The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon November 30 to December 1, 2002 Participants in the Paris Workshop Paris, France An international group of endoscopists, surgeons, type 0 - superficial polypoid, flat/depressed, or and pathologists gathered in Paris for an inten- excavated tumors sive workshop designed to explore the utility and type 1 - polypoid carcinomas, usually attached on clinical relevance of the Japanese endoscopic clas- a wide base sification of superficial neoplastic lesions of the GI type 2 - ulcerated carcinomas with sharply de- tract. This report summarizes the conclusions of the marcated and raised margins workshop and proposes a general framework for the type 3 - ulcerated, infiltrating carcinomas without endoscopic classification of superficial lesions of definite limits the esophagus, stomach, and colon. The clinical rele- type 4 - nonulcerated, diffusely infiltrating carci- vance of this classification is demonstrated in tables nomas that show the relative proportion of each subtype in type 5 - unclassifiable advanced carcinomas the esophagus, stomach, and colon, assessing the In summary, the macroscopic appearance of risk of submucosal invasion and the risk of lymph gastric cancer is distributed in 6 types (0-5) in the node metastases. JGCA classification. Type 0 with its subtypes adapted In the esophagus, stomach, and colon, neoplastic to endoscopic appearance includes both noninvasive lesions of the digestive tract are called ‘‘superficial’’ at neoplasia and cancer, which can be confirmed by endoscopy when the endoscopic appearance suggests pathologic analysis. The classification of gastric either a small cancer or a noninvasive neoplastic ‘‘superficial’’ neoplasia was promptly applied to lesion (dysplasia/adenoma). If invasive, ‘‘superficial’’ esophageal tumors,4 and later, when the incidence tumors correspond to the T1 stage of the TNM of colorectal cancer increased in Japan, to large bowel classification, in which invasion is limited to the tumors as well. mucosa and submucosa. ‘‘Superficial’’ tumors are Many endoscopists, particularly in the West, nonobstructive, usually are asymptomatic, and considered the Japanese classification, with its often are detected as an incidental finding or by numerous divisions for esophagus, stomach, and screening. colon, to be a ‘‘botanical hobby,’’ too complex for In Japan, neoplastic lesions of the stomach with practical use. Western endoscopists tend to base a ‘‘superficial’’ endoscopic appearance are classified treatment decisions largely on the size and the as subtypes of ‘‘type 0.’’1,2 The term ‘‘type 0’’ was location of the tumor and on the histology of biopsy chosen to distinguish the classification of ‘‘super- specimens. However, Japanese endoscopists have ficial’’ lesions from the Borrmann classification, found that the endoscopic classification of a lesion can proposed in 1926 for ‘‘advanced’’ gastric tumors, be an important determinant of when endoscopic which included types 1 to 4.3 Within type 0, there therapy should be applied. In choosing therapy, are polypoid and non-polypoid subtypes. The non- endoscopic appearance may be supplemented by polypoid subtypes include lesions with a small other endoscopic criteria, including EUS and EMR, variation of the surface (slightly elevated, flat, and to evaluate lifting of the lesion during endoscopy and slightly depressed) and excavated lesions. The to obtain a large pathology specimen. In patients at Japanese Gastric Cancer Association (JGCA) also increased risk for surgery, EMR may be the primary added a type 5 for unclassifiable advanced tumors. treatment, supplemented as needed by ablation The complete modification for gastric tumors treatments, such as electrocoagulation or photody- becomes: namic therapy. Skepticism of the value of endoscopic classification of superficial neoplastic lesions has been further Copyright Ó 2003 by the American Society for Gastrointestinal encouraged by East/West differences in pathology Endoscopy 0016-5107/2003/$30.00 + 0 classification of intramucosal neoplasia. The recent 5 PII: S0016-5107(03)02159-X Vienna classification has, to some extent, resolved VOLUME 58, NO. 6 (SUPPL), 2003 GASTROINTESTINAL ENDOSCOPY S3 Paris Workshop Participants The Paris endoscopic classification of superficial neoplastic lesions Table 1. Revised Vienna classification of epithelial polyp-cancer sequence established by Muto, Bussey, neoplasla for esophagus, stomach, and colon5,13 and Morson in 19756 is still valid. Chromoendoscopy Negative for IEN is much less useful for polypoid than for non-polypoid Indefinite for IEN lesions, and detailed endoscopic analyses of the Low-grade IEN morphology of a polyp are less helpful in the Adenoma/dysplasia prediction of invasive malignancy than is the gross High-grade neoplasia (intraepithelial evaluation of size or expansion of the stalk. There- or intramucosal) Adenoma/dysplasia (4-1) fore, routine chromoendoscopy at colonoscopy car- Noninvasive carcinoma (4-2) ried out to detect adenomas often is considered to 7 Suspicious for invasive carcinoma (4-3) have little value in the West. Consequently, small Intramucosal carcinoma (lamina (4-4) non-polypoid (flat) adenomas (noninvasive neopla- propria invasion) sia) or even carcinomas may go undetected. Submucosal carcinoma The East and West points of view are now much IEN, Intraepithelial neoplasia. closer. Asian, European, and American patholo- gists5,8-10 proposed a consensus histopathologic clas- these differences in the use of the terminology of sification in 3 major groups for intramucosal dysplasia, adenoma, early cancer, and advanced neoplasia: noninvasive low grade, noninvasive high cancer. Feedback from the analysis of the pathology grade, and cancer with invasion of the lamina propria specimen is critical to teaching endoscopic diagnosis (Table 1). This consensus, adopted in Vienna, has in Japan and leads to continuing education that helps been published in a recent supplement of Gastroin- move endoscopists along the learning curve. From testinal Endoscopy.11 Merging endoscopic and path- a Japanese perspective, Western endoscopists tend ologic terminologies will use the potential to lack attention to endoscopic detail in obtaining advantages of each of them. The Vienna classifica- images and descriptions of superficial lesions. While tion, adopted (in part) in the recent World Health this may be, in part, because of differences in Organization (WHO) classification of digestive tu- endoscopes and ancillary techniques such as chro- mors,12 has been slightly modified, with improved moendoscopy, there is the sense that Western endo- agreement scores and therapeutic relevance.13-15 scopists do not appreciate and underuse precise With respect to macroscopic morphology, the endoscopic description, which can be of great value existence of small, but potentially malignant, non- in assessing depth of invasion and in deciding polypoid lesions in the large bowel is now acknowl- treatment. edged; however, the importance of their role as The distinct East and West points of view on the precursors of advanced cancer is still unclear in importance of endoscopic description developed Western populations.7,16,17 Last, but not least, the during the second half of the twentieth century. In increasing incidence of neoplasia in Barrett’s esoph- Japan, the high burden of gastric cancer encouraged agus (where non-polypoid precursors play a major early detection, at first with endoscopy and then with role) has stimulated the interest of Western special- double contrast radiology. Because flat precursors ists in improving the detection, description, and play an almost exclusive role in gastric carcinogen- classification of non-polypoid dysplastic lesions. esis, early endoscopic detection required extreme rigor during the endoscopic procedure. Additional techniques, such as chromoendoscopy and magni- TERMINOLOGY AND DEFINITIONS fication, also were developed to help identify subtle Superficial neoplasia at endoscopy lesions. Meanwhile, improved gastroscopes were A neoplastic lesion is called ‘‘superficial’’ when its made in Japan. These instruments, with improved endoscopic appearance suggests that the depth of optics, were initially tested at leading Japanese penetration in the digestive wall is not more than into medical centers. the submucosa, i.e., there is no infiltration of the In Japan, the approach to early detection of muscularis propria. In the esophagus, neoplasia neoplastic lesions in the esophagus and later in the develops in the stratified squamous epithelium or in colon continued along similar lines to those of gastric a metaplastic columnar mucosa (Barrett’s esopha- cancer. Some highly skilled endoscopists limit their gus). Distal to the esophagus, neoplasia develops in practice to a single organ. At the same time the the columnar mucosa in the stomach. A distinction is Japanese were concentrating on gastric carcinoma, made between tumors located at the cardia and many other countries were emphasizing the pre- tumors distal to the cardia (sub-cardiac tumors). vention of colorectal cancer. Polypoid precursors play Tumors at the esophagogastric junction include a much greater role in large bowel neoplasia, and the adenocarcinoma in the distal esophagus and at the S4 GASTROINTESTINAL ENDOSCOPY VOLUME 58, NO. 6 (SUPPL), 2003 The Paris endoscopic classification of superficial neoplastic lesions Paris Workshop Participants Table 2. Neoplastic lesions with ‘‘superficial’’ morphology Diagram 1. Schematic representation