Advertisement

Magnitude, Risk Factors, and Factors Associated With Adenoma Miss Rate of Tandem Colonoscopy: A Systematic Review and Meta-analysis

  • Author Footnotes
    ∗ Authors share co-first authorship.
    Shengbing Zhao
    Footnotes
    ∗ Authors share co-first authorship.
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China

    Digestive Endoscopy Center, Changhai Hospital, Naval and Second Military Medical University, Shanghai, China

    National Clinical Research Center for Digestive Diseases, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    ∗ Authors share co-first authorship.
    Shuling Wang
    Footnotes
    ∗ Authors share co-first authorship.
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    ∗ Authors share co-first authorship.
    Peng Pan
    Footnotes
    ∗ Authors share co-first authorship.
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    ∗ Authors share co-first authorship.
    Tian Xia
    Footnotes
    ∗ Authors share co-first authorship.
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China

    Digestive Endoscopy Center, Changhai Hospital, Naval and Second Military Medical University, Shanghai, China
    Search for articles by this author
  • Xin Chang
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Xia Yang
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China

    Department of Gastroenterology, Number 905 Hospital of The Chinese PLA, Shanghai, China
    Search for articles by this author
  • Liliangzi Guo
    Affiliations
    Department of Gastroenterology, Shenzhen People's Hospital, Shenzhen, China
    Search for articles by this author
  • Qianqian Meng
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China

    Digestive Endoscopy Center, Changhai Hospital, Naval and Second Military Medical University, Shanghai, China

    National Quality Control Center of Digestive Endoscopy, Shanghai, China
    Search for articles by this author
  • Fan Yang
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Wei Qian
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Zhichao Xu
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Yuanqiong Wang
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Zhijie Wang
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Lun Gu
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Rundong Wang
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Fangzhou Jia
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China
    Search for articles by this author
  • Jun Yao
    Correspondence
    Reprint requests Address requests for reprints to: Jun Yao, MD, PhD, Department of Gastroenterology, Shenzhen People's Hospital, Shenzhen, People’s Republic of China.
    Affiliations
    Department of Gastroenterology, Shenzhen People's Hospital, Shenzhen, China
    Search for articles by this author
  • Zhaoshen Li
    Correspondence
    Zhaoshen Li, MD, PhD or Yu Bai, MD, PhD, Department of Gastroenterology, Changhai Hospital, Second Military Medical University, Shanghai, People’s Republic of China.
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China

    Digestive Endoscopy Center, Changhai Hospital, Naval and Second Military Medical University, Shanghai, China

    National Clinical Research Center for Digestive Diseases, Shanghai, China

    National Quality Control Center of Digestive Endoscopy, Shanghai, China
    Search for articles by this author
  • Yu Bai
    Correspondence
    Zhaoshen Li, MD, PhD or Yu Bai, MD, PhD, Department of Gastroenterology, Changhai Hospital, Second Military Medical University, Shanghai, People’s Republic of China.
    Affiliations
    Department of Gastroenterology, Changhai Hospital, Second Military Medical University and Naval Medical University, Shanghai, China

    Digestive Endoscopy Center, Changhai Hospital, Naval and Second Military Medical University, Shanghai, China

    National Clinical Research Center for Digestive Diseases, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    ∗ Authors share co-first authorship.
Published:February 06, 2019DOI:https://doi.org/10.1053/j.gastro.2019.01.260

      Background & Aims

      We performed a systematic review and meta-analysis to comprehensively estimate adenoma miss rate (AMR) and advanced AMR (AAMR) and explore associated factors.

      Methods

      We searched the PubMed, Web of Science, and Ovid EMBASE databases for studies published through April 2018 on tandem colonoscopies, with AMR and AAMR as the primary outcomes. We performed meta-regression analyses to identify risk factors and factors associated with outcome. Primary outcomes were AMR and AAMR and secondary outcomes were AMR and AAMR for different locations, sizes, pathologies, morphologies, and populations.

      Results

      In a meta-analysis of 43 publications and more than 15,000 tandem colonoscopies, we calculated miss rates of 26% for adenomas (95% confidence interval [CI] 23%–30%), 9% for advanced adenomas (95% CI 4%–16%), and 27% for serrated polyps (95% CI 16%–40%). Miss rates were high for proximal advanced adenomas (14%; 95% CI 5%–26%), serrated polyps (27%; 95% CI 16%–40%), flat adenomas (34%; 95% CI 24%–45%), and in patients at high risk for colorectal cancer (33%; 95% CI 26%–41%). Miss rates could be decreased by adequate bowel preparation and auxiliary techniques (P = .06; P = .04, and P = .01, respectively). The adenoma detection rate (ADR), adenomas per index colonoscopy, and adenomas per positive index colonoscopy (APPC) were independently associated with AMR (P = .02, P = .01, and P = .008, respectively), whereas APPC was the only factor independently associated with AAMR (P = .006). An APPC value greater than 1.8 was more effective in monitoring AMR (31% vs 15% for AMR P < .0001) than an ADR value of at least 34% (27% vs 17% for AMR; P = .008). The AAMR of colonoscopies with an APPC value below 1.7 was 35%, vs 2% for colonoscopies with an APPC value of at least 1.7 (P = .0005).

      Conclusions

      In a systematic review and meta-analysis, we found that adenomas and advanced adenomas are missed (based on AMR and AAMR) more frequently than previously believed. In addition to ADR, APPC deserves consideration as a complementary indicator of colonoscopy quality, if it is validated in additional studies.

      Graphical abstract

      Keywords

      Abbreviations used in this paper:

      AAMR (advanced adenoma miss rate), ADR (adenoma detection rate), AMR (adenoma miss rate), APIC (adenomas per index colonoscopy), APPC (adenomas per positive index colonoscopy), BBPS (Boston Bowel Preparation Scale), CI (confidence interval), CIR (cecal intubation rate), CRC (colorectal cancer), PDR (polyp detection rate), PPIC (polyps per index colonoscopy), SMR (serrated polyp miss rate), SSA/P (sessile serrated adenoma–polyp)
      To read this article in full you will need to make a payment
      AGA Member Login
      Login with your AGA username and password.
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Siegel R.L.
        • Miller K.D.
        • Fedewa S.A.
        • et al.
        Colorectal cancer statistics, 2017.
        CA Cancer J Clin. 2017; 67: 177-193
        • 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
        • Zauber A.G.
        • Winawer S.J.
        • O’Brien M.J.
        • et al.
        Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths.
        N Engl J Med. 2012; 366: 687-696
        • Peery A.F.
        • Dellon E.S.
        • Lund J.
        • et al.
        Burden of gastrointestinal disease in the United States: 2012 update.
        Gastroenterology. 2012; 143: 1179-1187.e3
        • Bressler B.
        • Paszat L.F.
        • Vinden C.
        • et al.
        Colonoscopic miss rates for right-sided colon cancer: a population-based analysis.
        Gastroenterology. 2004; 127: 452-456
        • Adler J.
        • Robertson D.J.
        Interval colorectal cancer after colonoscopy: exploring explanations and solutions.
        Am J Gastroenterol. 2015; 110 (quiz 1665): 1657-1664
        • Robertson D.J.
        • Lieberman D.A.
        • Winawer S.J.
        • et al.
        Colorectal cancers soon after colonoscopy: a pooled multicohort analysis.
        Gut. 2014; 63: 949-956
        • Pohl H.
        • Robertson D.J.
        Colorectal cancers detected after colonoscopy frequently result from missed lesions.
        Clin Gastroenterol Hepatol. 2010; 8: 858-864
        • Postic G.
        • Lewin D.
        • Bickerstaff C.
        • et al.
        Colonoscopic miss rates determined by direct comparison of colonoscopy with colon resection specimens.
        Am J Gastroenterol. 2002; 97: 3182-3185
        • Pickhardt P.J.
        • Nugent P.A.
        • Mysliwiec P.A.
        • et al.
        Location of adenomas missed by optical colonoscopy.
        Ann Intern Med. 2004; 141: 352-359
        • Cornett D.
        • Barancin C.
        • Roeder B.
        • et al.
        Findings on optical colonoscopy after positive CT colonography exam.
        Am J Gastroenterol. 2008; 103: 2068-2074
        • Lee H.S.
        • Jeon S.W.
        • Park H.Y.
        • et al.
        Improved detection of right colon adenomas with additional retroflexion following two forward-view examinations: a prospective study.
        Endoscopy. 2017; 49: 334-341
        • Lee H.S.
        • Jeon S.W.
        Is retroflexion helpful in detecting adenomas in the right colon?: A single center interim analysis.
        Intest Res. 2015; 13: 326-331
        • Rex D.K.
        • Cutler C.S.
        • Lemmel G.T.
        • et al.
        Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies.
        Gastroenterology. 1997; 112: 24-28
        • van Rijn J.C.
        • Reitsma J.B.
        • Stoker J.
        • et al.
        Polyp miss rate determined by tandem colonoscopy: a systematic review.
        Am J Gastroenterol. 2006; 101: 343-350
        • Rex D.K.
        • Bond J.H.
        • Winawer S.
        • et al.
        Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer.
        Am J Gastroenterol. 2002; 97: 1296-1308
        • Rex D.K.
        • Schoenfeld P.S.
        • Cohen J.
        • et al.
        Quality indicators for colonoscopy.
        Am J Gastroenterol. 2015; 110: 72-90
        • Corley D.A.
        • Jensen C.D.
        • Marks A.R.
        • et al.
        Adenoma detection rate and risk of colorectal cancer and death.
        N Engl J Med. 2014; 370: 1298-1306
        • Singh H.
        • Nugent Z.
        • Demers A.A.
        • et al.
        Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study.
        Am J Gastroenterol. 2010; 105: 2588-2596
        • Baxter N.N.
        • Goldwasser M.A.
        • Paszat L.F.
        • et al.
        Association of colonoscopy and death from colorectal cancer.
        Ann Intern Med. 2009; 150: 1-8
        • Aniwan S.
        • Orkoonsawat P.
        • Viriyautsahakul V.
        • et al.
        The secondary quality indicator to improve prediction of adenoma miss rate apart from adenoma detection rate.
        Am J Gastroenterol. 2016; 111: 723-729
        • Castaneda D.
        • Popov V.B.
        • Verheyen E.
        • et al.
        New technologies improve adenoma detection rate, adenoma miss rate, and polyp detection rate: a systematic review and meta-analysis.
        Gastrointest Endosc. 2018; 88: 209-222.e11
        • Pasha S.F.
        • Leighton J.A.
        • Das A.
        • et al.
        Comparison of the yield and miss rate of narrow band imaging and white light endoscopy in patients undergoing screening or surveillance colonoscopy: a meta-analysis.
        Am J Gastroenterol. 2012; 107 (quiz 371): 363-370
        • Zhao Z.Y.
        • Guan Y.G.
        • Li B.R.
        • et al.
        Detection and miss rates of autofluorescence imaging of adenomatous and polypoid lesions during colonoscopy: a systematic review and meta-analysis.
        Endosc Int Open. 2015; 3: E226-E235
        • Westwood D.A.
        • Alexakis N.
        • Connor S.J.
        Transparent cap-assisted colonoscopy versus standard adult colonoscopy: a systematic review and meta-analysis.
        Dis Colon Rectum. 2012; 55: 218-225
        • Whiting P.F.
        • Rutjes A.W.
        • Westwood M.E.
        • et al.
        QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies.
        Ann Intern Med. 2011; 155: 529-536
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • et al.
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
        BMJ. 2009; 339: b2535
        • Clark B.T.
        • Rustagi T.
        • Laine L.
        What level of bowel prep quality requires early repeat colonoscopy: systematic review and meta-analysis of the impact of preparation quality on adenoma detection rate.
        Am J Gastroenterol. 2014; 109 (quiz 1724): 1714-1723
        • DerSimonian R.
        • Laird N.
        Meta-analysis in clinical trials.
        Control Clin Trials. 1986; 7: 177-188
        • Rex D.K.
        • Chadalawada V.
        • Helper D.J.
        Wide angle colonoscopy with a prototype instrument: impact on miss rates and efficiency as determined by back-to-back colonoscopies.
        Am J Gastroenterol. 2003; 98: 2000-2005
        • Click B.
        • Pinsky P.F.
        • Hickey T.
        • et al.
        Association of colonoscopy adenoma findings with long-term colorectal cancer incidence.
        JAMA. 2018; 319: 2021-2031
        • Heresbach D.
        • Barrioz T.
        • Lapalus M.G.
        • et al.
        Miss rate for colorectal neoplastic polyps: a prospective multicenter study of back-to-back video colonoscopies.
        Endoscopy. 2008; 40: 284-290
        • Stryker S.J.
        • Wolff B.G.
        • Culp C.E.
        • et al.
        Natural history of untreated colonic polyps.
        Gastroenterology. 1987; 93: 1009-1013
        • Regula J.
        • Rupinski M.
        • Kraszewska E.
        • et al.
        Colonoscopy in colorectal-cancer screening for detection of advanced neoplasia.
        N Engl J Med. 2006; 355: 1863-1872
        • Snover D.C.
        Update on the serrated pathway to colorectal carcinoma.
        Hum Pathol. 2011; 42: 1-10
        • Spring K.J.
        • Zhao Z.Z.
        • Karamatic R.
        • et al.
        High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy.
        Gastroenterology. 2006; 131: 1400-1407
        • Bettington M.
        • Walker N.
        • Rosty C.
        • et al.
        Critical appraisal of the diagnosis of the sessile serrated adenoma.
        Am J Surg Pathol. 2014; 38: 158-166
        • Gourevitch R.A.
        • Rose S.
        • Crockett S.D.
        • et al.
        Variation in pathologist classification of colorectal adenomas and serrated polyps.
        Am J Gastroenterol. 2018; 113: 431-439
        • de Wijkerslooth T.
        • Stoop E.
        • Bossuyt P.
        • et al.
        Differences in proximal serrated polyp detection among endoscopists are associated with variability in withdrawal time.
        Gastrointest Endosc. 2013; 77: 617-623
        • Torlakovic E.
        • Skovlund E.
        • Snover D.C.
        • et al.
        Morphologic reappraisal of serrated colorectal polyps.
        Am J Surg Pathol. 2003; 27: 65-81
        • Dik V.K.
        • Gralnek I.M.
        • Segol O.
        • et al.
        Multicenter, randomized, tandem evaluation of EndoRings colonoscopy—results of the CLEVER study.
        Endoscopy. 2015; 47: 1151-1158
        • Gralnek I.M.
        • Siersema P.D.
        • Halpern Z.
        • et al.
        Standard forward-viewing colonoscopy versus full-spectrum endoscopy: an international, multicentre, randomised, tandem colonoscopy trial.
        Lancet Oncol. 2014; 15: 353-360
        • Gessl I.
        • Waldmann E.
        • Penz D.
        • et al.
        Evaluation of adenomas per colonoscopy and adenomas per positive participant as new quality parameters in screening colonoscopy.
        Gastrointest Endosc. 2019; 89: 496-502
        • Abdelfatah M.M.
        • Elhanafi S.
        • Zuckerman M.J.
        • et al.
        Correlation between adenoma detection rate and novel quality indicators for screening colonoscopy. A proposal for quality measures tool kit.
        Scand J Gastroenterol. 2017; 52: 1148-1157
        • Lee T.J.
        • Rutter M.D.
        • Blanks R.G.
        • et al.
        Colonoscopy quality measures: experience from the NHS Bowel Cancer Screening Programme.
        Gut. 2012; 61: 1050-1057
        • Shaukat A.
        • Gravely A.A.
        • Kim A.S.
        • et al.
        Rates of detection of adenoma, sessile serrated adenoma, and advanced adenoma are stable over time and modifiable.
        Gastroenterology. 2019; 156: 816-817
        • Byrne M.F.
        • Chapados N.
        • Soudan F.
        • et al.
        Real-time differentiation of adenomatous and hyperplastic diminutive colorectal polyps during analysis of unaltered videos of standard colonoscopy using a deep learning model.
        Gut. 2019; 68: 94-100
        • Wang Z.
        • Zhao S.
        • Bai Y.
        Artificial intelligence as a third eye in lesion detection by endoscopy.
        Clin Gastroenterol Hepatol. 2018; 16: 1537
        • Patel S.G.
        • Schoenfeld P.
        • Kim H.M.
        • et al.
        Real-time characterization of diminutive colorectal polyp histology using narrow-band imaging: implications for the resect and discard strategy.
        Gastroenterology. 2016; 150: 406-418
        • Brenner H.
        • Chang-Claude J.
        • Seiler C.M.
        • et al.
        Long-term risk of colorectal cancer after negative colonoscopy.
        J Clin Oncol. 2011; 29: 3761-3767