Endoscopy 2005; 37(6): 570-578
DOI: 10.1055/s-2005-861352
© Georg Thieme Verlag KG Stuttgart · New York

Update on the Paris Classification of Superficial Neoplastic Lesions in the Digestive Tract

Endoscopic Classification Review Group
Further Information

Publication History

Publication Date:
03 June 2005 (online)

Background and Study Aims: Neoplastic lesions in the digestive-tract mucosa are termed “superficial” when the depth of invasion is limited to the mucosa and submucosa. The endoscopic appearance has a predictive value for invasion into the submucosa, which is critical for the risk of nodal metastases.
Materials and Methods: The endoscopic morphology of superficial lesions can be assessed with a standard video endoscope after spraying of a dye - an iodine-potassium iodide solution for the stratified squamous epithelium, or an indigo carmine solution for the columnar epithelium. In 2002, a workshop was held in Paris to explore the relevance of the Japanese classification. The conclusions were revised in 2003 in Osaka in relation to the definition of the subtypes used in endoscopy and the evaluation of the depth of invasion into the submucosa. In Japan, the description of advanced cancer in the digestive-tract mucosa using types 1 - 4 is supplemented by a type 0 when the endoscopic appearance is that of a superficial lesion. Type 0 is divided into three categories: protruding (0 - I), nonprotruding and nonexcavated (0 - II), and excavated (0 - III). Type 0 - II lesions are then subdivided into slightly elevated (IIa), flat (IIb), or depressed (IIc). Nonprotruding depressed lesions are associated with a higher risk of submucosal invasion. After endoscopic resection, invasion into the submucosa is an important criterion for the necessity of additional surgical resection. Micrometer analysis of the depth of invasion in the specimen is more precise, and distinct cut-off limits have been established in the esophagus, stomach, and large bowel.
Conclusions: The morphology of superficial and nonprotruding neoplastic lesions is relevant to the prognosis. Following endoscopic detection, the lesions are analyzed using chromoendoscopy and assigned a subtype of the type 0 classification. The choice between endoscopic or surgical treatment is based on this description.


  • 1 Schlemper R J, Riddell R H, Kato Y. et al . The Vienna classification of gastrointestinal epithelial neoplasia.  Gut. 2000;  47 251-255
  • 2 Dixon M F. Gastrointestinal epithelial neoplasia: Vienna revisited.  Gut. 2002;  51 130-131
  • 3 The Paris Endoscopic Classification of Superficial Neoplastic Lesions . Esophagus, stomach, and colon.  Gastrointest Endosc. 2003;  58 (Suppl 6) S3-S43
  • 4 Ormsby A H, Vaezi M F, Richter J E. et al . Cytokeratin immunoreactivity patterns in the diagnosis of short segment Barrett’s esophagus.  Gastroenterology. 2000;  119 683-690
  • 5 Mohammed I A, Streutker C J, Riddell R H. et al . Utilization of cytokeratins 7 and 20 does not differentiate between Barrett’s esophagus and gastric cardiac intestinal metaplasia.  Mod Pathol. 2002;  15 611-616
  • 6 Tsukuma H, Oshima A, Narahara H. et al . Natural history of early gastric cancer: a non-concurrent long term follow up study.  Gut. 2000;  47 618-621
  • 7 Winawer S J, Zauber A G, O’Brien M J. et al . The National Polyp Study: design, methods, and characteristics of patients with newly diagnosed polyps. The National Polyp Study Workgroup.  Cancer. 1992;  70 1236-1245
  • 8 Inoue H, Rey J F, Lightdale C. Lugol chromoendoscopy for esophageal squamous cell cancer.  Endoscopy. 2001;  33 75-79
  • 9 Kudo S, Kashida H, Tamura S. et al . The problem of “flat” colonic adenoma.  Gastrointest Endosc Clin N Am. 1997;  7 87-98
  • 10 Jaramillo E, Watanabe M, Slezak P. et al . Flat neoplastic lesions of the colon and rectum detected by high resolution video-endoscopy and chromoscopy.  Gastrointest Endosc. 1995;  42 114-122
  • 11 Canto M I, Setrakian S, Willis J E. et al . Methylene blue staining of dysplastic and nondysplastic Barrett’s esophagus: an in vivo and ex vivo study.  Endoscopy. 2001;  33 391-400
  • 12 Kiesslich R, Hahn M, Herrmann G. et al . Screening for specialized columnar epithelium with methylene blue: chromoendoscopy in patients with Barrett’s esophagus and a normal control group.  Gastrointest Endosc. 2001;  53 47-52
  • 13 Sharma P, Topalovski M, Mayo M S. et al . Methylene blue chromoendoscopy for detection of short-segment Barrett’s esophagus.  Gastrointest Endosc. 2001;  54 289-293
  • 14 Lambert R, Rey J F, Sankaranarayanan R. Magnification and chromoscopy with the acetic acid test.  Endoscopy. 2003;  35 437-445
  • 15 Hurlstone D P, Cross S S, Adam I. et al . Efficacy of high magnification chromoscopic colonoscopy for the diagnosis of neoplasia in flat and depressed lesions of the colorectum: a prospective analysis.  Gut.. 2004;  53 284-290
  • 16 Inoue H, Kumagai Y, Yoshida T. et al . High magnification endoscopic diagnosis of the superficial esophageal cancer.  Dig Endosc. 2000;  12 (Suppl) S32-S35
  • 17 Yao K, Oishi T. Microgastroscopic findings of mucosal microvascular architecture as visualized by magnifying endoscopy.  Dig Endosc. 2001;  13 (Suppl) S27-S33
  • 18 Tobita K. Study on minute surface structures of the depressed-type early gastric cancer with magnifying endoscopy.  Dig Endosc. 2001;  13 121-126
  • 19 Kumagai Y, Inoue H, Nagai K. et al . Magnifying endoscopy, stereoscopic microscopy, and the microvascular architecture of superficial esophageal carcinoma.  Endoscopy. 2002;  34 369-375
  • 20 Guelrud M, Herrera I, Essenfeld H. et al . Enhanced magnification endoscopy: a new technique to identify specialized metaplasia in Barrett’s esophagus.  Gastrointest Endosc. 2001;  53 559-565
  • 21 Endo T, Awakawa T, Takahashi H. et al . Classification of Barrett’s epithelium by magnifying endoscopy.  Gastrointest Endosc. 2002;  55 641-647
  • 22 Sharma P, Weston A P, Topalovski M. et al . Magnification chromoendoscopy for the detection of intestinal metaplasia and dysplasia in Barrett’s oesophagus.  Gut. 2003;  52 24-27
  • 23 Kudo S, Kashida H, Tamura T. et al . Colonoscopic diagnosis and management of non polypoid early colorectal cancer.  World J Surg. 2000;  24 1081-1090
  • 24 Hurlstone D P, Fujii T, Lobo A J. Early detection of colorectal cancer using high-magnification chromoscopic colonoscopy.  Br J Surg. 2002;  89 272-282
  • 25 Kato S, Fujii T, Koba I. et al . Assessment of colorectal lesions using magnifying colonoscopy and mucosal dye spraying: can significant lesions be distinguished?.  Endoscopy. 2001;  33 306-310
  • 26 Konishi K, Kaneko K, Kurahashi T. A comparison of magnifying and nonmagnifying colonoscopy for diagnosis of colorectal polyps: a prospective study.  Gastrointest Endosc. 2003;  57 48-53
  • 27 Kudo S, Rubio C A, Teixeira C R. et al . Pit pattern in colorectal neoplasia: endoscopic magnifying view.  Endoscopy. 2001;  33 367-373
  • 28 Morita T, Tamura S, Miyasaki J. et al . Evaluation of endoscopic and histopathological features of serrated adenoma of the colon.  Endoscopy. 2001;  33 761-765
  • 29 Matsumoto T, Mizuno M, Shimizu M. et al . Serrated adenoma of the colorectum: colonoscopic and histologic features.  Gastrointest Endosc. 1999;  49 736-742
  • 30 Japanese Gastric Cancer Association . Japanese classification of gastric carcinoma: 2nd English edition.  Gastric Cancer. 1998;  1 10-24
  • 31 Japanese Society for Esophageal Diseases .Guidelines for the clinical and pathologic studies on carcinoma of the esophagus. 9th ed. Tokyo; Kanehara 1999
  • 32 Watanabe H, Komukai S, Ajioka Y. et al . Histopathology of m3 and sm1 invasive squamous cell carcinoma of the esophagus, with special reference to endoscopic resection [in Japanese].  Stomach Intest. 1998;  33 1001-1009
  • 33 Kobayashi M, Watanabe H, Maeo S. et al . Correlation of histological atypia and cancer-sprouting with vascular permeation and lymph nodal metastasis by our new histological classification of submucosal invasion by colorectal carcinomas [in Japanese].  Stomach Intest. 1994;  29 1151-1160
  • 34 Yokoyama J, Ajioka Y, Watanabe H. et al . Lymph node metastasis and micrometastasis of submucosal invasive colorectal carcinoma: an indicator of the curative potential of endoscopic treatment.  Acta Med Biol. 2002;  50 1-8
  • 35 Egashira Y, Yoshida T, Hirata I. et al . Analysis of pathological risk factors for lymph node metastasis of submucosal invasive colon cancer.  Mod Pathol. 2004;  17 503-511
  • 36 Ueno H, Mochizuki H, Hashiguchi Y. et al . Risk factors for an adverse outcome in early invasive colorectal carcinoma.  Gastroenterology. 2004;  127 385-394
  • 37 Watanabe H, Tada T, Iwafuchi M. et al . New definition and macroscopic characteristics of early carcinoma of the esophagus.  Stomach Intest. 1990;  25 1075-1086
  • 38 Kodama M, Kakegawa T. Treatment of superficial cancer of the esophagus: a summary of responses to a questionnaire on superficial cancer of the esophagus in Japan.  Surgery. 1998;  123 432-439
  • 39 Ell C, May A, Gossner L. et al . Endoscopic mucosal resection of early cancer and high-grade dysplasia in Barrett’s esophagus.  Gastroenterology. 2000;  18 670-677
  • 40 Tajima Y, Nakanishi Y, Yoshino T. et al . Clinicopathological study of early adenocarcinoma of the gastric cardia: comparison with early adenocarcinoma of the distal stomach and esophagus.  Oncology. 2001;  61 1-9
  • 41 Park D I, Rhee P L, Kim J E. et al . Factors suggesting malignant transformation of gastric adenoma: univariate and multivariate analysis.  Endoscopy. 2001;  33 501-506
  • 42 National Report of the Group Medical examination for digestive cancer in 1999 [in Japanese] . .  J Gastroenterol Mass Surv. 2002;  40 57-76
  • 43 Hosokawa O, Tsuda S, Kidani E. et al . Diagnosis of gastric cancer up to three years after negative upper gastrointestinal endoscopy.  Endoscopy. 1998;  30 669-674
  • 44 Rex D K, Cummings O W, Helper D J. et al . 5-year incidence of adenomas after negative colonoscopy in asymptomatic average-risk persons.  Gastroenterology. 1996;  11 1178-1181
  • 45 Winawer S J, Zauber A G, Ho M N. et al . Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup.  N Engl J Med. 1993;  329 1977-1981
  • 46 Gorski T F, Rosen L, Riether R. et al . Colorectal cancer after surveillance colonoscopy: false-negative examination or fast growth?.  Dis Colon Rectum. 1999;  42 877-880
  • 47 Bressler B, Paszat L F, Vinden C. et al . Colonoscopic miss rates for right-sided colon cancer: a population-based analysis.  Gastroenterology. 2004;  127 452-456
  • 48 Burgart L. Colorectal polyps and other precursor lesions: need for an expanded view.  Gastroenterol Clin North Am. 2002;  31 959-970
  • 49 Jass J R. Histopathology of early colorectal cancer.  World J Surg. 2000;  24 1016-1021
  • 50 George S M, Makinen M J, Jernvall P. et al . Classification of advanced colorectal carcinomas by tumor edge morphology: evidence for different pathogenesis and significance of polypoid and nonpolypoid tumors.  Cancer. 2000;  89 1901-1909
  • 51 Tanaka S, Yoshida S, Chayama K. Clinical usefulness of high frequency ultrasound probes for new invasion depth diagnosis in submucosal colorectal carcinoma.  Dig Endosc. 2004;  16 (Suppl 2) S161-S164

R. Lambert, M. D., F.R.C.P.

International Agency for Research on Cancer

150, cours Albert Thomas · Lyon 69372, Cedex 08 · France

Fax: +33-4-72 73 86 50

Email: lambert@iarc.fr