Endoscopy 2001; 33(8): 709-718
DOI: 10.1055/s-2001-16224
Review

© Georg Thieme Verlag Stuttgart · New York

Endoscopic Mucosal Resection

B. J. Rembacken 1 , T. Gotoda 2 , T. Fujii 2 , A. T. R. Axon 1
  • 1 Centre for Digestive Diseases, The General Infirmary at Leeds, United Kingdom
  • 2 National Cancer Centre, Tokyo, Japan
Further Information

Publication History

Publication Date:
31 December 2001 (online)

We are now finding more malignancies in their early stages than previously. Attempts to ablate these lesions are difficult and do not provide the histological information required to decide on further treatment. Surgery is difficult to justify, as only a minority of lesions are associated with lymph node metastases and lesions may not become clinically relevant within the lifetime of an elderly patient. Endoscopic mucosal resection allows cancers to be resected at minimal cost, morbidity and mortality. It is also the most reliable investigation when assessing lesions which are suspicious for containing early cancer. After endoscopic removal, histological assessment of depth of penetration and a search for invasion into lymphatics or venules allows the risk of microscopic lymph node metastases to be predicted. The risk of developing metastatic disease can then be balanced against the risks of surgery in view of the patient’s age and health.

References

  • 1 Earlam R, Cunha-Melo J R. Oesophageal squamous cell carcinoma: I. A critical review of surgery.  Br J Surg. 1980;  67 381-390
  • 2 Earlam R, Cunha-Melo J R. Oesophageal squamous cell carcinoma: II. A critical review of radiotherapy.  Br J Surg. 1980;  67 457-461
  • 3 Everett S M, Axon A TR. Early gastric cancer: disease or pseudo-disease.  Lancet. 1998;  351 1350-1352
  • 4 Sue-Ling H M, Martin I, Griffith J, et al. Early gastric cancer: 46 cases in one surgical department.  Gut. 1992;  33 1318-1322
  • 5 Yamazaki H, Oshima A, Murakami R, et al. A long-term follow up study of patients with gastric cancer detected by mass screening.  Cancer. 1989;  63 613-617
  • 6 Moreaux J, Catala M. Carcinoma of the colon: long-term survival and prognosis after surgical treatment in a series of 798 patients.  World J Surg. 1987;  11 804-809
  • 7 Kato H, Tachimori Y, Watanabe H, et al. Superficial esophageal carcinoma. Surgical treatment and the results.  Cancer. 1990;  66 2319-2323
  • 8 Japanese Society for Esophageal Diseases . Guidelines for clinical and pathologic studies on carcinoma of the esophagus.  Jpn J Surg. 1976;  6 69-78
  • 9 Murakami T. Pathomorphological diagnosis. Definition and gross classification of early gastric cancer.  Gann Monogr Cancer Res. 1971;  11 53-55
  • 10 Japanese Society for Cancer of the Colon and Rectum .General rules for clinical and pathological studies on cancer of the colon, rectum and anus. Japanese Society for Cancer of the Colon and Rectum. Tokyo; November 1998 6th ed.
  • 11 Medical Examinations for Digestive Cancer in 1995 Group . National Report (in Japanese).  J Gastroenterol Mass Surv. 1998;  130 251-269
  • 12 Yoshinaka H, Shimazu H, Fukumoto T, Baba M. Superficial esophageal carcinoma: a clinicopathological review of 59 cases.  Am J Gastroenterol. 1991;  86 1413-1418
  • 13 Shimuzu S, Tada M, Kawai K. Early gastric cancer: its surveillance and natural course.  Endoscopy. 1995;  27 27-31
  • 14 Ballantyne K C, Morris D L, Jones J A, et al. Accuracy of identification of early gastric cancer.  Br J Surg. 1987;  74 618-619
  • 15 Suvakovic Z, Bramble M G, Jones R, et al. Improving the detection rate of early gastric cancer requires more than open access endoscopy: a five year study.  Gut. 1997;  41 308-313
  • 16 Shida H, Ban K, Matsumoto M, Matsuda K, et al. Asymptomatic colorectal cancer detected by screening.  Dis Colon Rectum. 1996;  39 1130-1135
  • 17 Kitamura K, Taniguchi H, Yamaguchi T, et al. Clinical outcome of surgical treatment for invasive early colorectal cancer in Japan.  Hepatogastroenterology. 1997;  44 108-115
  • 18 Rembacken B J, Fujii T, Cairns A, et al. Flat and depressed colonic neoplasms: a prospective study of 1000 colonoscopies in the UK.  Lancet. 2000;  355 1211-1214
  • 19 Jaramillo E, Watanabe M, Slezak P, Rubio C. Flat neoplastic lesions of the colon and rectum detected by high-resolution video endoscopy and chromoscopy.  Gastrointest Endosc. 1995;  42 114-122
  • 20 Misumi A, Harada K, Murakami A. Role of Lugol’s dye endoscopy in the diagnosis of early esophageal cancer.  Endoscopy. 1990;  22 12-16
  • 21 Fennerty M B, Sampliner R E, McGee D, et al. Intestinal metaplasia of the stomach: identification by a selective mucosal staining technique.  Gastrointest Endosc. 1992;  38 696-698
  • 22 Canto M IF, Setrakian S, Willis J, et al. Methylene blue-directed biopsies improve detection of intestinal metaplasia and dysplasia in Barrett’s oesophagus.  Gastrointest Endosc. 2000;  51 560-568
  • 23 Kato H, Tachimori Y, Mizobuchi S, et al. Cervical, mediastinal and abdominal lymph node dissection (three-field dissection) for superficial carcinoma of the thoracic esophagus.  Cancer. 1993;  72 2879-2882
  • 24 Roth J A, Putman J B. Surgery for cancer of the esophagus.  Semin Oncol. 1994;  4 453-461
  • 25 Rusch V W, Levine D S, Haggitt R, Reid B J. The management of high grade dysplasia and early cancer in Barrett’s esophagus. A multidisciplinary problem.  Cancer. 1994;  74 1225-1229
  • 26 Reid B J, Weinstein W M, Lewin K J, et al. Endoscopic biopsy can detect high-grade dysplasia or early adenocarcinoma in Barrett’s esophagus without grossly recognizable neoplastic lesions.  Gastroenterology. 1988;  94 81-90
  • 27 Pera M, Trastek V F, Carpenter H A, et al. Barrett’s esophagus with high-grade dysplasia: an indication for esophagectomy?.  Ann Thorac Surg. 1992;  54 199-204
  • 28 Rice T W, Falk G W, Achkar E, Petras R E. Surgical management of high-grade dysplasia in Barrett’s esophagus.  Am J Gastroenterol. 1993;  88 1832-1836
  • 29 Moreaux J, Bougaran J. Early gastric cancer. A 25-year surgical experience.  Ann Surg. 1993;  217 347-355
  • 30 Bonenkamp J J, Hermans J, Sasako M, van de Veelde C JH. Extended lymph-node dissection for gastric cancer.  N Engl J Med. 1999;  340 908-914
  • 31 Royal College of Surgeons of England and Association of Coloproctology of Great Britain and Ireland .Guidelines for the management of colorectal cancer.  . London; Royal College of Surgeons of England and Association of Coloproctology of Great Britain and Ireland, 1996
  • 32 Sasako M. Risk factors for surgical treatment in the Dutch gastric cancer trial.  Br J Surg. 1997;  84 1567-1571
  • 33 Davies J, Johnston D, Sue-Ling H M, et al. Total or subtotal gastrectomy for gastric carcinoma? A study of quality of life.  World J Surg. 1998;  22 1048-1055
  • 34 Jentschura D, Winkler M, Strohmeier N, et al. Quality-of-life after curative surgery for gastric cancer: a comparison between total gastrectomy and subtotal gastrectomy resection.  Hepatogastroenterology. 1997;  44 1137-1142
  • 35 Jatzko G R, Lisborg P H, Denk H, et al. A 10-year experience with Japanese-type lymph node dissection for gastric cancer outside of Japan.  Cancer. 1995;  76 1302
  • 36 Cuschieri A, Fayers P, Fielding J, et al. Postoperative morbidity and mortality after D1 and D2 resection for gastric cancer: preliminary results of the MRC randomised controlled surgical trial.  Lancet. 1996;  347 995-999
  • 37 Collard J M, Otte J B, Reynaert M, Kestens P J. Quality of life three years or more after esophagectomy for cancer.  J Thorac Cardiovasc Surg. 1992;  104 391-394
  • 38 Baba M, Aikou T, Natsugoe S, et al. Appraisal of ten-year survival following esophagectomy for carcinoma of the esophagus with emphasis on quality of life.  World J Surg. 1997;  21 282-285
  • 39 Habu H, Kono M, Tani M, et al. Operative procedures and quality of postoperative life in patients with gastric cancer (In Japanese with English abstract).  Jpn J Gastroenterol Surg. 1990;  23 953-955
  • 40 Svedlund J, Sullivan M, Liedman B, Lundell L. Long term consequences of gastrectomy for patient’s quality of life: the impact of reconstructive techniques.  Am J Gastroenterol. 1999;  94 438-445
  • 41 Davies J, Johnston D, Sue-Ling H. Total or subtotal gastrectomy for gastric carcinoma? A study of quality of life.  World J Surg. 1998;  22 1048-1055
  • 42 Hamilton S R, Smith R RL. The relationship between columnar epithelial dysplasia and invasive adenocarcinoma arising in Barrett’s esophagus.  Am J Clin Pathol. 1987;  87 301-312
  • 43 Atkinson M, Iftikhar S Y, James P D, et al. The early diagnosis of oesophageal adenocarcinoma by endoscopic screening.  Eur J Cancer Prev. 1992;  1 327-330
  • 44 Levine D S, Haggitt R C, Blount P L, et al. An endoscopic biopsy protocol can differentiate high-grade dysplasia from early adenocarcinoma in Barrett’s esophagus.  Gastroenterology. 1993;  105 40-50
  • 45 De Baecque C, Potet F, Molas G, et al. Superficial adenocarcinoma of the oesophagus arising in Barrett’s mucosa with dysplasia: a clinicopathological study of 12 patients.  Histopathology. 1990;  16 213-220
  • 46 Schnell T, Sontag S, Chejfec G, et al. High grade dysplasia in Barrett’s esophagus: a report of experience in 43 patients (abstract).  Gastroenterology. 1989;  96 Suppl A452
  • 47 TsukumA H, Mishima T, Oshima A. Prospective study of “early” gastric cancer.  J Cancer. 1983;  31 421-426
  • 48 Tsukuma H, Oshima A, Narahar H, Morii T. Natural history of early gastric cancer: a non-concurrent, long term, follow up study.  Gut. 2000;  47 618-621
  • 49 Morson B. The polyp-cancer sequence in the large bowel.  Proc R Soc Med. 1974;  67 451-457
  • 50 Endo M, Yoshino K, Takeshita K, et al. Analysis of 1125 cases of early esophageal carcinoma in Japan.  Dis Esophagus. 1991;  2 71-76
  • 51 Bonavina L, Ruol A, Ancona E, Peracchia A. Prognosis of early squamous cell carcinoma of the esophagus after surgical therapy.  Dis Esophagus. 1997;  10 162-164
  • 52 Tajima Y, Nakanishi Y, Tachimori Y, et al. Histopathologic findings predicting lymph node metastases and prognosis of patients with superficial esophageal carcinoma.  Cancer. 2000;  88 1285-1293
  • 53 Okajima K, Yamada S, Isozaki H, et al. Some considerations on endoscopic radical resection of early gastric cancer (English abstract).  Stomach Intestine. 1991;  26 371-377
  • 54 Perri F, Iuliano R, Valente G, et al. Minute and small early gastric cancers in a Western population: a clinicopathologic study on 80 cases.  Dig Dis Sci. 1995;  41 475-480
  • 55 Baba H, Maehara Y, Okuyama T, et al. Lymph node metastases and macroscopic features in early gastric cancer.  Hepato-gastroenterology. 1994;  41 380-383
  • 56 Maehara Y, Orita H, Okuyama T, et al. Predictors of lymph node metastasis in early gastric cancer.  Br J Surg. 1992;  79 245-247
  • 57 Endo M, Habu H. Clinical studies of early gastric cancer.  Hepatogastroenterology. 1990;  37 408-410
  • 58 Kim J P, Hur Y S, Yang H K. Lymph node metastases as a significant prognostic factor in early gastric cancer: analysis of 1136 early gastric cancers.  Ann Surg Oncol. 1995;  2 308-313
  • 59 Kurihara N, Kubota T, Otani Y, et al. Lymph node metastasis of early gastric cancer with submucosal invasion.  Br J Surg. 1998;  85 835-839
  • 60 Gotoda T, Sasako M, Ono H, et al. An evaluation of the necessity of gastrectomy with lymph node dissection for patients with submucosal invasive gastric cancer.  Br J Surg. 2001;  88 444-449
  • 61 Wilcox G M, Anderson P B, Colacchio A. Early invasive carcinoma in colonic polyps. A review of the literature with emphasis on the assessment of the risk of metastasis.  Cancer. 1986;  57 60-71
  • 62 Kikuchi R, Takano M, Takagi K, et al. Management of early invasive colorectal cancer. Risks of recurrence and clinical guidelines.  Dis Colon Rectum. 1995;  38 1286-1295
  • 63 Fujii T. Personal observation. 
  • 64 Kodaira S, Yao T, Nakamura K, et al. The incidence of lymph node metastais of submucosal colorectal carcinomas in each submucosal invasion depth degree. Results from a questionnaire survey (In Japanese with English abstract).  Stomach Intestine. 1994;  29 1137-1142
  • 65 Tanaka S, Haruma K, Teixeira C R, et al.. Endoscopic treatment of submucosal invasive colorectal carcinoma with special reference to risk factors for lymph node metastasis.  J Gastroenterol. 1995;  30 710-717
  • 66 Aoki R, Tanaka S, Haruma K, et al. MUC-1 expression as a predictor of the curative endoscopic treatment of submucosally invasive colorectal carcinoma.  Dis Colon Rectum. 1998;  41 1262-1272
  • 67 Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer.  Endoscopy. 1993;  25 455-461
  • 68 Karita M, Tada M, Okita K, et al. Endoscopic therapy for early colon cancer: the strip biopsy resection technique.  Gastrointest Endosc. 1991;  37 128-132
  • 69 Yokota T, Sugihara K, Yoshida S. Endoscopic mucosal resection for colorectal neoplastic lesions.  Dis Colon Rectum. 1994;  37 1108-1111
  • 70 Nishi M, Ishihara S, Nakajima T, et al. Chronological changes of characteristics of early gastric cancer and therapy: experience in the Cancer Institute Hospital of Tokyo, 1950-1994.  J Cancer Res Clin Oncol. 1995;  121 535-541
  • 71 Hiki Y. Endoscopic mucosal resection (EMR) for early gastric cancer (In Japanese with English abstract).  Jpn J Surg. 1996;  97 273-278
  • 72 Nijhawan P K, Wang K K. Endoscopic mucosal resection for lesions with endoscopic features suggestive of malignancy and high-grade dysplasia within Barrett’s esophagus.  Gastrointest Endosc. 2000;  52 328-332
  • 73 Rösch T. Endosonographic staging of esophageal cancer: a review of literature results.  Gastrointest Endosc. 1995;  5 537-548
  • 74 Kurihara N, Kumai K, Otani Y, et al. The usefulness of a 20 MHz-sonoprobe for selection of surgical treatment for early gastric cancer.  Prog Dig Endosc. 1995;  47 69-72
  • 75 Yanai H, Noguchi T, Mizumachi S, et al. A blind comparison of the effectiveness of endoscopic ultrasonography and endoscopic staging in early gastric cancer.  Gut. 1999;  44 361-365
  • 76 Fujii T. Personal observation. 
  • 77 Tsuchiya A, Kikuchi Y, Ando Y, et al. Lymph node metastases in gastric cancer invading the submucosal layer.  Eur J Surg Oncol. 1995;  21 248-250
  • 78 Yasuda K, Shiraishi N, Suematsu T, et al. Rate of detection of lymph node metastasis is correlated with the depth of submucosal invasion in early stage gastric carcinoma.  Cancer. 1999;  85 2119-2123
  • 79 Nakano K, Yanagisawa A, Utsude T, et al. Limits of indication of endoscopic mucosal resection (EMR) for treatment of early gastric carcinoma of undifferentiated type - from a pathological viewpoint (In Japanese with English abstract).  Stomach Intestine. 1995;  30 1289-1294
  • 80 Gotoda T, Yanagisawa A, Sasako M, et al. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases in centres.  Gastric Cancer. 2000;  3 219-225
  • 81 Tanabe S. Koizumi W. Kokutou M, et al. Usefulness of endoscopic aspiration mucosectomy as compared with strip biopsy for the treatment of gastric mucosal cancer.  Gastrointest Endosc. 1999;  50 819-822
  • 82 Sadahiro S, Ishida H, Tokunaga N, et al. Experimental assessment of endoscopic mucosectomy with a cap-fitted panendoscope.  Endoscopy. 1998;  30 713-717
  • 83 Inoue H, Tani M, Nagai K, et al. Treatment of esophageal and gastric tumors.  Endoscopy. 1999;  31 47-55
  • 84 Makuuchi H, Kise Y, Shimada H, et al. Endoscopic mucosal resection for early gastric cancer.  Semin Surg Oncol. 1999;  17 108-116
  • 85 Inohue H, Takeshita K, Hori H, et al. Endoscopic mucosal resection with a cap-fitted panendoscope for esophagus, stomach and colon mucosal lesions.  Gastrointest Endosc. 1993;  39 58-62
  • 86 Oda I, Kondo H, Gotoda T, et al. Endoscopic diagnosis for multiple early gastric cancer (abstract). Proceedings of the Third International Gastric Cancer Congress, 1999 3
  • 87 Ono H, Kondo H, Gotoda T, et al. Endoscopic mucosal resection for treatment of early gastric cancer.  Gut. 2001;  48 225-229
  • 88 Uno Y, Munakata A. The non-lifting sign of invasive cancer.  Gastrointest Endosc. 1994;  40 485-489
  • 89 Inoue H, Kawano T, Tani M, et al. Endoscopic mucosal resection using a cap: techniques for use and preventing perforation.  Can J Gastroenterol. 1999;  13 477-480
  • 90 Kaneko E, Hanada H, Kasugai T, et al. The survey of gastrointestinal endoscopic complications in Japan (1993 - 1997, in Japanese).  Gastroenterol Endosc. 2000;  42 308-313
  • 91 Niwa H. Complications of colonoscopy - the results of a questionnaire from Japanese institutions.  Gastroenterol Endosc. 1979;  21 178-192
  • 92 Namiki M. Complications of endoscopic examination (in Japanese).  Gastroenterol Endosc. 1984;  26 2439-2455
  • 93 Kasugai E, Namiki M, Honda T, et al. Complications of endoscopic examinations - the results of multi-center analysis from 1983 to 1987 (in Japanese).  Gastroenterol Endosc. 1989;  31 2214-2229
  • 94 Kaneko E, Harada H, Kasugai T, Sakita T. The results of a multi-center analysis from 1988 - 1992 (in Japanese).  Gastroenterol Endosc. 1995;  37 642-652
  • 95 Tada M. One piece resection and piecemeal resection of early gastric cancer by strip biopsy (In Japanese with English abstract).  Tokyo; Igaku-Shoin 1998: 68-87
  • 96 Okamoto H, Tanaka S, Haruma K, et al. Japanese review of complications and measure by endoscopic treatment for colorectal tumor between 1989 - 1993 (in Japanese).  Hiroshimaigaku. 1996;  49 585-591
  • 97 Misumi A, Honmyo U. The present state of endoscopic mucosal resection for early gastric cancer (in Japanese).  Gastroenterol Endosc. 1998;  40 1947-1956
  • 98 Korenaga D, Orita H, Maekawa S, et al. Pathological appearance of the stomach after endoscopic mucosal resection for early gastric cancer.  Br J Surg. 1997;  84 1563-1566
  • 99 Gotoda T, Kondo H, Ono H, et al. A new endoscopic mucosal resection procedure using an insulation-tipped diathermic knife for rectal flat lesions.  Gastrointest Endosc. 1999;  50 560-563
  • 100 Ohmura K, Nagashima R, Takeda H, et al. Temporary stenting with metallic endoprosthesis for refractory esophageal stricture secondary to cylindrical resection of carcinoma.  Gastrointest Endosc. 1998;  48 214-217

B. Rembacken, M.D. 

Centre for Digestive Diseases
The General Infirmary at Leeds

Great George Street
Leeds LS1 3EX
United Kingdom


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Email: bjr@firstnet.co.uk