High-resolution endoscopy and early gastrointestinal cancer … dawn in the East

• Digital imaging - a revolution in endoscopy
• Endoscopy and patterns of tumor growth in the gastrointestinal mucosa
• Early detection of cancer and screening
• Endoscopic detection - a step-by-step methodology
• Step 1 - Cleanliness of the mucosal surface
• Step 2 - Detection of a suspect area
• Step 3 - Characterization of the lesion
• Step 4 - Classification of the lesion and treatment decisions
• References

Cancer in the esophagus, stomach, and large bowel accounted for 24 % of worldwide cancer mortality in 2002 [1]. This burden is expected to increase further as the world’s population ages. Prevention is based on early detection of potentially curable cancers and/or precursor conditions that have a significant risk of progression to malignancy. Early detection in the asymptomatic population can be achieved in: (a) people who comply with interventions proposed by health authorities (population-based screening); (b) people with a link to a particular health policy (e. g. occupational screening); and (c) people who contact their own doctor or private health check-up institutions (individual or ”opportunistic” screening). Factors that limit the benefit of early detection and treatment of neoplastic lesions include the degree of compliance with the selection procedure and compliance with recall for diagnosis and treatment in people with a positive test. The miss rate for small but potentially cancerous lesions is often responsible for interval cancers. There is also a danger of overdetection and overtreatment of lesions with a very low risk of progression to malignancy.

Digital imaging - a revolution in endoscopy

In the era of digital imaging, gastrointestinal endoscopy still maintains its gold-standard status for the early detection of neoplasia, in large part due to the Japanese capacity for innovation. In addition to improved mechanical properties and field of vision, the recent electronic video endoscopes reach the level of high-resolution endoscopy. The three principal reasons for this are (a) the increased density of pixels; (b) manipulation of the digital image processing; and (c) the modes and levels of magnification that can now be utilized.

The number of pixels is increased as a result of the miniaturization of the charge-coupled device (CCD). High resolution of the reconstituted image also depends on the processor and its coupling to a high-quality monitor: the higher number of lines available in the high-definition television (HDTV) standard is adapted to the increased pixel density of the CCD.

Image processing is made possible by digital technology. The incident photons hitting the tissue can be absorbed, reflected, or scattered. The modulation of specific frequencies of the reflected photons will increase the contrast between zones of the mucosa, showing up differences between the pits and ridges (structure enhancement), or in the densities of hemoglobin and microvessels (the adaptative index of hemoglobin) [2] [3].

In the narrow-band imaging (NBI) technique a special set of filters is interposed after the light source [4] [5] [6] [7] to restrict the incident light into two narrow bands of wavelengths (blue at 415 nm and green at 540 nm). The same bands are used in the two NBI systems that are available (Exera II and Lucera Spectrum; Olympus Medical Systems Corp., Tokyo, Japan), which only differ in the scanning mode they use for the reflected image (sequential vs. simultaneous). The selective reflection of the NBI light by the superficial layers of the mucosa improves the definition of the surface, while its selective absorption by hemoglobin enhances the contrast of the vascular network. The major contribution of NBI is therefore enhancement of the microvascular network of the normal and neoplastic mucosa [8] [9] [10]. The two reflected images from the mucosa, from the surface (415 nm) and from the deeper mucosa and submucosa (540 nm), are collected. The 415-nm image channel analyzes the fine surface architecture of the mucosa and the superficial capillary network; the 540-nm image channel analyzes the collecting vessels more in depth. In the final mixed image, the processor further enhances the contrast by reassigning the color channels: superficial and deep details are superimposed in a single image, enhancing the visibility of flat lesions and displaying subepithelial capillaries in brown and veins in the submucosa in cyan. Fujinon has recently proposed as an alternative to chromoscopy a procedure based on the computer reconstitution of virtual images at specific wavelengths (the ”Fuji Intelligent Chromo Endoscopy” or ”FICE” system, model EPX 4400; Fujinon Co., Omiya, Japan).

The magnifying system combines optical and electronic technologies to depict the architecture (pits and ridges) of the normal and abnormal epithelium in the esophagus [11] [12], stomach [13] [14], and colon [15] [16] [17] [18] [19]. The optical zoom (range × 60 to × 150) enlarges microstructures without loss in resolution; the macro objective lens is less powerful but easier to use and requires no distance adjustment. With the electronic zoom the resolution loss does not affect the practical examination if the image is processed in the HDTV standard. NBI is coupled with magnification, either with a macro objective lens (Olympus Evis Exera II) and the electronic zoom, or with an optical zoom (Olympus Evis Lucera Spectrum).

With magnification up to levels of × 1000, an approach to in-vivo cytology or histology is proposed with the Olympus endocytoscopy system or the Optiscan-Pentax confocal endoscope that uses laser light. These systems offer an approach to in-vivo cytology or histology but are not used in routine endoscopy [20] [21] [22].

Endoscopy and patterns of tumor growth in the gastrointestinal mucosa

Benign and malignant neoplastic lesions of the gastrointestinal mucosa are called ”superficial” when their appearance suggests that the depth of invasion is limited to the mucosa (m) or the submucosa (sm). In the stomach, the term ”early cancer” is also used to describe a superficial carcinoma (m or sm). In the gastrointestinal mucosa, the concept of progressive growth of a clone of neoplastic cells into a conspicuous polypoid lesion is now challenged: in the stomach, the usual morphology of early gastric cancer is flat; and in the colon, small, flat adenomas are common and progress either to polyps or to flat lesions. The flat (nonpolypoid) lesions remain superficial when they adopt a transverse model of growth; other lesions progress to invasive carcinoma in spite of their small size. It is thought that distinct molecular markers might control these differences in growth pattern.

During endoscopy, the diameter of a lesion is evaluated by comparing it with a standard (a graduated probe or biopsy forceps) placed on its side. The gross macroscopic appearance of the lesion is classified into subtypes of type 0 [23], as polypoid (0 - I), nonpolypoid (0 - II), or, rarely, excavated (0 - III). Polypoid lesions can be pedunculated (0 - Ip) or sessile (0 - Is). Nonpolypoid lesions are sligthly elevated (0 - IIa), completely flat (0 - IIb), or slightly depressed (0 - IIc). The proportion of nonpolypoid lesions is estimated to be 80 % in the esophagus, 95 % in the stomach, and 45 % in the colon [23]. The morphology of superficial lesions has prognostic significance, irrespective of the size of the lesion. The depressed type (0 - IIc), though rare, plays a significant role as a precursor of advanced cancer.

In Japan, the detection of early gastric cancer has developed from the beginning as a general strategy, using the gastrocamera, gastrophotofluorography, and the fiber-endoscope. From 1975 to 1978 the endoscopic description of early cancer focused on discolored (pale or red) areas in the mucosa, where minimal alterations of the surface could be revealed by chromoscopy [24] [25] [26] [27]. The same approach was adopted for the large bowel after the description of flat adenomas by Muto et al. in 1985 [28]. At first, the Japanese descriptions were treated with skepticism in the West. However, after similar findings were reported by Japanese clinicians in English and US populations, Western clinicians slowly began to acknowledge the role of nonpolypoid neoplastic lesions as precursors of cancer [29] [30] [31] [32] [33] [34]. The difference in the interpretation of an abnormal spot by Western and Eastern clinicians confirms the role of cognitive training in the adaptation of the eye to detection: etched in the long-term memory of Western endoscopists is the invariable image of a neoplastic lesion as a protruding abnormality, and flat, discolored spots are not recognized in the absence of a corresponding template in the brain linking the image to neoplasia [35]. There is no doubt that high-resolution endoscopy has proved to be a considerable help in developing the vision of Western endoscopists and in developing new cognitive templates. However, ”more“ is not necessarily ”better,“ and a large proportion of flat defects that are now visible on the surface of the mucosa have no clinical relevance. Discriminatory analysis is the only protection against overdetection and overtreatment.

Early detection of cancer and screening

Endoscopy is often the initial procedure for the early detection of gastrointestinal cancer in individual screening. Endoscopy is also proposed in organized screening for the small proportion of people who comply with a simpler filter test. Japan offers a good example of the concurrent impact of organized (population-based or occupational) and individual screening on the increased proportion of localized cancer, with improved prognosis in the stage distribution of detected tumors [36] (see [Table 1]).

Population-based screening, organized by the Japanese government, was instituted in 1983, the filter tests being gastrophotofluorography for stomach cancer and immunochemical fecal occult blood testing (1992) for colorectal cancer. The frequency of superficial cancer (m or sm) in cases detected by organized screening is high in Japan: in the national report on mass screening during 2002 [37], which includes data from population-based and from occupation-based interventions supported by industrial companies, the proportion of superficial cancer was 66.4 % for the stomach (4218 cases with pathology staging) and 64.4 % for the colon and rectum (3712 cases with pathology staging). On the other hand, the proportion of cancers detected by organized screening in Japan is low: 6969 cases of stomach cancer and 10 598 cases of colorectal cancer in 2003 (data from the Report on Health Center Activities and Health Services for the Aged [38]), this is a small proportion of the annual number of cases, estimated to be about 110 000 for stomach cancers and 95 000 for cancers of the colon and rectum [1]. The low yield results from successive and cumulative factors relating to compliance with screening.

The increasing trend toward early detection that has occurred during the last three decades in Japan strongly suggests that individual screening plays a role in early detection. Stomach cancer is a good example. Data from the Osaka Cancer Registry showed that the proportion of localized cancer, which consists of early cancer (m and sm) and advanced, lymph node-negative cancer, rose from 25 % in 1975 - 1977 to 50 % in 1993 - 1995 [38]. The proportion of localized stomach cancer is higher in the ten Japanese cancer registries (54 % in 2000) [39], than it is in the nine Surveillance, Epidemiology, and End Results (SEER) registries in the USA (24 % in 1995 - 2001). In a series of 1226 consecutive cases of early gastric cancer operated on at the National Cancer Center Hospital in Tokyo in the period 2001 - 2003 [40], the initial detection procedure was gastroscopy for 68.8 % of asymptomatic people and for 91.7 % of symptomatic people. In the same series, 64.3 % of patients were referred from outpatient clinics, 28.1 % from private health check-up units, and only 7.6 % from organized screening programs. The widespread acceptance of the guidelines on early detection explain the relatively high 5-year survival rate for gastric cancer at all stages that was observed in seven population-based registries (58 % in 1993 - 1996) [41].

Endoscopic detection - a step-by-step methodology

High resolution with image processing is not a substitute for careful exploration of the mucosa during endoscopy. A step-by-step method in the analysis of the lesion is even more important than before because more abnormalities are becoming visible; the risk of overtreatment of lesions with no clinical relevance is also increased.

Step 1 - Cleanliness of the mucosal surface

Any residual solid or liquid matter on the surface of the mucosa after incomplete bowel preparation can mask small, nonpolypoid lesions in the large bowel. The same exigency for cleanliness applies to upper gastrointestinal endoscopy: all particles inside the stomach should be dislodged with a jet of water and aspirated. Oral premedications can be administered 10 minutes before the procedure, including antifoam agents such as dimethylpolysiloxane (simethicone), a solution of N-acetylcysteine, or a proteolytic enzyme solution (pronase) that cleaves the glycoproteins. In the esophagus or stomach, mucolysis is particularly recommended before chromoscopy with methylene blue.

Step 2 - Detection of a suspect area

The surface of the mucosa should be completely explored. During upper gastrointestinal endoscopy, systematic retroflexion is required to explore the esophagogastric junction and the corpus of the stomach. During colonoscopy the recommended scope withdrawal time is 8 minutes. Abnormal areas in the gastrointestinal mucosa should be detected in standard endoscopy without image processing and chromoscopy. As a rule, polypoid neoplastic lesions (sessile or pedunculated) are conspicuous, even if they are small. In contrast, nonerosive, flat areas suggestive of neoplasia are usually inconspicuous. Polypoid lesions can be missed in sectors not accessible to frontal vision during the progression or withdrawal of the scope, such as the gastric cardia below the esophagogastric junction, the distal edge of the angulus in the stomach, and the proximal edge of a colonic valve. Nonpolypoid lesions can be missed if the clinician lacks training in recognition of slight changes in the color of the mucosa (more pale or more red), or of a strict line of demarcation within the normal mucosal surface with interruption of the subepithelial vascular network at this line. Among flat lesions, those with a depression deserve special attention because of their tendency to rapid progression, even when they are less than 10 mm in diameter.

Step 3 - Characterization of the lesion

The characterization of polypoid or nonpolypoid lesions relies on the recognition of three elements: gross morphology, the microvascular pattern, and the microarchitecture of the surface epithelium. (Examples of nonpolypoid lesions are shown on [Figures 1 - 3]).

Gross morphology. Concerns the limits and the relief of the lesion. In the squamous epithelium, iodine-potassium iodide (1.5 to 2 % Lugol solution) leaves neoplastic lesions unstained and is the easiest method for assessing the limits of flat neoplastic areas [42]. In the columnar epithelium, chromoscopy with indigo carmine solution (0.1 % - 0.5 %), a nonabsorbable dye, is easy and helpful. Other absorbed dyes have specific indications: application of acetic acid (3 % - 5 %) results in whitening of stratified squamous epithelium, and the mean duration of whitening has also been correlated with histology in the stomach [43]; methylene blue (0.5 %) stains intestinal metaplasia dark blue in the esophagus or the stomach; cresyl violet (0.2 %) and crystal violet (0.05 %), commonly applied in the investigation of early colorectal cancer in Japan, stain columnar cells purple.

The microvascular network. Best explored in transparency (i. e. with no chromoscopy) during endoscopy and with some magnification. With NBI, small vessels are clearly contrasted in dark brown and the subepithelial capillaries reproduce the architecture of the normal surface mucosa: intrapapillary capillary loops (IPCL) with a hair-clip appearance in the squamous epithelium of the esophagus [8]; a honeycomb network around the neck of gastric pits in the oxyntic mucosa of the stomach or coiled subepithelial capillaries in the antral mucosa and transversal collecting venules visible in the deeper layers [3] [9]; and hexagonal capillaries around the pits in the colon. In chronic inflammation and in neoplasia the microvascular network is altered. In the squamous epithelium of the esophagus, five types of vessels have been described: type I for normal IPCLs; type II for esophagitis with elongated IPCLs; and types III, IV, and V, with a punctuated pattern, for tumoral neoangiogenesis [8] [20]. A study conducted in operative specimens of the esophagus has confirmed the presence of a relationship between the diameter of superficial vessels and the histology, with average vessel diameters of 6.9 μ in normal mucosa, 12.9 μ in m1 cancer, 14.5 μ in m2 cancer, 18.1 μ in m3 cancer, and 20.1 μ in sm cancer [8]. In the columnar-lined esophagus, the microvascular network at the surface of neoplastic areas has relevance for the depth of invasion and the decision on whether endoscopic treatment is justified [10]. In the stomach, Helicobacter pylori infection causes a diffuse reddening of the surface of the oxyntic mucosa with regression of the honeycomb pattern and of collecting venules [14]. In intramucosal cancer, the appearance of abnormal superficial vessels (mesh, coil, or corkscrew) depends on tumor differentiation [6] [9] [13].

Surface microarchitecture of the surface epithelium. The superficial microarchitecture of the surface epithelium (i. e. depressions and ridges) is visible when using NBI or chromoscopy with the optical zoom or the macro objective lens. Two major contributions to this field have been: (a) the identification of areas with intestinal metaplasia or with a disorganized structure, suggesting low- or high-grade intraepithelial neoplasia in the columnar-lined esophagus [11] [12]; and (b) the analysis of the pit pattern of a neoplastic lesion in the large bowel and its classification using Kudo’s scheme [15] [16] [17] [19], type I describing the regular and narrow pits of normal epithelium, type II describing the enlarged, star-shaped colonic pits found in hyperplastic polyps, types IIIL, IIIs, and IV used to classify low- and high-grade intraepithelial neoplasia, and type V, with an irregular surface (V - I) or an amorphous neutral surface (V - N), suggesting invasive cancer.

When a video endoscope equipped with the newer technical facilities has detected an abnormal area, the next step is the analysis of the microcirculation at low magnification, with NBI and without chromoscopy. Slight vascular alterations suggest either a non-neoplastic lesion or low-grade neoplasia; the gross morphology is then assessed in standard vision with the help of chromoscopy. Severe vascular alterations suggest high-grade noninvasive or invasive neoplasia, and the surface microarchitecture (depressions and ridges) is explored under magnification with an optical zoom and chromoscopy (indigo carmine or cresyl violet). Magnification with NBI has been proposed as an alternative to magnification with chromoscopy [44]. When using a standard video endoscope that is not equipped with NBI and magnification, the analysis of the microcirculation in transparency is less accurate. The diagnosis relies on the assessment of the gross morphology of the lesion after staining with indigo carmine dye. In summary, there is still room for chromoscopy in the assessment of morphology; the major contribution of the NBI technique is in the analysis of the subepithelial vessels; and the optical zoom can be used to explore the pit pattern.

Step 4 - Classification of the lesion and treatment decisions

Classification after detection avoids the unnecessary resection of lesions with a very low malignant potential, or inappropriate endoscopic treatment of a lesion which should be treated by surgery. For lesions characterized as benign, non-neoplastic, and with no potential for malignancy, the clinician decides whether or not a biopsy is needed, and no endoscopic treatment is proposed. For lesions that are classified as benign, with a low potential for malignancy (low-grade dysplasia), the decision lies between endoscopic resection and surveillance. For lesions that are benign but with a high potential for intramucosal malignancy, endoscopic resection is proposed, with en-bloc resection preferred to piecemeal resection for lesions larger than 2 cm, though the location of the neoplastic lesion (i. e. esophagus, stomach, or colon) may play a determining role in the choice of technique. For carcinoma with invasion of the submucosa, the decision lies between endoscopic resection or surgery if deep invasion into the submucosa is suspected.

Competing interests: None

References

• 1 Ferlay F, Bray P, Pisani P. et al .GLOBOCAN 2002. Cancer incidence, mortality and prevalence worldwide. IARC CancerBase No. 5, version 2. 0, 2004. Lyon; IARC Press 2004
  Search in Google Scholar
• 2 Igarashi M, Saitoh Y, Fujii T. Adaptive index of hemoglobin color enhancement for the diagnosis of colorectal disease.  Endoscopy. 2005;  37 386-388
  Thieme ConnectPubMedSearch in Google Scholar
• 3 Yao K, Kato M, Fujisaki J. Techniques using the hemoglobin index of the gastric mucosa.  Endoscopy. 2005;  37 479-486
  Thieme ConnectPubMedSearch in Google Scholar
• 4 Gono K, Obi T, Yamaguchi M. et al . Appearance of enhanced tissue features in narrow-band endoscopic imaging.  J Biomed Opt. 2004;  9 568-577
  CrossrefPubMedSearch in Google Scholar
• 5 Kuznetsov K, Lambert R, Rey J F. Narrow-band imaging: potential and limitations.  Endoscopy. 2006;  38 76-81
  Thieme ConnectPubMedSearch in Google Scholar
• 6 Nakayoshi T, Tajiri H, Matsuda K. et al . Magnifying endoscopy combined with narrow-band imaging system for early gastric cancer: correlation of vascular pattern with histopathology.  Endoscopy. 2004;  36 1080-1084
  Thieme ConnectPubMedSearch in Google Scholar
• 7 Yoshida T, Inoue H, Susui S. et al . Narrow-band imaging system with magnifying endoscopy for superficial esophageal lesions.  Gastrointest Endosc. 2004;  59 288-295
  CrossrefPubMedSearch in Google Scholar
• 8 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
  Thieme ConnectPubMedSearch in Google Scholar
• 9 Yao K, Iwashita A, Kikuchi Y. Novel zoom endoscopy technique for visualizing the microvascular architecture in gastric mucosa.  Clin Gastroenterol Hepatol. 2005;  3 (Suppl 1) S23-S26
  CrossrefPubMedSearch in Google Scholar
• 10 Yao K, Takaki Y, Ohara J. et al . Magnification endoscopy outlines the microvascular architecture and extent of Barrett’s intramucosal carcinoma prior to endoscopic resection.  Gastrointest Endosc. 2006;  63 1064-1065
  CrossrefPubMedSearch in Google Scholar
• 11 Endo T, Awakawa T, Takahashi H. et al . Classification of Barrett’s epithelium by magnifying endoscopy.  Gastrointest Endosc. 2002;  55 641-647
  CrossrefPubMedSearch in Google Scholar
• 12 Kara M A, Peters F P, Rosmolen W D. et al . High-resolution endoscopy plus chromoendoscopy or narrow-band imaging in Barrett’s esophagus: a prospective randomized crossover study.  Endoscopy. 2005;  37 929-936
  Thieme ConnectPubMedSearch in Google Scholar
• 13 Tobita K. Study on minute surface structures of the depressed type early gastric cancer with magnifying endoscopy.  Dig Endosc. 2001;  13 121-126
  PubMedSearch in Google Scholar
• 14 Yagi K, Honda H, Yang J M. et al . Magnifying endoscopy in gastritis of the corpus.  Endoscopy. 2005;  37 660-666
  Thieme ConnectPubMedSearch in Google Scholar
• 15 Kudo S, Hirota S, Nakajima T. et al . Colorectal tumours and pit pattern.  J Clin Pathol. 1994;  47 880-885
  CrossrefPubMedSearch in Google Scholar
• 16 Kudo S, Rubio C A, Teixeira C S. et al . Pit pattern in colorectal neoplasia: endoscopic magnifying view.  Endoscopy. 2001;  33 367-373
  Thieme ConnectPubMedSearch in Google Scholar
• 17 Nagata S, Tanaka S, Haruma K. et al . Pit pattern diagnosis of early colorectal carcinoma by magnifying colonoscopy: clinical and histological implications.  Int J Oncol. 2000;  16 927-934
  PubMedSearch in Google Scholar
• 18 Sano Y, Saito Y, Fu K I. et al . Efficacy of magnifying endoscopy for the differential diagnosis of colorectal lesions.  Dig Endosc. 2005;  17 105-116
  CrossrefPubMedSearch in Google Scholar
• 19 Tanaka S, Haruma K, Nagata S. et al . Diagnosis of invasion depth in early colorectal carcinoma by pit pttern analysis with magnifying endoscopy.  Dig Endosc. 2001;  13 (Suppl) S2-S5
  CrossrefPubMedSearch in Google Scholar
• 20 Kumagai Y, Monma K, Kawada K. Magnifying chromoendoscopy of the esophagus: in-vivo pathological diagnosis using an endocytoscopy system.  Endoscopy. 2004;  36 590-594
  Thieme ConnectPubMedSearch in Google Scholar
• 21 Sasajima K, Kudo S E, Inoue H. et al . Real-time in vivo virtual histology of colorectal lesions when using the endocytoscopy system.  Gastrointest Endosc. 2006;  63 1010-1017
  CrossrefPubMedSearch in Google Scholar
• 22 Kiesslich R, Goetz M, Vieth M. et al . Confocal laser endomicroscopy.  Gastrointest Endosc Clin N Am. 2005;  15 715-731
  CrossrefPubMedSearch in Google Scholar
• 23 The Paris endoscopic classification of superficial neoplastic lesions . Esophagus, stomach, and colon (November 30 to December 1, 2002).  Gastrointest Endosc. 2003;  58 (6 Suppl) S3-S43
  CrossrefPubMedSearch in Google Scholar
• 24 Hisamichi S, Shirane A, Sugawara N. et al . Early endoscopic features of stomach cancer and its mode of growth.  Tohoku J Exp Med. 1978;  126 239-246
  PubMedSearch in Google Scholar
• 25 Ida K, Hashimoto Y, Takeda S. et al . Endoscopic diagnosis of gastric cancer with dye scattering.  Am J Gastroenterol. 1975;  63 316-320
  PubMedSearch in Google Scholar
• 26 Oshiba S, Ueno K, Mochizuki F. et al . Minute gastric cancer.  Tohoku J Exp Med. 1976;  118 (Suppl) 19-22
  PubMedSearch in Google Scholar
• 27 Sakaki N, Iida Y, Okasaki Y. et al . Magnifying endoscopic observation of the gastric mucosa, particularly in patients with atrophic gastritis.  Endoscopy. 1978;  10 269-274
  PubMedSearch in Google Scholar
• 28 Muto T, Kamiya J, Sawada T. et al . Small ”flat adenoma“ of the large bowel with special reference to its clinicopathologic features.  Dis Colon Rectum. 1985;  28 847-851
  CrossrefPubMedSearch in Google Scholar
• 29 Hurlsone D P, Fujii T. Practical uses of chromoendoscopy and magnification at colonoscopy.  Gastrointest Endosc Clin N Am. 2005;  15 687-702
  PubMedSearch in Google Scholar
• 30 Kiesslich R, Neurath M F. Chromo- and magnifying endoscopy for colorectal lesions.  Eur J Gastroenterol Hepatol. 2005;  17 793-801
  CrossrefPubMedSearch in Google Scholar
• 31 Ross A S, Waxman I. Flat and depressed neoplasms of the colon in Western populations.  Am J Gastroenterol. 2006;  10 172-180
  PubMedSearch in Google Scholar
• 32 Soetikno R, Friedland S, Kaltenbach T. et al . Nonpolypoid (flat and depressed) colorectal neoplasms.  Gastroenterology. 2006;  130 566-576
  CrossrefPubMedSearch in Google Scholar
• 33 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;  8 1211-1214
  PubMedSearch in Google Scholar
• 34 Fujii T, Rembacken B J, Dixon M F. et al . Flat adenomas in the United Kingdom: are treatable cancers being missed?.  Endoscopy. 1998;  30 437-443
  PubMedSearch in Google Scholar
• 35 Lambert R, Jeannerod M, Rey J F. Eyes wide shut.  Endoscopy. 2004;  36 723-725
  Thieme ConnectPubMedSearch in Google Scholar
• 36 Ajiki W, Tsukuma H, Oshima A. et al . The 10th collaborative survey on stage distribution of cancer patients among 10 cancer registries in Japan.  In: Tsukuma H (ed). Report of the Research Group for Population-based Cancer Registration in Japan. Osaka: Department of Cancer Control and Statistics, Osaka Medical Center for Cancer and Cardiovascular Diseases 2004: 13-48
  Search in Google Scholar
• 37 A nationwide totalling of mass screening for gastrointestinal cancers in 2002 [in Japanese].  J Gastroenterol Mass Survey. 2005;  43 54-73
  PubMedSearch in Google Scholar
• 38 Report on health center activities and health services for the aged 2003. Ministry of Health, Labour and Welfare of Japan. Tokyo 2003: 550-554
  Search in Google Scholar
• 39 Ajiki W, Tsukuma H, Oshima A. Trends in cancer incidence, mortality and survival in Osaka Prefecture. In: Oshima A, Kuroishi T, Tazima K (eds.) Cancer statistics: morbidity/prognosis. Shinohara Publ. Ltd. Tokyo 2004: 2-96
  Search in Google Scholar
• 40 Suzuki H, Gotoda T, Saito D. et al . Detection of early gastric cancer: overestimation of the role of mass screening [abstract].  Gastrointest Endosc. 2006;  63 AB146
  PubMedSearch in Google Scholar
• 41 Cancer Statistics in Japan 2005. Tokyo; National Cancer Center Tokyo, Japan 2005
  Search in Google Scholar
• 42 Inoue H, Rey J F, Lightdale C. Lugol chromoendoscopy for esophageal squamous cell cancer.  Endoscopy. 2001;  33 75-79
  Search in Google Scholar
• 43 Yagi K, Aruga Y, Nakamura A. et al . The study of dynamic chemical magnifying endoscopy in gastric neoplasia.  Gastrointest Endosc. 2005;  62 963-969
  CrossrefPubMedSearch in Google Scholar
• 44 Machida H, Sano Y, Yamamoto Y. et al . Narrow-band imaging in the diagnosis of colorectal mucosal lesions: a pilot study.  Endoscopy. 2004;  36 1094-1098
  Search in Google Scholar

R. Lambert, MD

International Agency for Research on Cancer (IARC)

150 Cours Albert Thomas

Lyon 69372

Cedex 08, France

Fax: + 33-4-7273-8650

Email: lambert@iarc.fr

References

• 1 Ferlay F, Bray P, Pisani P. et al .GLOBOCAN 2002. Cancer incidence, mortality and prevalence worldwide. IARC CancerBase No. 5, version 2. 0, 2004. Lyon; IARC Press 2004
  Search in Google Scholar
• 2 Igarashi M, Saitoh Y, Fujii T. Adaptive index of hemoglobin color enhancement for the diagnosis of colorectal disease.  Endoscopy. 2005;  37 386-388
  Thieme ConnectPubMedSearch in Google Scholar
• 3 Yao K, Kato M, Fujisaki J. Techniques using the hemoglobin index of the gastric mucosa.  Endoscopy. 2005;  37 479-486
  Thieme ConnectPubMedSearch in Google Scholar
• 4 Gono K, Obi T, Yamaguchi M. et al . Appearance of enhanced tissue features in narrow-band endoscopic imaging.  J Biomed Opt. 2004;  9 568-577
  CrossrefPubMedSearch in Google Scholar
• 5 Kuznetsov K, Lambert R, Rey J F. Narrow-band imaging: potential and limitations.  Endoscopy. 2006;  38 76-81
  Thieme ConnectPubMedSearch in Google Scholar
• 6 Nakayoshi T, Tajiri H, Matsuda K. et al . Magnifying endoscopy combined with narrow-band imaging system for early gastric cancer: correlation of vascular pattern with histopathology.  Endoscopy. 2004;  36 1080-1084
  Thieme ConnectPubMedSearch in Google Scholar
• 7 Yoshida T, Inoue H, Susui S. et al . Narrow-band imaging system with magnifying endoscopy for superficial esophageal lesions.  Gastrointest Endosc. 2004;  59 288-295
  CrossrefPubMedSearch in Google Scholar
• 8 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
  Thieme ConnectPubMedSearch in Google Scholar
• 9 Yao K, Iwashita A, Kikuchi Y. Novel zoom endoscopy technique for visualizing the microvascular architecture in gastric mucosa.  Clin Gastroenterol Hepatol. 2005;  3 (Suppl 1) S23-S26
  CrossrefPubMedSearch in Google Scholar
• 10 Yao K, Takaki Y, Ohara J. et al . Magnification endoscopy outlines the microvascular architecture and extent of Barrett’s intramucosal carcinoma prior to endoscopic resection.  Gastrointest Endosc. 2006;  63 1064-1065
  CrossrefPubMedSearch in Google Scholar
• 11 Endo T, Awakawa T, Takahashi H. et al . Classification of Barrett’s epithelium by magnifying endoscopy.  Gastrointest Endosc. 2002;  55 641-647
  CrossrefPubMedSearch in Google Scholar
• 12 Kara M A, Peters F P, Rosmolen W D. et al . High-resolution endoscopy plus chromoendoscopy or narrow-band imaging in Barrett’s esophagus: a prospective randomized crossover study.  Endoscopy. 2005;  37 929-936
  Thieme ConnectPubMedSearch in Google Scholar
• 13 Tobita K. Study on minute surface structures of the depressed type early gastric cancer with magnifying endoscopy.  Dig Endosc. 2001;  13 121-126
  PubMedSearch in Google Scholar
• 14 Yagi K, Honda H, Yang J M. et al . Magnifying endoscopy in gastritis of the corpus.  Endoscopy. 2005;  37 660-666
  Thieme ConnectPubMedSearch in Google Scholar
• 15 Kudo S, Hirota S, Nakajima T. et al . Colorectal tumours and pit pattern.  J Clin Pathol. 1994;  47 880-885
  CrossrefPubMedSearch in Google Scholar
• 16 Kudo S, Rubio C A, Teixeira C S. et al . Pit pattern in colorectal neoplasia: endoscopic magnifying view.  Endoscopy. 2001;  33 367-373
  Thieme ConnectPubMedSearch in Google Scholar
• 17 Nagata S, Tanaka S, Haruma K. et al . Pit pattern diagnosis of early colorectal carcinoma by magnifying colonoscopy: clinical and histological implications.  Int J Oncol. 2000;  16 927-934
  PubMedSearch in Google Scholar
• 18 Sano Y, Saito Y, Fu K I. et al . Efficacy of magnifying endoscopy for the differential diagnosis of colorectal lesions.  Dig Endosc. 2005;  17 105-116
  CrossrefPubMedSearch in Google Scholar
• 19 Tanaka S, Haruma K, Nagata S. et al . Diagnosis of invasion depth in early colorectal carcinoma by pit pttern analysis with magnifying endoscopy.  Dig Endosc. 2001;  13 (Suppl) S2-S5
  CrossrefPubMedSearch in Google Scholar
• 20 Kumagai Y, Monma K, Kawada K. Magnifying chromoendoscopy of the esophagus: in-vivo pathological diagnosis using an endocytoscopy system.  Endoscopy. 2004;  36 590-594
  Thieme ConnectPubMedSearch in Google Scholar
• 21 Sasajima K, Kudo S E, Inoue H. et al . Real-time in vivo virtual histology of colorectal lesions when using the endocytoscopy system.  Gastrointest Endosc. 2006;  63 1010-1017
  CrossrefPubMedSearch in Google Scholar
• 22 Kiesslich R, Goetz M, Vieth M. et al . Confocal laser endomicroscopy.  Gastrointest Endosc Clin N Am. 2005;  15 715-731
  CrossrefPubMedSearch in Google Scholar
• 23 The Paris endoscopic classification of superficial neoplastic lesions . Esophagus, stomach, and colon (November 30 to December 1, 2002).  Gastrointest Endosc. 2003;  58 (6 Suppl) S3-S43
  CrossrefPubMedSearch in Google Scholar
• 24 Hisamichi S, Shirane A, Sugawara N. et al . Early endoscopic features of stomach cancer and its mode of growth.  Tohoku J Exp Med. 1978;  126 239-246
  PubMedSearch in Google Scholar
• 25 Ida K, Hashimoto Y, Takeda S. et al . Endoscopic diagnosis of gastric cancer with dye scattering.  Am J Gastroenterol. 1975;  63 316-320
  PubMedSearch in Google Scholar
• 26 Oshiba S, Ueno K, Mochizuki F. et al . Minute gastric cancer.  Tohoku J Exp Med. 1976;  118 (Suppl) 19-22
  PubMedSearch in Google Scholar
• 27 Sakaki N, Iida Y, Okasaki Y. et al . Magnifying endoscopic observation of the gastric mucosa, particularly in patients with atrophic gastritis.  Endoscopy. 1978;  10 269-274
  PubMedSearch in Google Scholar
• 28 Muto T, Kamiya J, Sawada T. et al . Small ”flat adenoma“ of the large bowel with special reference to its clinicopathologic features.  Dis Colon Rectum. 1985;  28 847-851
  CrossrefPubMedSearch in Google Scholar
• 29 Hurlsone D P, Fujii T. Practical uses of chromoendoscopy and magnification at colonoscopy.  Gastrointest Endosc Clin N Am. 2005;  15 687-702
  PubMedSearch in Google Scholar
• 30 Kiesslich R, Neurath M F. Chromo- and magnifying endoscopy for colorectal lesions.  Eur J Gastroenterol Hepatol. 2005;  17 793-801
  CrossrefPubMedSearch in Google Scholar
• 31 Ross A S, Waxman I. Flat and depressed neoplasms of the colon in Western populations.  Am J Gastroenterol. 2006;  10 172-180
  PubMedSearch in Google Scholar
• 32 Soetikno R, Friedland S, Kaltenbach T. et al . Nonpolypoid (flat and depressed) colorectal neoplasms.  Gastroenterology. 2006;  130 566-576
  CrossrefPubMedSearch in Google Scholar
• 33 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;  8 1211-1214
  PubMedSearch in Google Scholar
• 34 Fujii T, Rembacken B J, Dixon M F. et al . Flat adenomas in the United Kingdom: are treatable cancers being missed?.  Endoscopy. 1998;  30 437-443
  PubMedSearch in Google Scholar
• 35 Lambert R, Jeannerod M, Rey J F. Eyes wide shut.  Endoscopy. 2004;  36 723-725
  Thieme ConnectPubMedSearch in Google Scholar
• 36 Ajiki W, Tsukuma H, Oshima A. et al . The 10th collaborative survey on stage distribution of cancer patients among 10 cancer registries in Japan.  In: Tsukuma H (ed). Report of the Research Group for Population-based Cancer Registration in Japan. Osaka: Department of Cancer Control and Statistics, Osaka Medical Center for Cancer and Cardiovascular Diseases 2004: 13-48
  Search in Google Scholar
• 37 A nationwide totalling of mass screening for gastrointestinal cancers in 2002 [in Japanese].  J Gastroenterol Mass Survey. 2005;  43 54-73
  PubMedSearch in Google Scholar
• 38 Report on health center activities and health services for the aged 2003. Ministry of Health, Labour and Welfare of Japan. Tokyo 2003: 550-554
  Search in Google Scholar
• 39 Ajiki W, Tsukuma H, Oshima A. Trends in cancer incidence, mortality and survival in Osaka Prefecture. In: Oshima A, Kuroishi T, Tazima K (eds.) Cancer statistics: morbidity/prognosis. Shinohara Publ. Ltd. Tokyo 2004: 2-96
  Search in Google Scholar
• 40 Suzuki H, Gotoda T, Saito D. et al . Detection of early gastric cancer: overestimation of the role of mass screening [abstract].  Gastrointest Endosc. 2006;  63 AB146
  PubMedSearch in Google Scholar
• 41 Cancer Statistics in Japan 2005. Tokyo; National Cancer Center Tokyo, Japan 2005
  Search in Google Scholar
• 42 Inoue H, Rey J F, Lightdale C. Lugol chromoendoscopy for esophageal squamous cell cancer.  Endoscopy. 2001;  33 75-79
  Search in Google Scholar
• 43 Yagi K, Aruga Y, Nakamura A. et al . The study of dynamic chemical magnifying endoscopy in gastric neoplasia.  Gastrointest Endosc. 2005;  62 963-969
  CrossrefPubMedSearch in Google Scholar
• 44 Machida H, Sano Y, Yamamoto Y. et al . Narrow-band imaging in the diagnosis of colorectal mucosal lesions: a pilot study.  Endoscopy. 2004;  36 1094-1098
  Search in Google Scholar

R. Lambert, MD

International Agency for Research on Cancer (IARC)

150 Cours Albert Thomas

Lyon 69372

Cedex 08, France

Fax: + 33-4-7273-8650

Email: lambert@iarc.fr