Access the full text.
Sign up today, get DeepDyve free for 14 days.
Hindawi Publishing Corporation International Journal of Surgical Oncology Volume 2011, Article ID 242608, 10 pages doi:10.1155/2011/242608 Clinical Study Imaging by Magnifying Endoscopy with NBI Implicates the Remnant Capillary Network As an Indication for Endoscopic Resection in Early Colon Cancer 1 1, 2 1 2 Shoichi Saito, Hisao Tajiri, Tomohiko Ohya, Toshiki Nikami, 1 3 Hiroyuki Aihara, and Masahiro Ikegami Department of Endoscopy, The Jikei University School of Medicine, 3-25-8, Nishi-Shinbashi, Minato-Ward, Tokyo 105-8461, Japan Division of Gastroenterology and Hepatology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo 105-8461, Japan Department of Pathology, The Jikei University School of Medicine, Tokyo 105-8461, Japan Correspondence should be addressed to Shoichi Saito, firstname.lastname@example.org Received 20 August 2010; Accepted 11 December 2010 Academic Editor: Michael Hun ¨ erbein Copyright © 2011 Shoichi Saito et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction. This study examined whether magnifying endoscopy with NBI observation (ME-NBI) could be useful selecting the appropriate treatment for submucosal invasive cancer (SM cancer). Patients and Methods. We analyzed 515 cases of colon tumors excised endoscopically or surgically. We classiﬁed capillary network pattern into four types according to the degree of dilatation, irregularity, and distribution of microcapillary features. Results. The comparison of capillary pattern and histological features revealed microcapillary networks by using confocal laser-scanning microscopy and ME-NBI in intramucosal lesion or SM cancer with remnant neoplastic glands at the superﬁcial layer. In contrast, the network was absent in SM cancer with desmoplastic reactions, which invaded deeper into the submucosal layer. Conclusions. The remaining microcapillary network is designed to maintain the architecture of neoplastic glands. Consequently, loss of this network could correlate with depth of tumor invasion and desmoplastic reaction. Therefore, we can decide the appropriate treatment by using ME-NBI method. 1. Introduction provides vascular information in a simple way. ME-NBI provides a simple and fast alternative for vascular imaging Recent technological advances in endoscopy have supported that is widely used to examine tumors in the upper gastric a ﬂood of new diagnostic methods, collectively reported as tract including the esophagus and stomach for diagnostic “Consensus Terminology” . The narrow band imaging purposes [2–7]. NBI has also been used successfully for (NBI) used in this study ﬁts into the well-studied image- endoscopic examination of the lower gastrointestinal tract enhancing endoscopy (IEE) category [2–25] as autoﬂuo- [8–25]. In Japan; however, the capillary network classiﬁ- rescence imaging (AFI) [21–24], as distinct from standard cation using ME-NBI is not popular due to its compli- imaging with white light. cation and each medical institution tends to adopt their There is almost uniform agreement that magnifying own classiﬁcation [11–14]. An important point with NBI endoscopy combined with crystal violet (CV) staining is observation is establishing early in the diagnosis whether the cancer is best resected endoscopically or surgically. If useful for pit pattern delineation [26–42]. However, this diagnostic imaging technique is not widely used because this point can be resolved, ME-NBI has great potential as it is troublesome and time-consuming, and because mucus an additional tool in the diagnosis and treatment of colon on the lesion surface may obstruct image acquisition. cancer. Magnifying endoscopy with NBI observation (ME-NBI), This study histopathologically evaluated submucosal by contrast, does not involve a complicated technique and invasive cancer (SM cancer) by ME-NBI examination in 2 International Journal of Surgical Oncology Pattern 1 Normal colon mucosa and Hyperplastic polyp No dilated microcapillary vessels Pattern 2 Slightly dilated microcapillary vessels Pattern3V(Villous pattern) Regular, dilated microcapillary vessels with villous components Marked dilated microcapillary vessels Pattern3I(Irregular pattern) Remaining capillary networks showing irregularity Pattern 4 Loss of capillary networks Figure 1: Classiﬁcation of capillary patterns. Pattern 1: No dilated microcapillary vessels in mucosa. Pattern 2: Regular, smooth microcapillary vessels, slightly dilated. Pattern 3V: Regular dilated capillary vessels in the stromal area with villous component. Pattern 3I: Capillary network preserved by markedly dilated vessels that resemble corkscrew. Pattern 4: No capillary network observed. comparison to the images obtained by confocal laser-scan- ME-NBI and magnifying observation CV staining by two ning microscopy, as a simple and useful means of selecting experienced specialists (S.S., T.N.) with more than 15 years the appropriate therapeutic intervention. of endoscopy experience. CF-H260AZI and CF-FH260AZI endoscopes were used in this study (Olympus Medical Systems Co., Ltd Tokyo, Japan). 2. Patients and Methods Figure 1 depicts the capillary-pattern classiﬁcation into The study analyzed 515 colon tumors in patients who under- four groups used in this study; pattern 1 capillaries followed went endoscopic or surgical resection at The Jikei University an unrecognized course; pattern 2 capillaries were slightly Hospital from September 2005 to March 2010. These lesions dilated; pattern 3 capillaries were markedly dilated; pattern were preoperatively performed with examination by using 4 was characterized by sparse capillaries not following International Journal of Surgical Oncology 3 (µm) Rb, rectal carcinoid 12 mm 0 10203040506070 (a) (b) Figure 2(d) (c) (d) Figure 2: Normal colon mucosa containing carcinoid tumor. (a) The microcapillary vessels are not usually observed using NBI systems in normal colon mucosa. This magnifying image shows microcapillary network in normal colon mucosa (NCM) removed surface epithelium (white box). (b) Three-dimensional structure of the microcapillary network surrounding normal glands displayed using laser scanning microscopy (LSM) in NCM. This ﬁnding corresponded with the image obtained by NBI systems. (c, d) Histological view of exposed microcapillary vessels at the surface of mucosa containing carcinoid tumor cells without absorptive tissues (black box). an obvious vascular course in the lesion. Pattern 3 was phosphate-buﬀers saline (PBS) and treated with 0.5% Triton further divided into 2 subtypes, whereby one subtype of X-100 in PBS for 5 min at 4 C. Indirect immunoﬂuorescent capillaries assumed a regular course, while the other featured microscopy was then performed. after incubation for 30 min irregularities such as capillary tortuousness, abrupt caliber at room temperature with a blocking solution containing 1% change, and heterogeneity in shape . Since the type IV normal goat serum in PBS, the specimens were incubated in a pit pattern is observed indirectly in the former subtype, blocking solution containing mouse monoclonal antihuman along with a villous component, capillaries of this type endothelium antibody (CD34; Novocastra Laboratories, Ltd. were classiﬁed as a 3-villous pattern (pattern 3V). The latter Newcastle, United Kingdom) for 60 min at room temper- subtype was designated as a 3-irregular pattern (pattern 3I). ature, and then placed at 4 C after extensive washing in SM cancer wasclassiﬁedasslight(SM-S) ifthe depth PBS, the cells were labeled with ﬂuorescein isothiocyanate- of invasion was ≤1000 µm or massive (SM-M) cancer if the (FITC-) conjugated goat anti-mouse IgG (Molecular Probes, depth of invasion exceeded 1000 µm according to the General Inc., Eugene, Oregon, USA) in the blocking solution for Rules for Clinical and Pathological Studies on Cancer of 60 min at room temperature. After washing in PBS, the the Colon, Rectum and Anus . Cancers were measured specimens were embedded in 50% glycerol in PBS. The as recommended by the Japanese Society for Cancer of the specimens were examined using confocal laser-scanning Colon and Rectum. microscopy (LSM 510; Carl Zeiss Co, Jena, Germany). The resected specimens were ﬁxed in 10% buﬀered Excitation ﬂuorescein was achieved with an argon laser formalin for 24 hours. The specimens were cut into 2 mm at a wavelength of 488 nm. An image analysis processing to 3 mm blocks. Pathological examinations were performed software LSM 5 Image Browser (Carl Zeiss) was used for 3D on HE stain by a single pathologist (M.I.), with extensive reconstruction of the immunostained microvessel. experience in gastrointestinal tract histopathology without The proportions of histological ﬁndings and construc- prior knowledge of the endoscopic ﬁndings. tions of lesions within the capillary pattern groups were For immunoﬂuorescent microscopy, cells were ﬁxed with compared by using the x test as statistical analysis. To 1% paraformaldehyde in a 0.1 M phosphate buﬀer for 30 min determine diﬀerences in the mean distance of invasion each at 4 C. The specimens ﬁxed in this way were washed in into SM layer, comparisons between the capillary pattern 4 International Journal of Surgical Oncology Figure 3(c) Figure 3(b) (µm) 0 102030405060 70 80 (a) (b) (c) Figure 3(e) (d) (e) Figure 3: Neoplastic lesion. (a) Endoscopic image of protruding-type colon polyp. (b) Magnifying endoscopy with NBI observation (ME- NBI) showing slightly dilated microcapillary vessels at the tumor edge. (c) LSM imaging showed the corkscrew-like dilated and meandering vessels. (d, e) Histological view revealed tubular adenoma with high-grade dysplastic change by HE stain ((c) low power view, (d) high power view). groups were performed by one-way analysis of variance into the submucosa (Figure 4(d)), but their caliber could not (ANOVA), followed by multiple comparison testing using be measured. the Bonferroni-Dunn method. Statistical signiﬁcance was deﬁned as P< .05. 3.2. Relationship between Capillary Pattern and Histological Type or Depth of Invasion (Figures 1 and 5). In the capillary pattern 1 group, large hyperplastic polyps (HP; 15 mm or larger) accounted for 82.4% of lesions, with serrated 3. Results adenomas (SA) 14.9%, and tubular adenomas (TA) 2.7%. 3.1. Capillary Patterns As Determined by Laser Scanning In the group of capillary pattern 2 lesions showing slight Microscopy (LSM) (Figures 2–4). Capillaries in the nor- dilation, HP and SA accounted for only about less than mal colon mucosa, tubular adenoma, intramucosal cancer, 3.0%, with 60.0% of the patterns observed in TA, and and SM cancer were examined for course and caliber. A remaining 5 lesions (2.8%) being SM cancers. In the group honeycomb-like network was formed by minute vessels of 3V capillary pattern lesions (villous component showing of approximately 10 µm in diameter in the normal colon notable dilation), SA accounted for 4.3% of lesions, TA mucosa (Figures 2(a) and 2(b)). Vascular dilation to about 19.4%, and intramucosal cancers for the remaining 62.6%. 12.11 µm in diameter was observed by LSM (Figure 3(c))in The frequency of atypical lesions was higher in the pattern 3V tubular adenomas. In the tubular adenoma, vascular dilation than pattern 2 lesions group. Furthermore, 13.7% of study was brought into view by ME-NBI (Figure 3(b)), and at the lesions were identiﬁed as SM cancer and 7.9% as SM-M sites of notable dilation (Figure 4(b)) thin vessels were found cancer. In the group of subtype 3I lesions (irregular vascular arranged in bundle form on an enlarged view, and vessels course), on the other hand, intramucosal lesions decreased were as thin as 3 to 4 µm individually but formed bundles to 18.2%, with SM-S and SM-M cancers representing 22.7% which observed like dilated vessels 40 to 50 µmindiameter and 56.1%, respectively. In the group of pattern 3I lesions, (Figure 4(c)). At sites where no apparent capillary course was about 50% were indicated for surgical resection. In the type seen by ME-NBI, only a few minute vessels could be observed 4 lesions (untraceable capillary course), intramucosal lesion travelling from the superﬁcial layer of the lesions to deeper accounted for 1.6% of the total number and this case was International Journal of Surgical Oncology 5 Figure 4(c) Figure 4(d) (a) (b) (µm) (µm) 0 5 10 15 20 25 10 20 30 40 50 (c) (d) Figure 4: SM cancer with persistent intramucosal lesion. (a) Endoscopic image of protruding-type tumor with a depressed lesion. (b) representative ME-NBI showing marked dilated microcapillary at the protrusion edges on the left side. These congestive vessels form an oval around the gland pits. In contrast, no capillary vessel network remained at depressed lesion. (c) A representative LSM image showing the minimum narrow vessels gathered into a bundle around the gland pits. (d) In the depressed lesion, it was revealed small capillary vessels shaped abrupt caliber change has not left any longer by using LSM. diagnosed as moderately diﬀerentiated adenocarcinoma. The type B accounted for 24.1% of lesions with the reminder remaining 98.4% of lesions were SM cancer, with 96.8% of (75.9%) classiﬁed as type C. these being, SM-M cancer. 3.4. Rate of Accurate Diagnosis of Early Colon Cancer as 3.3. Relationship between Superﬁcial Histological Character- Determined by Pit Pattern and Capillary Pattern (Table 1). istics and Capillary Patterns (Figures 6 and 7). The char- The rate of accurate diagnosis was determined prospectively acteristics of histological invasive ﬁndings in SM cancers based on the ﬁndings of vascular dilation between the pit (n = 133) were classiﬁed into three types: type A showed and the capillary patterns in 291 lesions of early colon cancer an intramucosal lesion across the entire area of tumor; at the preoperative examination. When the highly irregular type B showed a ruptured muscular mucosa permitting the type V irregular (V ) pit pattern or type V nonstructure invading SM end to be exposed to the superﬁcial layer, but (V ) pit pattern was selected as pit pattern-related indicators no accompanying desmoplastic reaction; type C showed a of SM-M, sensitivity and speciﬁcity were 94.5% and 86.2%, desmoplastic reaction and were thus analyzed with respect respectively, with no appreciable diﬀerence between V and capillary pattern. V pits. In contrast, sensitivity and speciﬁcity were 95.6% All lesions in the group with capillary pattern 2 lesions and 77.3%, respectively, when patterns 3I and 4 were selected were of type A, while only 47.1% of lesions in the pattern as the indicators of SM-M. Accuracy rate as an indicator 3I group were type A, with type B accounting for 47.1% of was not signiﬁcantly diﬀerent from pit pattern (91.4%) and lesions, and type C 5.8%. In the capillary pattern 4 group, capillary pattern (88.7%). 6 International Journal of Surgical Oncology (%) 0 50 100 (n: 515) Pattern 1 82.4% (61/74) 14.9% (11/74) 2.7% (2/74) 60% (105/175) 32% (56/175) Pattern 2 2.9% (5/175) 1.7% (3/175) 1.1% (2/175) 2.3% (4/175) Pattern 3V 19.4% (27/139) 62.6% (87/139) 4.3% (6/139) 5.8% (8/139) 7.9% (11/139) Pattern 3I 18.2% (12/66) 22.7% (15/66) 56.1% (37/66) 3% (2/66) Pattern 4 96.8% (59/61) P< .001 ANOVAR 1.6% (1/61) SM Cancer (n: 135) HP: hyperplastic polyp SA: serrted adenoma TA (n: 136) <1000 µm (SM-S) HP (n: 65) TA: tubular adenoma M-Ca. (n: 156) SA (n: 23) 1000 µm < (SM-M) M-Ca: intramucosal cancer Figure 5: Comparison between capillary pattern and histological ﬁndings. Table 1: Comparison of diagnostic accuracy with capillary pattern ME-NBI diﬀers from magnifying observation with CV and pit pattern on intramucosal cancer and SM cancer. staining in that images are easily interchangeable with the former technique. ME-NBI is also extremely useful for Sensitivity Speciﬁcity Accuracy examining capillaries for dilation to diﬀerentiate, which Capillary pattern 95.6% 77.3% 88.7% is particularly valuable for diﬀerentiating a tumor from Pit pattern 94.5% 86.2% 91.4% a nontumorous lesion. To this end, Sano et al. [8, 9, (n: 291) 11] proposed a classiﬁcation into 3 types for capillary pattern observed by ME-NBI, based on the initial degree of microcapillary dilatation at the mucosal surface. In contrast, another study proposed that assessing the degree of the 4. Discussion dilatation of the capillary vessel dilatation should include An appropriate therapeutic modality for the resection of the pit pattern, which is indirectly observed by ME-NBI, to distinguish between SM-S and SM-M cancer . Based on colon cancer is selected according to criteria established by the Japanese Society for Cancer of the Colon and Rectum the present study, we alternatively propose that classiﬁcations of capillary pattern, including ours, are diﬃcult to use in Japan. These criteria consider cancer of the colon and without experience, because they are complicated patterns rectum an indication for endoscopic resection if the depth of invasion into the SM layer is ≤1000 µm and no vessels are and the estimation is quite subjective of endoscopists. Hence a simpler means of endoscopic examination by ME-NBI is involved [42–45]. Preoperative diagnosis is of overriding importance from needed to enable meaningful selection of the appropriate both a clinical and economic standpoint as it may avoid treatment. In the present case, nearly 90% of patter 1 lesions without unnecessary treatment. As part of this, a thorough endo- scopic examination is considered necessary for selecting the vascular dilation were hyperplastic polyps. The tumorous appropriate therapeutic modality. Examination by magni- lesions included traditional serrated adenomas and also seemed to include sessile serrated polyps/adenomas [47, 48]. fying endoscopy with CV staining is one such modality, although time limitations can preclude this technique in Given that the concept of sessile serrated polyps/adenoma remains to be fully accepted by Japanese pathologists, further some cases. Endoscopic equipment has improved markedly investigation and consideration are warranted. with respect to resolution in recent years such that pit pattern can be clearly visualized. As a result, magnifying observa- The distance of the capillary pattern observed by ME- NBI from the mucosal surface remains unclear. Thus, we tion is rarely needed to distinguish SM cancer from HP or TA. used LSM to accurately resecte the specimen by endoscopic International Journal of Surgical Oncology 7 Type A Well-preserved mucosal neoplastic component (a) Type B Desmoplastic reaction (−) Desmin stain (b) Type C Desmoplastic reaction (+) Desmin stain (c) Figure 6: Classiﬁcation of SM cancer according to superﬁcial histological features. (%) 0 100 (n: 133) Pattern 2-3V 62.5% (15/24) 37.5% (9/24) Pattern 3I 47.1% (24/51) 47.1% (24/51) 5.8% (3/51) Pattern 4 24.1% (14/58) 75.9% (44/58) P< .001 Type A Type B Type C Figure 7: Comparison between capillary pattern and superﬁcial histological characteristics in SM cancer. 8 International Journal of Surgical Oncology forceps [2, 5], and the LSM images were comparable to those References by ME-NBI. Therefore, it seemed that the observation by  H. Tajiri and H. Niwa, “Proposal for a consensus terminology ME-NBI does represent the surface histological architecture in endoscopy: how should diﬀerent endoscopic imaging of the mucosa. techniques be grouped and deﬁned?” Endoscopy, vol. 40, no. Lesions were classiﬁed as pattern 3 or 4 according to 9, pp. 775–778, 2008. the vascular-course details. This is an important point of  T. Nakayoshi, H. Tajiri, K. Matsuda, M. Kaise, M. Ikegami, diﬀerence that will help beginners to interpret ﬁndings and H. Sasaki, “Magnifying endoscopy combined with narrow obtained by ME-NBI. For that reason, we classiﬁed lesions band imaging system for early gastric cancer: correlation without a recognizable vascular course into a separate of vascular pattern with histopathology (including video),” category called pattern 4. LSM imaging conﬁrmed that these Endoscopy, vol. 36, no. 12, pp. 1080–1084, 2004. lesions were virtually without microcapillary vessels, further  H. Tajiri, K. Matsuda, and J. Fujisaki, “What can we see with the endoscope? Present status and future perspectives,” indicating that the desmoplastic reaction occurs on the Digestive Endoscopy, vol. 14, no. 4, pp. 131–137, 2002. surface of the tumor due to the invasion into the SM layer.  T.Yoshida, H.Inoue,S. Usui, H. Satodate, N.Fukami, and Lesions of pattern 3 were also divided into patterns 3V S. E. Kudo, “Narrow-band imaging system with magnifying and 3I, with the former predominately intramucosal and endoscopy for superﬁcial esophageal lesions,” Gastrointestinal thus clearly indicated for endoscopic resection. On the other Endoscopy, vol. 59, no. 2, pp. 288–295, 2004. hand, 50% or less pattern 3I lesions were also indicated for  K.I.Goda, H. Tajiri, M.Ikegami, M. Urashima, T. Nakayoshi, endoscopic resection even if they had an irregular vascular and M. Kaise, “Usefulness of magnifying endoscopy with course and intramucosal or SM invasion depth within narrow band imaging for the detection of specialized intestinal 1000 µm. These lesions showed limited desmoplastic reaction metaplasia in columnar-lined esophagus and Barrett’s adeno- and were left with neoplastic glands leading to the surface carcinoma,” Gastrointestinal Endoscopy, vol. 65, no. 1, pp. 36– layer of the tumor. 46, 2007.  T. Tahara, T. Shibata, M. Nakamura et al., “Gastric mucosal In lesions of pattern 4, the vascular course is already pattern by using magnifying narrow-band imaging endoscopy devastated and surgical resection should be selected without clearly distinguishes histological and serological severity of hesitation when such ﬁndings are obtained. The selection chronic gastritis,” Gastrointestinal Endoscopy,vol.70, no. 2,pp. of an appropriate therapeutic modality would therefore rest 246–253, 2009. with the presence or absence of a vascular course.  M. Kaise, M. Kato, M. Urashima et al., “Magnifying endoscopy In the case of pattern 3I lesions, however, more than combined with narrow-band imaging for diﬀerential diagno- 50% were from cases of SM-M cancer. In such cases where sis of superﬁcial depressed gastric lesions,” Endoscopy,vol.41, selecting an appropriate modality remains diﬃcult, magni- no. 4, pp. 310–315, 2009. fying observation of the pit pattern with conventional CV  H. Machida, Y. Sano, Y. Hamamoto et al., “Narrow-band staining and endoscopic ultrasound examination should be imaging in the diagnosis of colorectal mucosal lesions: a pilot combined with due discretion. study,” Endoscopy, vol. 36, no. 12, pp. 1094–1098, 2004. As discussed above, microcapillary patterns do not  Y. Sano, T. Horimatsu, K. I. Fu, A. Katagiri, M. Muto, directly reﬂect the depth of cancer invasion, and ME-NBI and H. Ishikawa, “Magnifying observation of microvascular architecture of colorectal lesions using a narrow-band imaging observation can accordingly be considered a useful aid to pit system,” Digestive Endoscopy, vol. 18, no. 1, pp. S44–S51, 2006. pattern diagnosis. Endoscopic resection may be selected as a  M. Hirata, S. Tanaka, S. Oka et al., “Magnifying endoscopy temporary measure for the treatment of pattern 3I lesions with narrow band imaging for diagnosis of colorectal tumors,” that are suspected of invasion by SM-M cancer if patients Gastrointestinal Endoscopy, vol. 65, no. 7, pp. 988–995, 2007. have a tumor in the lower part of the rectum or serious  Y. Sano, H. Ikematsu, K. I. Fu et al., “Meshed capillary vessels complications in the cardiovascular or respiratory systems. by use of narrow-band imaging for diﬀerential diagnosis of small colorectal polyps,” Gastrointestinal Endoscopy,vol.69, no. 2, pp. 278–283, 2009. Abbreviations  H. Kanao, S. Tanaka, S. Oka, M. Hirata, S. Yoshida, and AFI: Auto ﬂuorescence imaging; K. Chayama, “Narrow-band imaging magniﬁcation predicts IEE: Image enhancing endoscopy; the histology and invasion depth of colorectal tumors,” NBI: Narrow band imaging; Gastrointestinal Endoscopy, vol. 69, no. 3, pp. 631–636, 2009. ME-NBI: Magnifying endoscopy with NBI observation;  Y. Wada, S.E.Kudo, H. Kashidaetal.,“Diagnosis ofcolorectal lesions with the magnifying narrow-band imaging system,” NCM: Normal colon mucosa; Gastrointestinal Endoscopy, vol. 70, no. 3, pp. 522–531, 2009. SM cancer: Submucosal invasive cancer;  T. Nikamf, S. Saito, H. Tajiri, and M. Ikegami, “The evaluation CV: Crystal violet; of histological atypia and depth of invasion of colorectal LSM: Laser scanning microscopy. lesions using magniﬁed endoscopy with narrow-band imag- ing,” Gastroenterological Endoscopy, vol. 51, no. 1, pp. 10–19, Acknowledgment 2009 (Japanese).  R. Hun ¨ eburg, F. Lammert, C. Rabe et al., “Chromo- The authors wish to thank Dr. Kyohei Hayashi (department colonoscopy detects more adenomas than white light of social medicine and cultural sciences, Kyoto prefectural colonoscopy or narrow band imaging colonoscopy in heredi- university, school of medicine) for useful suggestions of tary nonpolyposis colorectal cancer screening,” Endoscopy,vol. statistical analysis and comments in this paper. 41, no. 4, pp. 316–322, 2009. International Journal of Surgical Oncology 9  F. J. C. van den Broek, E. J. Van Soest, A. H. Naber  S. E. Kudo, H. Kashida, T. Tamura et al., “Colonoscopic et al., “Combining autoﬂuorescence imaging and narrow- diagnosis and management of nonpolypoid early colorectal band imaging for the diﬀerentiation of adenomas from cancer,” World Journal of Surgery, vol. 24, no. 9, pp. 1081–1090, non-neoplastic colonic polyps among experienced and non- 2000. experienced endoscopists,” American Journal of Gastroenterol-  S. Tanaka,K.Haruma, M. Ito et al.,“Detailed colonoscopy for ogy, vol. 104, no. 6, pp. 1498–1507, 2009. detecting early superﬁcial carcinoma: recent developments,”  F. J. C. van den Broek, P. Fockens, S. Van Eeden et al., Journal of Gastroenterology, vol. 35, no. 12, pp. 121–125, 2000. “Clinical evaluation of endoscopic trimodal imaging for the  T. Fujii, R. T. Hasegawa, Y. Saitoh et al., “Chromoscopy during detection and diﬀerentiation of colonic polyps,” Clinical colonoscopy,” Endoscopy, vol. 33, no. 12, pp. 1036–1041, 2001. Gastroenterology and Hepatology, vol. 7, no. 3, pp. 288–295,  D. P. Hurlstone, S. S. Cross, R. Slater, D. S. Sanders, and S. Brown, “Detecting diminutive colorectal lesions at  T. Uraoka, Y. Saito, T. Matsuda et al., “Detectability of colorec- colonoscopy: a randomised controlled trial of pan-colonic tal neoplastic lesions using a narrow-band imaging system: versus targeted chromoscopy,” Gut, vol. 53, no. 3, pp. 376–380, apilot study,” Journal of Gastroenterology and Hepatology,vol. 23, no. 12, pp. 1810–1815, 2008.  D. P. Hurlstone and T. Fujii, “Practical uses of chromoen-  J. E. East, N. Suzuki, M. Stavrinidis et al., “Narrow band doscopy and magniﬁcation at colonoscopy,” Gastrointestinal imaging with magniﬁcation for the characterization of small Endoscopy Clinics of North America, vol. 15, no. 4, pp. 687–702, and diminutive colonic polyps: pit pattern and vascular 2005. pattern intensity,” Endoscopy, vol. 40, no. 10, pp. 811–817,  R. Kiesslich, M. von Bergh, M. Hahn, G. Hermann, and M. Jung, “Chromoendoscopy with indigocarmine improves the  S. Sikka, D. A. Ringold, S. Jonnalagandda, and B. Banerjee, detection of adenomatous and nonadenomatous lesions in the “Comparison of white light and narrow band high deﬁnition colon,” Endoscopy, vol. 33, no. 12, pp. 1001–1006, 2001. images in predicting colon polyp histology, using standard  S. Y. Tung, C. S. Wu, and M. Y. Su, “Magnifying colonoscopy colonoscopes without optical magniﬁcation,” Endoscopy,vol. in diﬀerentiating neoplastic from nonneoplastic colorectal 40, no. 10, pp. 818–822, 2008. lesions,” American Journal of Gastroenterology, vol. 96, no. 9,  S. Saito, H. Aihara, H. Tajri et al., “Autoﬂuorescence imaging pp. 2628–2632, 2001. makes it easy to diﬀerentiate neoplastic lesions from non-  S. Kato, T. Fujii, I. Koba et al., “Assessment of colorectal lesions neoplastic lesions in the colon,” in New Challenges in Gastroin- using magnifying colonoscopy and mucosal dye spraying: can testinal Endoscopy, pp. 330–337, Springer, Tokyo, Japan, 2008. signiﬁcant lesions be distinguished?” Endoscopy,vol.33, no.4,  T. Matsuda, Y. Saito, K. I. Fu et al., “Does autoﬂuorescence pp. 306–310, 2001. imaging videoendoscopy system improve the colonoscopic  K. Konishi, K. Kaneko, T. Kurahashi et al., “A comparison polyp detection rate?—a pilot study,” American Journal of of magnifying and nonmagnifying colonoscopy for diagnosis Gastroenterology, vol. 103, no. 8, pp. 1926–1932, 2008. of colorectal polyps: a prospective study,” Gastrointestinal Endoscopy, vol. 57, no. 1, pp. 48–53, 2003.  H. Aihara,K.Sumiyama, S. Saito, H. Tajiri,and M. Ikegami, “Numerical analysis of the autoﬂuorescence intensity of  D. P. Hurlstone, S. S. Cross, I. Adam et al., “Eﬃcacy of high neoplastic and non-neoplastic colorectal lesions by using magniﬁcation chromoscopic colonoscopy for the diagnosis of a novel videoendoscopy system,” Gastrointestinal Endoscopy, neoplasia in ﬂat and depressed lesions of the colorectum: a vol. 69, no. 3, pp. 726–e1, 2009. prospective analysis,” Gut, vol. 53, no. 2, pp. 284–290, 2004.  K. S. Boparai, F. J. C. van den Broek, S. van Eeden, P.  K. I. Fu, Y. Sano, S. Kato et al., “Chromoendoscopy using Fockens, and E. Dekker, “Hyperplastic polyposis syndrome: indigo carmine dye spraying with magnifying observation is a pilot study for the diﬀerentiation of polyps by using high- themost reliablemethodfor diﬀerential diagnosis between resolution endoscopy, autoﬂuorescence imaging, and narrow- non-neoplastic and neoplastic colorectal lesions: a prospective band imaging,” Gastrointestinal Endoscopy,vol.70, no. 5, pp. study,” Endoscopy, vol. 36, no. 12, pp. 1089–1093, 2004. 947–955, 2009.  S. Tanaka, S. Nagata, S. Oka et al., “Determining depth of  R. Higashi, T. Uraoka, J. Kato et al., “Diagnostic accuracy of invasion by VN pit pattern analysis in submucosal colorectal narrow-band imaging and pit pattern analysis signiﬁcantly carcinoma,” Oncology Reports, vol. 9, no. 5, pp. 1005–1008, improved for less-experienced endoscopists after an expanded training program,” Gastrointestinal Endoscopy,vol. 72, no.1,  H. Kanao, S. Tanaka, S. Oka et al., “Clinical signiﬁcance pp. 127–135, 2010. of type V pit pattern subclassiﬁcation in determining the  S. E. Kudo, S. Tamura, T. Nakajima, H. O. Yamano, H. Kusaka, depth of invasion of colorectal neoplasms,” World Journal of and H. Watanabe, “Diagnosis of colorectal tumorous lesions Gastroenterology, vol. 14, no. 2, pp. 211–217, 2008. by magnifying endoscopy,” Gastrointestinal Endoscopy, vol. 44,  Japanese Society for Cancer of the Colon and Rectum, General no. 1, pp. 8–14, 1996. Rules for Clinical and Pathological Studies on Cancer of the  S. Kudo, S. Hirota, T. Nakajima et al., “Colorectal tumours and Colon, Rectum and Anus, Japanese Society for Cancer of the pit pattern,” Journal of Clinical Pathology, vol. 47, no. 10, pp. Colon and Rectum, Tokyo, Japan, 7th edition, 2006. 880–885, 1994.  K. Kitajima, T. Fujimori, S. Fuji et al., “Correlations between  S. Nagata, S. Tanaka, K. Haruma et al., “Pit pattern diagnosis lymph node metastasis and depth of submucosal invasion of early colorectal carcinoma by magnifying colonoscopy: in submucosal invasive colorectal carcinoma: a Japanese clinical and histological implications,” International Journal of collaborative study,” Journal of Gastroenterology, vol. 39, no. Oncology, vol. 16, no. 5, pp. 927–934, 2000. 6, pp. 534–543, 2004.  S. Tanaka, T. Kaltenbach, K. Chayama, and R. Soetikno,  H. Ueno, H. Mochizuki, Y. Hashiguchi et al., “Risk factors for “High-magniﬁcation colonoscopy (with videos),” Gastroin- an adverse outcome in early invasive colorectal carcinoma,” testinal Endoscopy, vol. 64, no. 4, pp. 604–613, 2006. Gastroenterology, vol. 127, no. 2, pp. 385–394, 2004. 10 International Journal of Surgical Oncology  T. A. Longacre and C. M. Fenoglio-Preiser, “Mixed hyperplas- tic adenomatous polyps/serrated adenomas. A distinct form of colorectal neoplasia,” American Journal of Surgical Pathology, vol. 14, no. 6, pp. 524–537, 1990.  S. Oka, S. Tanaka, T. Hiyama et al., “Clinicopathologic and endoscopic features of colorectal serrated adenoma: diﬀer- ences between polypoid and superﬁcial types,” Gastrointestinal Endoscopy, vol. 59, no. 2, pp. 213–219, 2004.  E. Torlakovic, E. Skovlund, D. C. Snover, G. Torlakovic, and J. M. Nesland, “Morphologic reappraisal of serrated colorectal polyps,” American Journal of Surgical Pathology,vol. 27, no.1, pp. 65–81, 2003. MEDIATORS of INFLAMMATION The Scientific Gastroenterology Journal of World Journal Research and Practice Diabetes Research Disease Markers Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 International Journal of Journal of Immunology Research Endocrinology Hindawi Publishing Corporation Hindawi Publishing Corporation http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 Submit your manuscripts at http://www.hindawi.com BioMed PPAR Research Research International Hindawi Publishing Corporation Hindawi Publishing Corporation http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 Journal of Obesity Evidence-Based Journal of Journal of Stem Cells Complementary and Ophthalmology International Alternative Medicine Oncology Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 Parkinson’s Disease Computational and Behavioural Mathematical Methods AIDS Oxidative Medicine and in Medicine Research and Treatment Cellular Longevity Neurology Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014
International Journal of Surgical Oncology – Hindawi Publishing Corporation
Published: Feb 10, 2011
Access the full text.
Sign up today, get DeepDyve free for 14 days.