Topic Highlight Open Access
Copyright ©2011 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastroenterol. Jan 7, 2011; 17(1): 9-14
Published online Jan 7, 2011. doi: 10.3748/wjg.v17.i1.9
Autofluorescence imaging and magnification endoscopy
Monalisa Filip, Sevastiţa Iordache, Adrian Săftoiu, Tudorel Ciurea, Research Center of Gastroenterology and Hepatology, University of Medicine and Pharmacy, Craiova, Dolj, 200349, Romania
Author contributions: Filip M, Iordache S, Săftoiu A and Ciurea T performed the research; Filip M, Iordache S, Săftoiu A and Ciurea T analyzed the data; Filip M and Săftoiu A wrote the paper.
Correspondence to: Monalisa Filip, MD, Gastroenterology Department, University of Medicine and Pharmacy, 2-4 Petru Rares Street, Craiova, Dolj, 200349, Romania. monalisafilip@yahoo.com
Telephone: +40-72-7972250 Fax: +40-25-1310287
Received: July 2, 2010
Revised: August 26, 2010
Accepted: September 2, 2010
Published online: January 7, 2011

Abstract

It is well known that angiogenesis is critical in the transition from premalignant to malignant lesions. Consequently, early detection and diagnosis based on morphological changes to the microvessels are crucial. In the last few years, new imaging techniques which utilize the properties of light-tissue interaction have been developed to increase early diagnosis of gastrointestinal (GI) tract neoplasia. We analyzed several “red-flag” endoscopic techniques used to enhance visualization of the vascular pattern of preneoplastic and neoplastic lesions (e.g. trimodal imaging including autofluorescence imaging, magnifying endoscopy and narrow band imaging). These new endoscopic techniques provide better visualization of mucosal microsurface structure and microvascular architecture and may enhance the diagnosis and characterization of mucosal lesions in the GI tract. In the near future, it is expected that trimodal imaging endoscopy will be practiced as a standard endoscopy technique as it is quick, safe and accurate for making a precise diagnosis of gastrointestinal pathology, with an emphasis on the diagnosis of early GI tract cancers. Further large-scale randomized controlled trials comparing these modalities in different patient subpopulations are warranted before their endorsement in the routine practice of GI endoscopy.

Key Words: Angiogenesis; Autofluorescence imaging; Multiband imaging; Narrow band imaging; Zoom endoscopy



INTRODUCTION

It is well known that angiogenesis is critical in the transition from premalignant to malignant lesions. Consequently, early detection and diagnosis based on morphologic changes to the microvessels are crucial. Conventional endoscopic diagnosis using white light is based on subtle morphological changes such as superficially elevated, flat, or depressed lesions and minimal changes in color. However, these findings are difficult to recognize, especially for inexperienced endoscopists. As a result, the diagnosis may be inaccurate or a superficial cancer in the gastrointestinal (GI) tract may be overlooked.

New imaging techniques which utilize the properties of light-tissue interaction have recently been developed to enhance early diagnosis of GI tract neoplasia. Endoscopic autofluorescence imaging (AFI) produces real-time pseudocolor images based on the detection of natural tissue fluorescence generated from endogenous fluorophores (collagen, nicotinamide, adenine dinucleotide, flavin and porphyrins) through emission induced by excitation light. The system can visualize lesions, including malignancies, by differences in tissue fluorescence properties and can reveal early stage cancers not detectable by conventional white light endoscopy (WLE)[1,2]. Magnifying endoscopy with narrow band imaging (ME-NBI) represents a real-time endoscopic imaging technique which enhances visualization of the surface texture and the vascular network of the mucosa with the aim of improving tissue characterization and differentiation[3].

AUTOFLUORESCENCE IMAGING

The principle of autofluorescence diagnosis is based on the interaction between light with a specific wavelength and tissue fluorophores. When tissues are exposed to short wavelength light, endogenous fluorophores (collagen, nicotinamide, adenine dinucleotide, flavin and porphyrins) are excited, leading to the emission of fluorescent light of a longer wavelength (i.e. autofluorescence)[4]. Normal, inflamed and neoplastic tissue have different autofluorescence characteristics that may thus enable their differentiation. Thus, normal tissue is pseudocolored as green, blood vessels as dark green, while hypertrophic fundic mucosa of the stomach and dysplastic/neoplastic areas appear as magenta. During AFI, a suspected neoplasia (AFI-positive lesion) is defined as any area that is different in color from the surrounding mucosa, and which has a defined circumferential margin[5].

Autofluorescence is abnormal in neoplastic tissues due to several mechanisms: (1) increase in the nuclear-cytoplasmic ratio, which consequently determines decreased autofluorescence as nuclei show no autofluorescence as compared with cytoplasm; (2) loss of collagen, submucosal collagen is the strongest fluorophore which disappears due to thickening of the mucosa; and (3) neovascularization, inducing increased hemoglobin concentration which absorbs autofluorescence light[6].

Several published studies showed an increased sensitivity for the detection of high-grade dysplasia and early cancer in the GI tract when autofluorescence techniques were used[1,2,5-9]. Kara et al[7] showed the effectiveness of AFI in identifying high-grade dysplasia and early cancer in patients with Barrett′s esophagus. Compared with WLE and random 4-quadrant biopsies, AFI increased the detection of high-grade dysplasia and esophageal adenocarcinoma by an additional 6 out of 60 patients, representing an increase of 10%, from 23% to 33%. False-positive lesions were determined by the presence of acute inflammation. On the other hand, Kara et al[8] showed that fluorescence imaging with light-induced fluorescence endoscopy (LIFE) using a fiber-optic endoscope was no better than standard WLE for the detection of high-grade dysplasia and early cancer in a randomized crossover study of patients with Barrett′s esophagus. Another study tested the diagnostic performance of AFI for early gastric neoplasms, thus Ohkawa et al[9] concluded that LIFE is highly sensitive (sensitivity 96.4%) but not very specific (specificity 49.1%), since 50.9% of benign lesions were also identified as having abnormal fluorescence images. Using the latest technology incorporated in AFI systems, Kato et al[5] obtained similar results, with approximately 25% of superficial elevated neoplasia diagnosed only by AFI and missed by WLE. In principle, a superficial elevated neoplasm of a similar hue to the surrounding mucosa might be overlooked during WLE, but it can be revealed by AFI if the elevated neoplasm appears as magenta within a normal looking green mucosa (Figure 1, Figure 2, Figure 3, Figure 4).

Figure 1
Figure 1 Normal esophageal mucosa. A: Normal vascular pattern above the gastroesophageal (GE) junction visualized in white light endoscopy; B: Autofluorescence imaging of the normal mucosa and vascular pattern above the GE junction; C: Magnifying endoscopy with narrow band imaging depicting the submucosal vessels in cyan and intrapapillary capillary loops in brown.
Figure 2
Figure 2 Esophageal squamous cell carcinoma invading the gastroesophageal junction. A: Elevated irregular mucosa with abnormal vascular pattern, difficult to see in white light endoscopy in retroflexion, immediately below the gastroesophageal junction; B: Autofluorescence imaging showing the lesion extension in magenta, with surrounding green normal mucosa; C: Magnifying endoscopy with narrow band imaging showing irregular, thick and distorted mucosal vessels characteristic for tumor angiogenesis.
Figure 3
Figure 3 Early gastric adenocarcinoma at the level of the gastric angle. A: Irregular ulcer visualized in white light endoscopy (WLE); B: Autofluorescence imaging showing in magenta the neoplastic margins and a larger lesion extension, as compared with WLE; C: Magnifying endoscopy with narrow band imaging showing a modified pit pattern, with irregular and distorted vascular pattern in the center suggesting high-grade dysplasia/ early cancer, and with villous pits and light blue crest sign in the margins suggesting intestinal metaplasia.
Figure 4
Figure 4 Gastric polyp with moderate dysplasia. A: White light endoscopy showing a 10 mm gastric polyp; B: Autofluorescence imaging with magenta areas on the surface of the polyp, surrounded by green normal mucosa; C: Magnifying endoscopy with narrow band imaging showing a modified pit pattern of the mucosa with an increased number of capillaries.

While all these studies demonstrate the vast potential of AFI to target premalignant lesions (high grade dysplasia) and early cancers, they also reveal important limitations of this technique and set-up directions for future improvement. The large number of false-positive results with a consequent low positive predictive value implies a potential benefit from adjunct methods such as ME-NBI, optical-coherence tomography (OCT) or confocal laser endomicroscopy (CLE)[10] which would provide greater detection specificity. The use of trimodal imaging endoscopy that includes WLE, AFI and ME-NBI incorporated in one endoscopy system might improve diagnostic accuracy for high-grade dysplasia and early cancer[11-13]. ME-NBI is currently considered the technique of choice for improvement of diagnostic accuracy because it reduces the high rate of false-positive results associated with WLE and AFI. Autofluorescence consists primarily of visible light, resulting in images limited essentially to the mucosal surface. Consequently, the development of infrared techniques may provide greater tissue penetration, obtaining images with greater contrast between lesions and their surrounding regions, and allowing the visualization of vascularization in deeper lesions, including the submucosa. Some studies reported that infrared endoscopy is capable of detecting abnormal submucosal vascularization in tumor lesions, with retention of indocyanine green being correlated with the size of the submucosal vascular bed[14-18]. There is also a direct correlation between the presence of infrared fluorescence and the number of submucosal vessels. With the development of tumor invasion, there is a tendency for more abnormal blood vessels to be formed, further accompanied by an increase in fluorescence[18].

NARROW BAND IMAGING

Narrow band imaging (NBI) is an optical image technology that enhances structural mucosal patterns (pit-pattern), as well as mucosal/submucosal vessels, by employing the characteristics of the light spectrum. The technology consists of placing narrow bandpass filters in front of a conventional white-light source to obtain tissue illumination at selected narrow wavelength bands. Currently available NBI systems use 2 narrow band filters that provide tissue illumination in the blue (415 nm) and green (540 nm) spectrum of light. The superficial penetrating wavelength of 415 nm corresponds to the main peak on the absorption spectrum of hemoglobin, while the deeper penetrating wavelength of 540 nm corresponds to a secondary hemoglobin absorption peak. Capillaries in the superficial mucosal layer are emphasized by the 415 nm light and are displayed in brown, whereas deeper mucosal and submucosal vessels are made visible by the 540 nm light and are displayed in cyan (Figures 1-4). NBI performance is certainly maximized when it is combined with magnification (ME-NBI)[3,19]. This technique improves the morphological analysis of epithelial crests of the mucosa and enables a more precise analysis of the abnormal surface architecture (pit-pattern) of neoplastic lesions. However, the most important contribution is represented by the clear visualization of the vascular network in the mucosa, being especially useful in evaluation of the abnormal neoangiogenesis process in high-grade dysplasia/early cancer[20].

It was previously recognized that the morphological changes of an intrapapillary capillary loop (IPCL) might represent a new option for early diagnosis of squamous cell carcinoma in the esophagus[21,22]. However, evaluation of IPCLs under white light observation requires high levels of proficiency and is usually not possible during the usual clinical workup. By using the magnifying scope, the normal appearance of the IPCL is identified as red dots. NBI enables a more vivid observation of the IPCLs, increasing diagnostic accuracy, especially for inexperienced endoscopists (Figure 1C)[23]. Branching vessels which are located relatively deeper in the wall layers are observed in cyan, while IPCLs which are located in a more superficial layer, are observed as brown loops (brown dots).

Changes in the IPCL pattern include dilatation, tortuosity and/or caliber change of individual IPCL or multiple IPCLs of various shapes. According to the degree of change, these are classified into five types[23,24]: type I is associated with normal epithelium and IPCLs are observed as smooth running small-diameter capillary vessels; type II involves minimal dilatation and elongation of IPCLs, and is often equivalent to regenerative tissue or inflammation; type III assumes minimal changes in IPCLs and corresponds to borderline lesions which potentially include esophagitis and low-grade intraepithelial neoplasia; in type IV, 3 of the 4 abnormal IPCLs patterns are present and correspond to high-grade intraepithelial neoplasia; finally, type V includes all 4 abnormal IPCLs characteristics and signifies the presence of cancer. Type V is subdivided in four types, type V-1, V-2, V-3 to VN which reflect cancer infiltration depth. In type V-1, IPCLs demonstrate characteristic changes, dilatation, meandering, irregular caliber and variable form, and corresponds to m1 lesions (carcinoma in situ). As it advances to m2 and m3, destruction of IPCL advances gradually and these changes are further extended into the submucosa. Thus, in type VN, which is characteristic of sm deep invasive carcinoma, new tumor vessels appear, around 10 times larger than the irregular vessels which appear in IPCLs type V-3 (Figure 2C)[23,24].

ME-NBI is very useful for identifying superficial squamous cell carcinoma in the head and neck region. Muto et al[25,26] reported that visualization of abnormal microvessel architecture in cancerous lesions is significantly improved by NBI as compared with WLE. This finding is clinically significant because no cases of superficial cancer in the oropharynx or hypopharynx were previously reported before the advent of NBI.

Most of the studies using NBI were designed to evaluate the mucosal pattern and capillary network of patients with Barrett′s esophagus, knowing that during WLE it is difficult to identify dysplastic and early neoplastic changes. In all these studies, the accuracy of the diagnosis was higher for NBI as compared with WLE[27-34]. NBI with magnifying endoscopy thus enables visualization of the details of the mucosal surface and capillary networks without using dyes. Regular villous/gyrus-forming mucosal patterns, as well as flat mucosa with long branching blood vessels are highly predictive for specialized intestinal metaplasia without dysplasia. Irregular/disrupted mucosal pattern, an irregular vascular pattern and abnormal blood vessels are associated with high-grade intraepithelial neoplasia or early cancer. Abnormal vascularity was defined as dilated, corkscrew vessels with increased vascularity and an abnormal, nonuniform branching pattern (Figure 2C)[27,28]. All high-grade intraepithelial neoplasia have at least one abnormality, and 85% have two or more abnormalities[27]. Goda et al[29] reported that the addition of capillary pattern to fine mucosal patterns improved the diagnostic value of ME-NBI for detecting specialized intestinal metaplasia and superficial adenocarcinoma.

In a recent study, Singh et al[30] validated a simplified classification of the various morphologic patterns visualized in Barrett′s esophagus in four easily distinguishable types: A, round pits with regular microvasculature (columnar mucosa without intestinal mucosa); B, villous/ridge pits with regular microvasculature (intestinal metaplasia); C, absent pits with regular microvasculature (intestinal metaplasia); D, distorted pits with irregular microvasculature (high-grade intraepithelial neoplasia). This classification showed reproducibility and repeatability, both by experienced endoscopists and for those unfamiliar with NBI, suggesting a rapid learning curve. Therefore, ME-NBI allows all endoscopists to perform targeted biopsies for specialized intestinal metaplasia and high-grade intraepithelial neoplasia with a high rate of success[30-34].

There is no evidence to prove the clinical usefulness of NBI during non-magnifying endoscopic observation for detecting abnormal pathology within the stomach and the duodenum. From a technical point of view, the mucosal image by non-magnification observation with NBI is too dark and noisy for meaningful investigation, because the lumen of the stomach is large[35]. Feasibility studies showed the potential of NBI with magnification to identify gastric intestinal metaplasia[36], predict the histologic subtypes of early gastric cancer[37], and improve margin delineation of gastric cancer for endoscopic mucosal resection[38]. Uedo et al[36] reported that a distinctive finding called light blue crests is a good indicator of histological intestinal metaplasia, which is a well-known risk factor for the development of differentiated-type gastric cancer. NBI observation of a light blue crest, defined as a fine blue-white line on the crests of the epithelial surface or gyri, correlated with the histologic diagnosis of intestinal metaplasia with 89% sensitivity and 93% specificity. The light blue crest was frequently observed in the mucosa surrounding differentiated-type early gastric cancers, and it demarcated the extent of the tumors (Figure 3C).

In a study involving 165 patients with depressed-type early gastric cancers, Nakayoshi et al[37] reported that ME-NBI is not sufficient to replace conventional histology, but is capable of predicting the histological characteristics of gastric cancer. They classified the abnormal microvascular pattern into two types. In the case of differentiated-type depressed early gastric cancer, a relatively regular fine network pattern was more likely to be observed, while for the undifferentiated-type, a irregular, twisting, or corkscrew pattern was more likely to be observed, representing a relatively low density of microvessels. However, ME-NBI may not be sufficient to replace conventional histology, but it may allow improved differentiation between benign and malignant minute lesions and may be useful for diagnosing the extent of cancerous infiltration.

MULTIBAND IMAGING

Multiband imaging (MBI) represents a digital image processing technique that enhances the appearance of mucosal surface structures by using selected wavelengths of light in reconstructed virtual images. MBI technology uses a software-driven image-processing algorithm that is based on spectral estimation methods. A standard image captured by a color charge-coupled device video endoscope is sent to a spectral estimation matrix processing circuit contained in the video processor. Here, reflectance spectra of corresponding pixels that make up the conventional image are mathematically estimated. From these spectra, it is feasible to reconstruct a virtual image of a single wavelength. Three such single-wavelength images can be selected and assigned to the red, green and blue monitor inputs, respectively, to display a composite color-enhanced MBI image in real-time[3]. There are very few published data thus far on the efficacy of MBI for detection or differentiation of GI tract lesions, although the technique seems to be superior to WLE, noninvasive and may more easily detect lesions without dye, during both routine and detailed examinations[39,40].

In conclusion, these new endoscopic techniques provide better visualization of mucosal surface microstructure and microvascular architecture and may enhance the diagnosis and characterization of mucosal lesions in the GI tract. In the near future, trimodal imaging endoscopy, which combines WLE, AFI and ME-NBI, is expected to be practiced as a standard endoscopy technique as it is quick, safe and accurate for making a precise diagnosis of GI pathology. Although there is compelling evidence that these new techniques are superior to conventional endoscopy, current clinical guidelines are still limited. Further large-scale randomized controlled trials comparing these modalities in different patient subpopulations are, of course, warranted before their endorsement in the routine practice of GI endoscopy.

Footnotes

Peer reviewer: Naoaki Sakata, MD, PhD, Division of Hepato-Biliary Pancreatic Surgery, Tohoku University Graduate School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8574, Japan

S- Editor Sun H L- Editor Webster JR E- Editor Ma WH

References
1.  Haringsma J, Tytgat GN, Yano H, Iishi H, Tatsuta M, Ogihara T, Watanabe H, Sato N, Marcon N, Wilson BC. Autofluorescence endoscopy: feasibility of detection of GI neoplasms unapparent to white light endoscopy with an evolving technology. Gastrointest Endosc. 2001;53:642-650.  [PubMed]  [DOI]  [Cited in This Article: ]
2.  Uedo N, Iishi H, Tatsuta M, Yamada T, Ogiyama H, Imanaka K, Sugimoto N, Higashino K, Ishihara R, Narahara H. A novel videoendoscopy system by using autofluorescence and reflectance imaging for diagnosis of esophagogastric cancers. Gastrointest Endosc. 2005;62:521-528.  [PubMed]  [DOI]  [Cited in This Article: ]
3.  Song LM, Adler DG, Conway JD, Diehl DL, Farraye FA, Kantsevoy SV, Kwon R, Mamula P, Rodriguez B, Shah RJ. Narrow band imaging and multiband imaging. Gastrointest Endosc. 2008;67:581-589.  [PubMed]  [DOI]  [Cited in This Article: ]
4.  Haringsma J, Tytgat GN. Fluorescence and autofluorescence. Baillieres Best Pract Res Clin Gastroenterol. 1999;13:1-10.  [PubMed]  [DOI]  [Cited in This Article: ]
5.  Kato M, Kaise M, Yonezawa J, Yoshida Y, Tajiri H. Autofluorescence endoscopy versus conventional white light endoscopy for the detection of superficial gastric neoplasia: a prospective comparative study. Endoscopy. 2007;39:937-941.  [PubMed]  [DOI]  [Cited in This Article: ]
6.  Ragunath K. Autofluorescence endoscopy--not much gain after all? Endoscopy. 2007;39:1021-1022.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Kara MA, Peters FP, Ten Kate FJ, Van Deventer SJ, Fockens P, Bergman JJ. Endoscopic video autofluorescence imaging may improve the detection of early neoplasia in patients with Barrett's esophagus. Gastrointest Endosc. 2005;61:679-685.  [PubMed]  [DOI]  [Cited in This Article: ]
8.  Kara MA, Smits ME, Rosmolen WD, Bultje AC, Ten Kate FJ, Fockens P, Tytgat GN, Bergman JJ. A randomized crossover study comparing light-induced fluorescence endoscopy with standard videoendoscopy for the detection of early neoplasia in Barrett's esophagus. Gastrointest Endosc. 2005;61:671-678.  [PubMed]  [DOI]  [Cited in This Article: ]
9.  Ohkawa A, Miwa H, Namihisa A, Kobayashi O, Nakaniwa N, Ohkusa T, Ogihara T, Sato N. Diagnostic performance of light-induced fluorescence endoscopy for gastric neoplasms. Endoscopy. 2004;36:515-521.  [PubMed]  [DOI]  [Cited in This Article: ]
10.  Wang TD, Triadafilopoulos G. Autofluorescence imaging: have we finally seen the light? Gastrointest Endosc. 2005;61:686-688.  [PubMed]  [DOI]  [Cited in This Article: ]
11.  Curvers WL, Singh R, Song LM, Wolfsen HC, Ragunath K, Wang K, Wallace MB, Fockens P, Bergman JJ. Endoscopic tri-modal imaging for detection of early neoplasia in Barrett's oesophagus: a multi-centre feasibility study using high-resolution endoscopy, autofluorescence imaging and narrow band imaging incorporated in one endoscopy system. Gut. 2008;57:167-172.  [PubMed]  [DOI]  [Cited in This Article: ]
12.  Kara MA, Bergman JJ. Autofluorescence imaging and narrow-band imaging for the detection of early neoplasia in patients with Barrett's esophagus. Endoscopy. 2006;38:627-631.  [PubMed]  [DOI]  [Cited in This Article: ]
13.  Kato M, Kaise M, Yonezawa J, Goda K, Toyoizumi H, Yoshimura N, Yoshida Y, Kawamura M, Tajiri H. Trimodal imaging endoscopy may improve diagnostic accuracy of early gastric neoplasia: a feasibility study. Gastrointest Endosc. 2009;70:899-906.  [PubMed]  [DOI]  [Cited in This Article: ]
14.  Gostout CJ, Jacques SL. Infrared video imaging of subsurface vessels: a feasibility study for the endoscopic management of gastrointestinal bleeding. Gastrointest Endosc. 1995;41:218-224.  [PubMed]  [DOI]  [Cited in This Article: ]
15.  Iseki K, Tatsuta M, Iishi H, Sakai N, Yano H, Ishiguro S. Effectiveness of the near-infrared electronic endoscope for diagnosis of the depth of involvement of gastric cancers. Gastrointest Endosc. 2000;52:755-762.  [PubMed]  [DOI]  [Cited in This Article: ]
16.  Mataki N, Nagao S, Kawaguchi A, Matsuzaki K, Miyazaki J, Kitagawa Y, Nakajima H, Tsuzuki Y, Itoh K, Niwa H. Clinical usefulness of a new infrared videoendoscope system for diagnosis of early stage gastric cancer. Gastrointest Endosc. 2003;57:336-342.  [PubMed]  [DOI]  [Cited in This Article: ]
17.  Ito S, Muguruma N, Kimura T, Yano H, Imoto Y, Okamoto K, Kaji M, Sano S, Nagao Y. Principle and clinical usefulness of the infrared fluorescence endoscopy. J Med Invest. 2006;53:1-8.  [PubMed]  [DOI]  [Cited in This Article: ]
18.  Kimura T, Muguruma N, Ito S, Okamura S, Imoto Y, Miyamoto H, Kaji M, Kudo E. Infrared fluorescence endoscopy for the diagnosis of superficial gastric tumors. Gastrointest Endosc. 2007;66:37-43.  [PubMed]  [DOI]  [Cited in This Article: ]
19.  Muto M, Horimatsu T, Ezoe Y, Hori K, Yukawa Y, Morita S, Miyamoto S, Chiba T. Narrow-band imaging of the gastrointestinal tract. J Gastroenterol. 2009;44:13-25.  [PubMed]  [DOI]  [Cited in This Article: ]
20.  Kuznetsov K, Lambert R, Rey JF. Narrow-band imaging: potential and limitations. Endoscopy. 2006;38:76-81.  [PubMed]  [DOI]  [Cited in This Article: ]
21.  Inoue H, Honda T, Nagai K, Kawano T, Yoshino K, Takeshita K, Endo M. Ultra-high magnification endoscopic observation of carcinoma in situ of the oesophagus. Dig Endosc. 1997;9:16-18.  [PubMed]  [DOI]  [Cited in This Article: ]
22.  Kumagai Y, Inoue H, Nagai K, Kawano T, Iwai T. Magnifying endoscopy, stereoscopic microscopy, and the microvascular architecture of superficial esophageal carcinoma. Endoscopy. 2002;34:369-375.  [PubMed]  [DOI]  [Cited in This Article: ]
23.  Yoshida T, Inoue H, Usui S, Satodate H, Fukami N, Kudo SE. Narrow-band imaging system with magnifying endoscopy for superficial esophageal lesions. Gastrointest Endosc. 2004;59:288-295.  [PubMed]  [DOI]  [Cited in This Article: ]
24.  Inoue H, Kaga M, Sato Y, Sugaya S, Kudo S. Magnifying endoscopic diagnosis of tissue atypia and cancer invasion depth in the area of pharyngo-esophageal squamous epithelium by NBI enhanced magnification image: IPCL pattern classification. Comprehensive atlas of high resolution endoscopy and narrow band imaging. Oxford, UK: Blackwell Publishing Ltd 2007; 49-66.  [PubMed]  [DOI]  [Cited in This Article: ]
25.  Muto M, Katada C, Sano Y, Yoshida S. Narrow band imaging: a new diagnostic approach to visualize angiogenesis in superficial neoplasia. Clin Gastroenterol Hepatol. 2005;3:S16-S20.  [PubMed]  [DOI]  [Cited in This Article: ]
26.  Muto M, Nakane M, Katada C, Sano Y, Ohtsu A, Esumi H, Ebihara S, Yoshida S. Squamous cell carcinoma in situ at oropharyngeal and hypopharyngeal mucosal sites. Cancer. 2004;101:1375-1381.  [PubMed]  [DOI]  [Cited in This Article: ]
27.  Kara MA, Ennahachi M, Fockens P, ten Kate FJ, Bergman JJ. Detection and classification of the mucosal and vascular patterns (mucosal morphology) in Barrett's esophagus by using narrow band imaging. Gastrointest Endosc. 2006;64:155-166.  [PubMed]  [DOI]  [Cited in This Article: ]
28.  Sharma P, Bansal A, Mathur S, Wani S, Cherian R, McGregor D, Higbee A, Hall S, Weston A. The utility of a novel narrow band imaging endoscopy system in patients with Barrett's esophagus. Gastrointest Endosc. 2006;64:167-175.  [PubMed]  [DOI]  [Cited in This Article: ]
29.  Goda K, Tajiri H, Ikegami M, Urashima M, Nakayoshi T, Kaise M. Usefulness of magnifying endoscopy with narrow band imaging for the detection of specialized intestinal metaplasia in columnar-lined esophagus and Barrett's adenocarcinoma. Gastrointest Endosc. 2007;65:36-46.  [PubMed]  [DOI]  [Cited in This Article: ]
30.  Singh R, Anagnostopoulos GK, Yao K, Karageorgiou H, Fortun PJ, Shonde A, Garsed K, Kaye PV, Hawkey CJ, Ragunath K. Narrow-band imaging with magnification in Barrett's esophagus: validation of a simplified grading system of mucosal morphology patterns against histology. Endoscopy. 2008;40:457-463.  [PubMed]  [DOI]  [Cited in This Article: ]
31.  Singh R, Karageorgiou H, Owen V, Garsed K, Fortun PJ, Fogden E, Subramaniam V, Shonde A, Kaye P, Hawkey CJ. Comparison of high-resolution magnification narrow-band imaging and white-light endoscopy in the prediction of histology in Barrett's oesophagus. Scand J Gastroenterol. 2009;44:85-92.  [PubMed]  [DOI]  [Cited in This Article: ]
32.  Herrero LA, Curvers WL, Bansal A, Wani S, Kara M, Schenk E, Schoon EJ, Lynch CR, Rastogi A, Pondugula K. Zooming in on Barrett oesophagus using narrow-band imaging: an international observer agreement study. Eur J Gastroenterol Hepatol. 2009;21:1068-1075.  [PubMed]  [DOI]  [Cited in This Article: ]
33.  Curvers WL, Bohmer CJ, Mallant-Hent RC, Naber AH, Ponsioen CI, Ragunath K, Singh R, Wallace MB, Wolfsen HC, Song LM. Mucosal morphology in Barrett's esophagus: interobserver agreement and role of narrow band imaging. Endoscopy. 2008;40:799-805.  [PubMed]  [DOI]  [Cited in This Article: ]
34.  Kara MA, Peters FP, Rosmolen WD, Krishnadath KK, ten Kate FJ, Fockens P, Bergman JJ. High-resolution endoscopy plus chromoendoscopy or narrow-band imaging in Barrett's esophagus: a prospective randomized crossover study. Endoscopy. 2005;37:929-936.  [PubMed]  [DOI]  [Cited in This Article: ]
35.  Yao K, Nagahama T, Hirai F, Sou S, Matsui T, Tanabe H, Iwashita A, Kaye P, Ragunath K. Clinical application of magnification endoscopy with NBI in the stomach and the duodenum. Comprehensive atlas of high resolution endoscopy and narrow band imaging. Oxford, UK: Blackwell Publishing Ltd 2007; 83-103.  [PubMed]  [DOI]  [Cited in This Article: ]
36.  Uedo N, Ishihara R, Iishi H, Yamamoto S, Yamamoto S, Yamada T, Imanaka K, Takeuchi Y, Higashino K, Ishiguro S. A new method of diagnosing gastric intestinal metaplasia: narrow-band imaging with magnifying endoscopy. Endoscopy. 2006;38:819-824.  [PubMed]  [DOI]  [Cited in This Article: ]
37.  Nakayoshi T, Tajiri H, Matsuda K, Kaise M, Ikegami M, Sasaki H. Magnifying endoscopy combined with narrow band imaging system for early gastric cancer: correlation of vascular pattern with histopathology (including video). Endoscopy. 2004;36:1080-1084.  [PubMed]  [DOI]  [Cited in This Article: ]
38.  Sumiyama K, Kaise M, Nakayoshi T, Kato M, Mashiko T, Uchiyama Y, Goda K, Hino S, Nakamura Y, Matsuda K. Combined use of a magnifying endoscope with a narrow band imaging system and a multibending endoscope for en bloc EMR of early stage gastric cancer. Gastrointest Endosc. 2004;60:79-84.  [PubMed]  [DOI]  [Cited in This Article: ]
39.  Mouri R, Yoshida S, Tanaka S, Oka S, Yoshihara M, Chayama K. Evaluation and validation of computed virtual chromoendoscopy in early gastric cancer. Gastrointest Endosc. 2009;69:1052-1058.  [PubMed]  [DOI]  [Cited in This Article: ]
40.  Parra-Blanco A, Jiménez A, Rembacken B, González N, Nicolás-Pérez D, Gimeno-García AZ, Carrillo-Palau M, Matsuda T, Quintero E. Validation of Fujinon intelligent chromoendoscopy with high definition endoscopes in colonoscopy. World J Gastroenterol. 2009;15:5266-5273.  [PubMed]  [DOI]  [Cited in This Article: ]