Image-enhanced endoscopy for gastric preneoplastic conditions and neoplastic lesions: a systematic review and meta-analysis

Abstract

Background Image-enhanced endoscopy (IEE) improves the accuracy of endoscopic diagnosis. We aimed to assess the value of IEE for gastric preneoplastic conditions and neoplastic lesions.

Methods Medline and Embase were searched until December 2018. Studies allowing calculation of diagnostic measures were included. Risk of bias and applicability were assessed using QUADAS-2. Subgroup analysis was performed to explore heterogeneity.

Results 44 studies met the inclusion criteria. For gastric intestinal metaplasia (GIM), narrow-band imaging (NBI) obtained a pooled sensitivity and specificity of 0.79 (95 %CI 0.72–0.85) and 0.91 (95 %CI 0.88–0.94) on per-patient basis; on per-biopsy basis, it was 0.84 (95 %CI 0.81–0.86) and 0.95 (95 %CI 0.94–0.96), respectively. Tubulovillous pattern was the most accurate marker to detect GIM and it was effectively assessed without high magnification. For dysplasia, NBI showed a pooled sensitivity and specificity of 0.87 (95 %CI 0.84–0.89) and 0.97 (95 %CI 0.97–0.98) on per-biopsy basis. The use of magnification improved the performance of NBI to characterize early gastric cancer (EGC), especially when the vessel plus surface (VS) classification was applied. Regarding other technologies, trimodal imaging also obtained a high accuracy for dysplasia (sensitivity 0.93 [95 %CI 0.85–0.98], specificity 0.98 [95 %CI 0.92–1.00]). For atrophic gastritis, no specific pattern was noted and none of the technologies reached good diagnostic yield.

Conclusion NBI is highly accurate for GIM and dysplasia. The presence of tubulovillous pattern and the VS classification seem to be useful to detect GIM and characterize EGC, respectively. These features should be used in current practice and to standardize endoscopic criteria for other technologies.

Publikationsverlauf

Eingereicht: 06. März 2020

Angenommen: 28. Mai 2020

Artikel online veröffentlicht:
14. Juli 2020

• References

• 1 East JE, Vleugels JL, Roelandt P. et al. Advanced endoscopic imaging: European Society of Gastrointestinal Endoscopy (ESGE) Technology Review. Endoscopy 2016; 48: 1029-1045
• 2 Barbeiro S, Libanio D, Castro R. et al. Narrow-band imaging: clinical application in gastrointestinal endoscopy. GE Port J Gastroenterol 2018; 26: 40-53
• 3 Dias-Silva D, Pimentel-Nunes P, Magalhaes J. et al. The learning curve for narrow-band imaging in the diagnosis of precancerous gastric lesions by using Web-based video. Gastrointest Endosc 2014; 79: 910-920
• 4 Rodriguez-Carrasco M, Libanio D, Dinis-Ribeiro M. et al. Where should gastric biopsies be performed when areas of intestinal metaplasia are observed?. Endosc Int Open 2019; 7: 1636-1639
• 5 Uedo N, Ishihara R, Iishi H. et al. A new method of diagnosing gastric intestinal metaplasia: narrow-band imaging with magnifying endoscopy. Endoscopy 2006; 38: 819-824
• 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 (including video). Endoscopy 2004; 36: 1080-1084
• 7 Tanaka K, Toyoda H, Kadowaki S. et al. Surface pattern classification by enhanced-magnification endoscopy for identifying early gastric cancers. Gastrointest Endosc 2008; 67: 430-437
• 8 Capelle LG, Haringsma J, de Vries AC. et al. Narrow band imaging for the detection of gastric intestinal metaplasia and dysplasia during surveillance endoscopy. Dig Dis Sci 2010; 55: 3442-3448
• 9 Rerknimitr R, Imraporn B, Klaikeaw N. et al. Non-sequential narrow band imaging for targeted biopsy and monitoring of gastric intestinal metaplasia. World J Gastroenterol 2011; 17: 1336-1342
• 10 Pimentel-Nunes P, Dinis-Ribeiro M, Soares JB. et al. A multicenter validation of an endoscopic classification with narrow band imaging for gastric precancerous and cancerous lesions. Endoscopy 2012; 44: 236-246
• 11 Savarino E, Corbo M, Dulbecco P. et al. Narrow-band imaging with magnifying endoscopy is accurate for detecting gastric intestinal metaplasia. World J Gastroenterol 2013; 19: 2668-2675
• 12 Boeriu A, Boeriu C, Drasovean S. et al. Narrow-band imaging with magnifying endoscopy for the evaluation of gastrointestinal lesions. World J Gastrointest Endosc 2015; 7: 110-120
• 13 Kikuste I, Marques-Pereira R, Monteiro-Soares M. et al. Systematic review of the diagnosis of gastric premalignant conditions and neoplasia with high-resolution endoscopic technologies. Scand J Gastroenterol 2013; 48: 1108-1117
• 14 Tahara T, Shibata T, Nakamura M. et al. Gastric mucosal pattern by using magnifying narrow-band imaging endoscopy clearly distinguishes histological and serological severity of chronic gastritis. Gastrointest Endosc 2009; 70: 246-253
• 15 An JK, Song GA, Kim GH. et al. Marginal turbid band and light blue crest, signs observed in magnifying narrow-band imaging endoscopy, are indicative of gastric intestinal metaplasia. BMC Gastroenterol 2012; 12: 169
• 16 Bansal A, Ulusarac O, Mathur S. et al. Correlation between narrow band imaging and nonneoplastic gastric pathology: a pilot feasibility trial. Gastrointest Endosc 2008; 67: 210-216
• 17 Liu H, Wu J, Lin XC. et al. Evaluating the diagnoses of gastric antral lesions using magnifying endoscopy with narrow-band imaging in a Chinese population. Dig Dis Sci 2014; 59: 1513-1519
• 18 Ang TL, Pittayanon R, Lau JY. et al. A multicenter randomized comparison between high-definition white light endoscopy and narrow band imaging for detection of gastric lesions. Eur J Gastroenterol Hepatol 2015; 27: 1473-1478
• 19 Lage J, Pimentel-Nunes P, Figueiredo PC. et al. Light-NBI to identify high-risk phenotypes for gastric adenocarcinoma: do we still need biopsies?. Scand J Gastroenterol 2016; 51: 501-506
• 20 Pimentel-Nunes P, Libanio D, Lage J. et al. A multicenter prospective study of the real-time use of narrow-band imaging in the diagnosis of premalignant gastric conditions and lesions. Endoscopy 2016; 48: 723-730
• 21 Kanemitsu T, Yao K, Nagahama T. et al. Extending magnifying NBI diagnosis of intestinal metaplasia in the stomach: the white opaque substance marker. Endoscopy 2017; 49: 529-535
• 22 Sha J, Wang P, Zhu B. et al. Acetic acid enhanced narrow band imaging for the diagnosis of gastric intestinal metaplasia. PloS One 2017; 12: e0170957
• 23 Tahara T, Tahara S, Tuskamoto T. et al. Magnifying NBI patterns of gastric mucosa after Helicobacter pylori eradication and its potential link to the gastric cancer risk. Dig Dis Sci 2017; 62: 2421-2427
• 24 Sobrino-Cossio S, Abdo Francis JM, Emura F. et al. Efficacy of narrow-band imaging for detecting intestinal metaplasia in adult patients with symptoms of dyspepsia. Rev Gastroenterol Mex 2018; 83: 245-252
• 25 Esposito G, Pimentel-Nunes P, Angeletti S. et al. Endoscopic grading of gastric intestinal metaplasia (EGGIM): a multicenter validation study. Endoscopy 2019; 51: 515-521
• 26 Lim LG, Yeoh KG, Srivastava S. et al. Comparison of probe-based confocal endomicroscopy with virtual chromoendoscopy and white-light endoscopy for diagnosis of gastric intestinal metaplasia. Surg Endosc 2013; 27: 4649-4655
• 27 Ezoe Y, Muto M, Horimatsu T. et al. Magnifying narrow-band imaging versus magnifying white-light imaging for the differential diagnosis of gastric small depressive lesions: a prospective study. Gastrointest Endosc 2010; 71: 477-484
• 28 Ezoe Y, Muto M, Uedo N. et al. Magnifying narrowband imaging is more accurate than conventional white-light imaging in diagnosis of gastric mucosal cancer. Gastroenterology 2011; 141: 2017-2025
• 29 Kato M, Kaise M, Yonezawa J. et al. Magnifying endoscopy with narrow-band imaging achieves superior accuracy in the differential diagnosis of superficial gastric lesions identified with white-light endoscopy: a prospective study. Gastrointest Endosc 2010; 72: 523-529
• 30 Wang SF, Yang YS, Yuan J. et al. Magnifying endoscopy with narrow-band imaging may improve diagnostic accuracy of differentiated gastric intraepithelial neoplasia: a feasibility study. Chin Med J 2012; 125: 728-732
• 31 Li HY, Dai J, Xue HB. et al. Application of magnifying endoscopy with narrow-band imaging in diagnosing gastric lesions: a prospective study. Gastrointest Endosc 2012; 76: 1124-1132
• 32 Miwa K, Doyama H, Ito R. et al. Can magnifying endoscopy with narrow band imaging be useful for low grade adenomas in preoperative biopsy specimens?. Gastric Cancer 2012; 15: 170-178
• 33 Tsuji Y, Ohata K, Sekiguchi M. et al. Magnifying endoscopy with narrow-band imaging helps determine the management of gastric adenomas. Gastric Cancer 2012; 15: 414-418
• 34 Maki S, Yao K, Nagahama T. et al. Magnifying endoscopy with narrow-band imaging is useful in the differential diagnosis between low-grade adenoma and early cancer of superficial elevated gastric lesions. Gastric Cancer 2013; 16: 140-146
• 35 Kawai T, Yanagizawa K, Naito S. et al. Evaluation of gastric cancer diagnosis using new ultrathin transnasal endoscopy with narrow-band imaging: preliminary study. J Gastroenterol Hepatol 2014; 29: 33-36
• 36 Tao G, Xing-Hua L, Ai-Ming Y. et al. Enhanced magnifying endoscopy for differential diagnosis of superficial gastric lesions identified with white-light endoscopy. Gastric Cancer 2014; 17: 122-129
• 37 Yamada S, Doyama H, Yao K. et al. An efficient diagnostic strategy for small, depressed early gastric cancer with magnifying narrow-band imaging: a post-hoc analysis of a prospective randomized controlled trial. Gastrointest Endosc 2014; 79: 55-63
• 38 Yao K, Doyama H, Gotoda T. et al. Diagnostic performance and limitations of magnifying narrow-band imaging in screening endoscopy of early gastric cancer: a prospective multicenter feasibility study. Gastric Cancer 2014; 17: 669-679
• 39 Fujiwara S, Yao K, Nagahama T. et al. Can we accurately diagnose minute gastric cancers (</=5 mm)? Chromoendoscopy (CE) vs magnifying endoscopy with narrow band imaging (M-NBI). Gastric Cancer 2015; 18: 590-596
• 40 Gong S, Xue HB, Ge ZZ. et al. Value of magnifying endoscopy with narrow-band imaging and confocal laser endomicroscopy in detecting gastric cancerous lesions. Medicine 2015; 94: e1930
• 41 Yu H, Yang AM, Lu XH. et al. Magnifying narrow-band imaging endoscopy is superior in diagnosis of early gastric cancer. World J Gastroenterol 2015; 21: 9156-9162
• 42 Nonaka T, Inamori M, Honda Y. et al. Can magnifying endoscopy with narrow-band imaging discriminate between carcinomas and low grade adenomas in gastric superficial elevated lesions?. Endosc Int Open 2016; 4: 1203-1210
• 43 Inoue T, Uedo N, Ishihara R. et al. Autofluorescence imaging videoendoscopy in the diagnosis of chronic atrophic fundal gastritis. J Gastroenterol 2010; 45: 45-51
• 44 So J, Rajnakova A, Chan YH. et al. Endoscopic tri-modal imaging improves detection of gastric intestinal metaplasia among a high-risk patient population in Singapore. Dig Dis Sci 2013; 58: 3566-3575
• 45 Shi J, Jin N, Li Y. et al. Clinical study of autofluorescence imaging combined with narrow band imaging in diagnosing early gastric cancer and precancerous lesions. J BUON 2015; 20: 1215-1222
• 46 Kobayashi M, Tajiri H, Seike E. et al. Detection of early gastric cancer by a real-time autofluorescence imaging system. Cancer Lett 2001; 165: 155-159
• 47 Kato M, Kaise M, Yonezawa J. et al. Autofluorescence endoscopy versus conventional white light endoscopy for the detection of superficial gastric neoplasia: A prospective comparative study. Endoscopy 2007; 39: 937-941
• 48 Kato M, Kaise M, Yonezawa J. et al. Trimodal imaging endoscopy may improve diagnostic accuracy of early gastric neoplasia: a feasibility study. Gastrointest Endosc 2009; 70: 899-906
• 49 Imaeda H, Hosoe N, Kashiwagi K. et al. Surveillance using trimodal imaging endoscopy after endoscopic submucosal dissection for superficial gastric neoplasia. World J Gastroenterol 2014; 20: 16311-16317
• 50 Li CQ, Li Y, Zuo XL. et al. Magnified and enhanced computed virtual chromoendoscopy in gastric neoplasia: a feasibility study. World J Gastroenterol 2013; 19: 4221-4227
• 51 Pittayanon R, Rerknimitr R, Wisedopas N. et al. Flexible spectral imaging color enhancement plus probe-based confocal laser endomicroscopy for gastric intestinal metaplasia detection. J Gastroenterol Hepatol 2013; 28: 1004-1009
• 52 Dohi O, Yagi N, Majima A. et al. Diagnostic ability of magnifying endoscopy with blue laser imaging for early gastric cancer: a prospective study. Gastric Cancer 2017; 20: 297-303
• 53 Chen H, Liu Y, Lu Y. et al. Ability of blue laser imaging with magnifying endoscopy for the diagnosis of gastric intestinal metaplasia. Lasers Med Sci 2018; 33: 1757-1762
• 54 Chen H, Wu X, Liu Y. et al. Blue laser imaging with acetic acid enhancement improved the detection rate of gastric intestinal metaplasia. Lasers Med Sci 2019; 34: 555-559
• 55 Fukuda H, Miura Y, Osawa H. et al. Linked color imaging can enhance recognition of early gastric cancer by high color contrast to surrounding gastric intestinal metaplasia. J Gastroenterol 2019; 54: 396-406
• 56 Ono S, Kato M, Tsuda M. et al. Lavender color in linked color imaging enables noninvasive detection of gastric intestinal metaplasia. Digestion 2018; 98: 222-230
• 57 Yao K, Anagnostopoulos GK, Ragunath K. Magnifying endoscopy for diagnosing and delineating early gastric cancer. Endoscopy 2009; 41: 462-467
• 58 Bray F, Ferlay J, Soerjomataram I. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394-424
• 59 Pimentel-Nunes P, Libanio D, Marcos-Pinto R. et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy 2019; 51: 365-388
• 60 Areia M, Spaander MC, Kuipers EJ. et al. Endoscopic screening for gastric cancer: A cost-utility analysis for countries with an intermediate gastric cancer risk. United European Gastroenterol J 2018; 6: 192-202
• 61 Dinis-Ribeiro M, Areia M, de Vries AC. et al. Management of precancerous conditions and lesions in the stomach (MAPS): guideline from the European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter Study Group (EHSG), European Society of Pathology (ESP), and the Sociedade Portuguesa de Endoscopia Digestiva (SPED). Endoscopy 2012; 44: 74-94
• 62 Pimentel-Nunes P, Libanio D, Dinis-Ribeiro M. Evaluation and management of gastric superficial neoplastic lesions. GE Port J Gastroenterol 2017; 24: 8-21
• 63 Banks M, Graham D, Jansen M. et al. British Society of Gastroenterology guidelines on the diagnosis and management of patients at risk of gastric adenocarcinoma. Gut 2019; 68: 1545-1575
• 64 Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T. et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2015; 47: 829-854
• 65 Libanio D, Braga V, Ferraz S. et al. Prospective comparative study of endoscopic submucosal dissection and gastrectomy for early neoplastic lesions including patients' perspectives. Endoscopy 2019; 51: 30-39
• 66 Kaminishi M, Yamaguchi H, Nomura S. et al. Endoscopic classification of chronic gastritis based on a pilot study by the research society for gastritis. Dig Endosc 2002; 14: 138-151
• 67 Nagata N, Shimbo T, Akiyama J. et al. Predictability of gastric intestinal metaplasia by mottled patchy erythema seen on endoscopy. Gastroenterology Res 2011; 4: 203-209
• 68 Hirasawa T, Aoyama K, Tanimoto T. et al. Application of artificial intelligence using a convolutional neural network for detecting gastric cancer in endoscopic images. Gastric Cancer 2018; 21: 653-660
• 69 Mori Y, Kudo SE, Mohmed HEN. et al. Artificial intelligence and upper gastrointestinal endoscopy: Current status and future perspective. Dig Endosc 2019; 31: 378-388
• 70 Song J, Zhang J, Wang J. et al. Meta-analysis: narrow band imaging for diagnosis of gastric intestinal metaplasia. PloS One 2014; 9: e94869
• 71 Wang L, Huang W, Du J. et al. Diagnostic yield of the light blue crest sign in gastric intestinal metaplasia: a meta-analysis. PloS One 2014; 9: e92874
• 72 Muto M, Yao K. et al. Magnifying endoscopy simple diagnostic algorithm for early gastric cancer (MESDA-G). Dig Endosc 2016; 28: 379-393
• 73 Castro R, Rodriguez M, Libânio D. et al. Reliability and accuracy of blue light imaging for staging of intestinal metaplasia in the stomach. Scand J Gastroenterol 2019; 54: 1301-1305