Narrow-band imaging in the diagnosis of deep submucosal colorectal cancers: a systematic review and meta-analysis

Abstract

Background and aims Magnifying endoscopy with narrow-band imaging (M-NBI) has been widely used in the differential diagnosis of deep submucosal colorectal cancers (dSMCs) from superficial submucosal cancers (sSMCs) and intramucosal neoplasms. We aimed to pool the diagnostic efficacy of M-NBI and compare it with that of magnifying chromoendoscopy (M-CE) in diagnosing colorectal dSMC.

Methods PubMed, EMBASE, and the Cochrane Library were searched to identify eligible studies. Meeting abstracts were also searched. A bivariate mixed-effects binary regression model was used in the meta-analysis to calculate the pooled diagnostic efficacy of M-NBI and compare it with that of M-CE in the diagnosis of dSMC. Subgroup analyses and meta-regression were conducted to explore sources of heterogeneity.

Results We included 17 studies: 14 full texts and 3 meeting abstracts. The pooled sensitivity, specificity, and area under the summary receiver operating characteristic curve (AUC) with 95 % confidence intervals (CIs) in diagnosing dSMC were 74 % (66 % – 81 %; I² = 84.6 %), 98 % (94 % – 99 %; I² = 94.4 %), and 0.91 (0.88 – 0.93), respectively, for M-NBI. The pooled sensitivity, specificity and AUC (95 %CI) were 84 % (76 % – 89 %; I² = 76.9 %), 97 % (94 % – 99 %; I² = 90.2 %), and 0.97 (0.95 – 0.98), respectively, for M-CE. M-NBI had lower sensitivity (P < 0.01) than M-CE with similar specificity (P = 0.32). Subgroup analyses and meta-regression indicated that endoscopic diagnostic criteria, study type, endoscope type, risk of index test bias, and histopathological diagnostic criteria might be the sources of heterogeneity.

Conclusions M-NBI and M-CE had comparable specificities in diagnosing dSMC, but the sensitivity of M-NBI was slightly lower than that of M-CE.

^* These authors contributed equally to this work.

• References

• 1 Saito Y, Uraoka T, Yamaguchi Y. et al. A prospective, multicenter study of 1111 colorectal endoscopic submucosal dissections (with video). Gastrointest Endosc 2010; 72: 1217-1225
• 2 Kitajima K, Fujimori T, Fujii S. et al. Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol 2004; 39: 534-543
• 3 Tanaka S, Haruma K, Oh EH. et al. Conditions of curability after endoscopic resection for colorectal carcinoma with submucosally massive invasion. Oncol Rep 2000; 7: 783-788
• 4 Watanabe T, Itabashi M, Shimada Y. et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. Int J Clin Oncol 2012; 17: 1-29
• 5 Matsuda T, Fujii T, Saito Y. et al. Efficacy of the invasive/non-invasive pattern by magnifying chromoendoscopy to estimate the depth of invasion of early colorectal neoplasms. Am J Gastroenterol 2008; 103: 2700-2706
• 6 Ikematsu H, Matsuda T, Emura F. et al. Efficacy of capillary pattern type IIIA/IIIB by magnifying narrow band imaging for estimating depth of invasion of early colorectal neoplasms. BMC Gastroenterol 2010; 10: 33
• 7 Wada Y, Kudo SE, Kashida H. et al. Diagnosis of colorectal lesions with the magnifying narrow-band imaging system. Gastrointest Endosc 2009; 70: 522-531
• 8 Fukuzawa M, Saito Y, Matsuda T. et al. Effectiveness of narrow-band imaging magnification for invasion depth in early colorectal cancer. World J Gastroenterol 2010; 16: 1727-1734
• 9 Hayashi N, Tanaka S, Kanao H. et al. Relationship between narrow-band imaging magnifying observation and pit pattern diagnosis in colorectal tumors. Digestion 2013; 87: 53-58
• 10 Hisabe T, Yao K, Beppu T. et al. Validity of the usefulness of microvascular architecture and microsurface structure using magnifying endoscopy with narrow-band imaging in the colorectal neoplasm. Ann Gastroenterol 2013; 26: 45-51
• 11 Jang HW, Park SJ, Cheon JH. et al. Does magnifying narrow-band imaging or magnifying chromoendoscopy help experienced endoscopists assess invasion depth of large sessile and flat polyps?. Dig Dis Sci 2014; 59: 1520-1528
• 12 Kawasaki K, Kurahara K, Yanai S. et al. Significance of a white opaque substance under magnifying narrow-band imaging colonoscopy for the diagnosis of colorectal epithelial neoplasms. Gastrointest Endosc 2015; 82: 1097-1104
• 13 Misawa M, Kudo SE, Wada Y. et al. Magnifying narrow-band imaging of surface patterns for diagnosing colorectal cancer. Oncol Rep 2013; 30: 350-356
• 14 Okamoto Y, Watanabe H, Tominaga K. et al. Evaluation of microvessels in colorectal tumors by narrow band imaging magnification: including comparison with magnifying chromoendoscopy. Dig Dis Sci 2011; 56: 532-538
• 15 Saito S, Tajiri H, Ohya T. et al. Imaging by magnifying endoscopy with NBI implicates the remnant capillary network as an indication for endoscopic resection in early colon cancer. Int J Surg Oncol 2011; 2011: 242608
• 16 Sakamoto T, Saito Y, Nakajima T. et al. Comparison of magnifying chromoendoscopy and narrow-band imaging in estimation of early colorectal cancer invasion depth: A pilot study. Dig Endosc 2011; 23: 118-123
• 17 Takahashi M, Sasajima K, Chinzei R. Feasibility of narrow band imaging magnification for the invasion depth diagnosis of early colorectal cancers. Gastrointest Endosc 2014; 79: AB443-AB444
• 18 Yoshida N, Hisabe T, Inada Y. et al. The ability of a novel blue laser imaging system for the diagnosis of invasion depth of colorectal neoplasms. J Gastroenterol 2014; 49: 73-80
• 19 Yoshida N, Naito Y, Kugai M. et al. Efficacy of magnifying endoscopy with flexible spectral imaging color enhancement in the diagnosis of colorectal tumors. J Gastroenterol 2011; 46: 65-72
• 20 Zhang JJ, Gu LY, Chen XY. et al. Endoscopic diagnosis of invasion depth for early colorectal carcinomas: a prospective comparative study of narrow-band imaging, acetic acid, and crystal violet. Medicine (Baltimore) 2015; 94: e528
• 21 Hiraga Y, Sumioka M, Hiramoto T. et al. Comparison with narrow band imaging (NBI) magnification and flexible spectral imaging color enhancement (FICE) magnification in the invasion depth diagnosability of colorectal tumors. Gastrointest Endosc 2011; 73: AB379-AB380
• 22 Myung YS, Ko BM, Park SK. et al. Combination of narrow band image, chromoendoscopy and endoscopic ultrasonography to predict deep submucosal invasion in scheduled ESD patients. Gastrointest Endosc 2015; 81: AB252
• 23 Wada Y, Kudo SE, Misawa M. et al. Vascular pattern classification of colorectal lesions with narrow band imaging magnifying endoscopy. Dig Endosc 2011; 23 (Suppl. 01) 106-111
• 24 Kaminski MF, Hassan C, Bisschops R. et al. Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2014; 46: 435-449
• 25 Moher D, Liberati A, Tetzlaff J. et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Int Med 2009; 151: 264-269 , W64
• 26 Whiting PF, Rutjes AW, Westwood ME. et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Int Med 2011; 155: 529-536
• 27 Chu H, Cole SR. Bivariate meta-analysis of sensitivity and specificity with sparse data: a generalized linear mixed model approach. J Clin Epidemiol 2006; 59: 1331-1332 ; author reply 1332–1333
• 28 Reitsma JB, Glas AS, Rutjes AW. et al. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 2005; 58: 982-990
• 29 Higgins JP, Thompson SG, Deeks JJ. et al. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-560
• 30 Deeks JJ, Macaskill P, Irwig L. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol 2005; 58: 882-893
• 31 Wada Y, Kashida H, Kudo SE. et al. Diagnostic accuracy of pit pattern and vascular pattern analyses in colorectal lesions. Dig Endosc 2010; 22: 192-199
• 32 Dixon MF. Gastrointestinal epithelial neoplasia: Vienna revisited. Gut 2002; 51: 130-131
• 33 Stanley R, Hamilton S, Aaltonen Le. World Health Organization classification of tumors: Pathology and genetics of tumors of the digestive system. Lyon: International Agency for Research on Cancer; 2000: 103-119
• 34 Japanese Society for Cancer of the Colon and Rectum. General rules for clinical and pathological studies on cancer of the colon, rectum and anus. 7th edn. Tokyo: Kanahara Shuppan; 2006
• 35 The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc; 2003 58. Suppl: S3–S43
• 36 Kudo S, Tamura S, Nakajima T. et al. Diagnosis of colorectal tumorous lesions by magnifying endoscopy. Gastrointest Endosc 1996; 44: 8-14
• 37 Kudo S, Hirota S, Nakajima T. et al. Colorectal tumours and pit pattern. J Clin Pathol 1994; 47: 880-885
• 38 Fujii T, Hasegawa RT, Saitoh Y. et al. Chromoscopy during colonoscopy. Endoscopy 2001; 33: 1036-1041
• 39 Tanaka S, Kaltenbach T, Chayama K. et al. High-magnification colonoscopy (with videos). Gastrointest Endosc 2006; 64: 604-613
• 40 Kanao H, Tanaka S, Oka S. et al. Narrow-band imaging magnification predicts the histology and invasion depth of colorectal tumors. Gastrointest Endosc 2009; 69: 631-636
• 41 Zhu LY, Ren L, Ge Z. et al. Observation of microvessels and invasion in early colorectal neoplasms on narrow band imaging: combination with CD34 and matrix metalloproteinase-7 expression. Eur J Gastroenterol Hepatol 2014; 26: 1428-1433
• 42 Wakelin LP, Adams A, Hunter C. et al. Interaction of crystal violet with nucleic acids. Biochemistry 1981; 20: 5779-5787
• 43 Ikematsu H, Kaneko K, Fukuda D. et al. Accuracy of capillary pattern classification using NBI magnification for diagnosis of colorectal lesions. Gastrointest Endosc 2008; 67: AB311
• 44 Wada Y, Kashida H, Kudo S. Microvascular architecture of localized colorectal lesions observed with narrow band imaging. Clin Gastroenterol 2008; 23: 1569-1577
• 45 Ikematsu H, Kaneko K, Sano Y. Efficacy of capillary pattern classification using NBI magnification for diagnosis of colorectal lesions. Early Colorectal Cancer 2008; 12: 389-394
• 46 Yamada M, Saito Y, Sakamoto T. et al. Endoscopic predictors of deep submucosal invasion in colorectal laterally spreading tumors. Endoscopy 2016; 48: 456-464
• 47 Uraoka T, Saito Y, Matsuda T. et al. Endoscopic indications for endoscopic mucosal resection of laterally spreading tumours in the colorectum. Gut 2006; 55: 1592-1597
• 48 Rotondano G, Bianco MA, Buffoli F. et al. The Cooperative Italian FLIN Study Group: prevalence and clinico-pathological features of colorectal laterally spreading tumors. Endoscopy 2011; 43: 856-861
• 49 Saitoh Y, Obara T, Watari J. et al. Invasion depth diagnosis of depressed type early colorectal cancers by combined use of videoendoscopy and chromoendoscopy. Gastrointest Endosc 1998; 48: 362-370
• 50 Kobayashi N, Saito Y, Sano Y. et al. Determining the treatment strategy for colorectal neoplastic lesions: endoscopic assessment or the non-lifting sign for diagnosing invasion depth?. Endoscopy 2007; 39: 701-705
• 51 Hayashi N, Tanaka S, Hewett DG. et al. Endoscopic prediction of deep submucosal invasive carcinoma: validation of the narrow-band imaging international colorectal endoscopic (NICE) classification. Gastrointest Endosc 2013; 78: 625-632
• 52 Sano Y, Tanaka S, Kudo SE. et al. Narrow-band imaging (NBI) magnifying endoscopic classification of colorectal tumors proposed by the Japan NBI Expert Team. Dig Endosc 2016; 28: 526-533
• 53 Nakadoi K, Oka S, Tanaka S. et al. Condition of muscularis mucosae is a risk factor for lymph node metastasis in T1 colorectal carcinoma. Surg Endosc 2014; 28: 1269-1276
• 54 Kawachi H, Eishi Y, Ueno H. et al. A three-tier classification system based on the depth of submucosal invasion and budding/sprouting can improve the treatment strategy for T1 colorectal cancer: a retrospective multicenter study. Mod Pathol 2015; 28: 872-879
• 55 Bosch SL, Teerenstra S, de Wilt JH. et al. Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy 2013; 45: 827-834