Full Text].
Curcio G, Granata A, Ligresti D, Tarantino I, Barresi L, Liotta R, et al. Underwater colorectal EMR: remodeling endoscopic mucosal resection. Gastrointest Endosc. 2015 May. 81 (5):1238-42. [Medline].
Tada M, Murata M, Murakami F, et al. Development of the strip-off biopsy [in Japanese with English abstract]. Gastrointest Endosc. 1984. 26:833.
Larghi A, Waxman I. State of the art on endoscopic mucosal resection and endoscopic submucosal dissection. Gastrointest Endosc Clin N Am. 2007 Jul. 17(3):441-69, v. [Medline].
Yamamoto H, Sekine Y, Higashizawa T, Kihira K, Kaneko Y, Hosoya Y. Successful en bloc resection of a large superficial gastric cancer by using sodium hyaluronate and electrocautery incision forceps. Gastrointest Endosc. 2001 Nov. 54(5):629-32. [Medline].
Fujishiro M, Yahagi N, Nakamura M, Kakushima N, Kodashima S, Ono S. Successful outcomes of a novel endoscopic treatment for GI tumors: endoscopic submucosal dissection with a mixture of high-molecular-weight hyaluronic acid, glycerin, and sugar. Gastrointest Endosc. 2006 Feb. 63(2):243-9. [Medline].
Uraoka T, Fujii T, Saito Y, Sumiyoshi T, Emura F, Bhandari P, et al. Effectiveness of glycerol as a submucosal injection for EMR. Gastrointest Endosc. 2005 May. 61(6):736-40. [Medline].
Giday SA, Magno P, Buscaglia JM, Canto MI, Ko CW, Shin EJ, et al. Is blood the ideal submucosal cushioning agent? A comparative study in a porcine model. Endoscopy. 2006 Dec. 38(12):1230-4. [Medline].
Sato T. A novel method of endoscopic mucosal resection assisted by submucosal injection of autologous blood (blood patch EMR). Dis Colon Rectum. 2006 Oct. 49(10):1636-41. [Medline].
Yandrapu H, Desai M, Siddique S, Vennalganti P, Vennalaganti S, Parasa S, et al. Normal saline solution versus other viscous solutions for submucosal injection during endoscopic mucosal resection: a systematic review and meta-analysis. Gastrointest Endosc. 2017 Apr. 85 (4):693-699. [Medline].
Inoue H, Endo M, Takeshita K, Yoshino K, Muraoka Y, Yoneshima H. A new simplified technique of endoscopic esophageal mucosal resection using a cap-fitted panendoscope (EMRC). Surg Endosc. 1992 Sep-Oct. 6(5):264-5. [Medline].
Fleischer DE, Wang GQ, Dawsey S, Tio TL, Newsome J, Kidwell J, et al. Tissue band ligation followed by snare resection (band and snare): a new technique for tissue acquisition in the esophagus. Gastrointest Endosc. 1996 Jul. 44(1):68-72. [Medline].
Chaves DM, Sakai P, Mester M, Spinosa SR, Tomishige T, Ishioka S. A new endoscopic technique for the resection of flat polypoid lesions. Gastrointest Endosc. 1994 Mar-Apr. 40(2 Pt 1):224-6. [Medline].
Kawahara Y, Hori K, Takenaka R, Nasu J, Kawano S, Kita M, et al. Endoscopic submucosal dissection of esophageal cancer using the Mucosectom2 device: a feasibility study. Endoscopy. 2013 Nov. 45 (11):869-75. [Medline].
Okano A, Hajiro K, Takakuwa H, Nishio A, Matsushita M. Predictors of bleeding after endoscopic mucosal resection of gastric tumors. Gastrointest Endosc. 2003 May. 57(6):687-90. [Medline].
Lee SH, Park JH, Park do H, Chung IK, Kim HS, Park SH. Clinical efficacy of EMR with submucosal injection of a fibrinogen mixture: a prospective randomized trial. Gastrointest Endosc. 2006 Nov. 64(5):691-6. [Medline].
ASGE Technology Committee., Hwang JH, Konda V, Abu Dayyeh BK, Chauhan SS, Enestvedt BK, et al. Endoscopic mucosal resection. Gastrointest Endosc. 2015 Aug. 82 (2):215-26. [Medline].
Tomizawa Y, Iyer PG, Wong Kee Song LM, Buttar NS, Lutzke LS, Wang KK. Safety of endoscopic mucosal resection for Barrett’s esophagus. Am J Gastroenterol. 2013 Sep. 108 (9):1440-7; quiz 1448. [Medline]. [Full Text].
Ono H. Early gastric cancer: diagnosis, pathology, treatment techniques and treatment outcomes. Eur J Gastroenterol Hepatol. 2006 Aug. 18 (8):863-6. [Medline].
Park YM, Cho E, Kang HY, Kim JM. The effectiveness and safety of endoscopic submucosal dissection compared with endoscopic mucosal resection for early gastric cancer: a systematic review and metaanalysis. Surg Endosc. 2011 Aug. 25 (8):2666-77. [Medline].
Yoshikane H, Hidano H, Sakakibara A, Ayakawa T, Mori S, Kawashima H, et al. Endoscopic repair by clipping of iatrogenic colonic perforation. Gastrointest Endosc. 1997 Nov. 46(5):464-6. [Medline].
Kim HS, Lee DK, Jeong YS, Kim KH, Baik SK, Kwon SO, et al. Successful endoscopic management of a perforated gastric dysplastic lesion after endoscopic mucosal resection. Gastrointest Endosc. 2000 May. 51(5):613-5. [Medline].
Binmoeller KF, Grimm H, Soehendra N. Endoscopic closure of a perforation using metallic clips after snare excision of a gastric leiomyoma. Gastrointest Endosc. 1993 Mar-Apr. 39(2):172-4. [Medline].
Kantsevoy SV, Bitner M, Mitrakov AA, Thuluvath PJ. Endoscopic suturing closure of large mucosal defects after endoscopic submucosal dissection is technically feasible, fast, and eliminates the need for hospitalization (with videos). Gastrointest Endosc. 2014 Mar. 79 (3):503-7. [Medline].
Takahashi R, Yoshio T, Horiuchi Y, Omae M, Ishiyama A, Hirasawa T, et al. Endoscopic tissue shielding for esophageal perforation caused by endoscopic resection. Clin J Gastroenterol. 2017 Jun. 10 (3):214-219. [Medline].
Konda VJ, Gonzalez Haba Ruiz M, Koons A, Hart J, Xiao SY, Siddiqui UD, et al. Complete endoscopic mucosal resection is effective and durable treatment for Barrett’s-associated neoplasia. Clin Gastroenterol Hepatol. 2014 Dec. 12 (12):2002-10.e1-2. [Medline].
van Vilsteren FG, Pouw RE, Seewald S, Alvarez Herrero L, Sondermeijer CM, Visser M, et al. Stepwise radical endoscopic resection versus radiofrequency ablation for Barrett’s oesophagus with high-grade dysplasia or early cancer: a multicentre randomised trial. Gut. 2011 Jun. 60 (6):765-73. [Medline].
Seewald S, Akaraviputh T, Seitz U, Brand B, Groth S, Mendoza G, et al. Circumferential EMR and complete removal of Barrett’s epithelium: a new approach to management of Barrett’s esophagus containing high-grade intraepithelial neoplasia and intramucosal carcinoma. Gastrointest Endosc. 2003 Jun. 57 (7):854-9. [Medline].
Peters FP, Kara MA, Rosmolen WD, ten Kate FJ, Krishnadath KK, van Lanschot JJ, et al. Stepwise radical endoscopic resection is effective for complete removal of Barrett’s esophagus with early neoplasia: a prospective study. Am J Gastroenterol. 2006 Jul. 101 (7):1449-57. [Medline].
Qumseya B, Panossian AM, Rizk C, Cangemi D, Wolfsen C, Raimondo M, et al. Predictors of esophageal stricture formation post endoscopic mucosal resection. Clin Endosc. 2014 Mar. 47 (2):155-61. [Medline]. [Full Text].
Pech O, Behrens A, May A, Nachbar L, Gossner L, Rabenstein T, et al. Long-term results and risk factor analysis for recurrence after curative endoscopic therapy in 349 patients with high-grade intraepithelial neoplasia and mucosal adenocarcinoma in Barrett’s oesophagus. Gut. 2008 Sep. 57 (9):1200-6. [Medline].
Pouw RE, Seewald S, Gondrie JJ, Deprez PH, Piessevaux H, Pohl H, et al. Stepwise radical endoscopic resection for eradication of Barrett’s oesophagus with early neoplasia in a cohort of 169 patients. Gut. 2010 Sep. 59 (9):1169-77. [Medline].
Chung A, Bourke MJ, Hourigan LF, Lim G, Moss A, Williams SJ, et al. Complete Barrett’s excision by stepwise endoscopic resection in short-segment disease: long term outcomes and predictors of stricture. Endoscopy. 2011 Dec. 43 (12):1025-32. [Medline].
Miyamoto S, Muto M, Hamamoto Y, Boku N, Ohtsu A, Baba S. A new technique for endoscopic mucosal resection with an insulated-tip electrosurgical knife improves the completeness of resection of intramucosal gastric neoplasms. Gastrointest Endosc. 2002 Apr. 55(4):576-81. [Medline].
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
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
Disclosure: Nothing to disclose.
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.
Endoscopic Mucosal Resection (EMR)
Research & References of Endoscopic Mucosal Resection (EMR)|A&C Accounting And Tax Services