Low value of second-look endoscopy for detecting residual colorectal cancer after endoscopic removal

Published:February 25, 2020DOI:

      Background and Aims

      Endoscopic resection is often feasible for submucosal invasive colorectal cancers (T1 CRCs) and usually judged as complete. If histology casts doubt on the radicality of resection margins, adjuvant surgical resection is advised, although residual intramural cancer is found in only 5% to 15% of patients. We assessed the sensitivity of biopsy specimens from the resection area for residual intramural cancer as a potential tool to estimate the preoperative risk of residual intramural cancer in patients without risk factors for lymph node metastasis (LNM).


      In this multicenter prospective cohort study, patients with complete endoscopic resection of T1 CRC, scheduled for adjuvant resection due to pathologically unclear resection margins, but absent risk factors for LNM, were asked to consent to second-look endoscopy with biopsies. The results were compared with the pathology results of the surgical resection specimen (criterion standard).


      One hundred three patients were included. In total, 85% of resected lesions were unexpectedly malignant, and 45% were removed using a piecemeal resection technique. Sixty-four adjuvant surgical resections and 39 local full-thickness resections were performed. Residual intramural cancer was found in 7 patients (6.8%). Two of these patients had cancer in second-look biopsy specimens, resulting in a sensitivity of 28% (95% confidence interval, <58%). The preoperative risk of residual intramural cancer in the case of negative biopsy specimens was not significantly reduced (P = .61).


      The sensitivity of second-look endoscopy with biopsies for residual intramural cancer after endoscopic resection of CRC is low. Therefore, it should not be used in the decision whether or not to perform adjuvant resection. (Clinical trial registration number: NCT02328664.)


      CRC (colorectal cancer), LNM (lymph node metastasis)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Gastrointestinal Endoscopy
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Anonymous
        National Cancer Registry, The Netherlands.
        (Available at:) (Accessed January 6, 2019)
        • Larsen M.B.
        • Njor S.
        • Ingeholm P.
        • et al.
        Effectiveness of colorectal cancer screening in detecting earlier-stage disease-a nationwide cohort study in Denmark.
        Gastroenterology. 2018; 155: 99-106
        • Bosch S.L.
        • Teerenstra S.
        • de Wilt J.H.
        • 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
        • Beaton C.
        • Twine C.P.
        • Williams G.L.
        • et al.
        Systematic review and meta-analysis of histopathological factors influencing the risk of lymph node metastasis in early colorectal cancer.
        Colorectal Dis. 2013; 15: 788-797
        • Lugli A.
        • Kirsch R.
        • Ajioka Y.
        • et al.
        Recommendations for reporting tumor budding in colorectal cancer based on the International Tumor Budding Consensus Conference (ITBCC) 2016.
        Mod Pathol. 2017; 30: 1299-1311
        • Yasue C.
        • Chino A.
        • Takamatsu M.
        • et al.
        Pathological risk factors and predictive endoscopic factors for lymph node metastasis of T1 colorectal cancer: a single-center study of 846 lesions.
        J Gastroenterol. 2019; 54: 708-717
      1. Dutch Working Group for Gastrointestinal Tumours: National Guideline on the treatment of colorectal carcinoma, version 3.0.
        2014. p: 34-37
        • Meining A.
        • von Delius S.
        • Eames T.M.
        • et al.
        Risk factors for unfavorable outcomes after endoscopic removal of submucosal invasive colorectal tumors.
        Clin Gastroenterol Hepatol. 2011; 9: 590-594
        • Benizri E.I.
        • Bereder J.M.
        • Rahili A.
        • et al.
        Additional colectomy after colonoscopic polypectomy for T1 colon cancer: a fine balance between oncologic benefit and operative risk.
        Int J Colorectal Dis. 2012; 27: 1473-1478
        • Hassan C.
        • Zullo A.
        • Risio M.
        • et al.
        Histologic risk factors and clinical outcome in colorectal malignant polyp: a pooled-data analysis.
        Dis Colon Rectum. 2005; 48: 1588-1596
        • Bagnall N.M.
        • Pring E.T.
        • Malietzis G.
        • et al.
        Perioperative risk prediction in the era of enhanced recovery: a comparison of POSSUM, ACPGBI, and E-PASS scoring systems in major surgical procedures of the colorectal surgeon.
        Int J Colorectal Dis. 2018; 33: 1627-1634
        • Kuellmer A.
        • Mueller J.
        • Caca K.
        • et al.
        Endoscopic full-thickness resection for early colorectal cancer.
        Gastrointest Endosc. 2019; 89 (e1181): 1180-1189
        • Serra-Aracil X.
        • Pallisera-Lloveras A.
        • Mora-Lopez L.
        • et al.
        Transanal endoscopic surgery is effective and safe after endoscopic polypectomy of potentially malignant rectal polyps with questionable margins.
        Colorectal Dis. 2018; 20: 789-796
        • Leicher L.W.
        • de Vos Tot Nederveen Cappel W.H.
        • van Westreenen H.L.
        Limited endoscopic-assisted wedge resection for excision of colon polyps.
        Dis Colon Rectum. 2017; 60: 299-302
      2. Palga Dutch Foundation of the Pathological Anatomy National Automated Archive.
        Protocol colonic biopsy-TEM (1). January 2015; (Available at: Accessed August 13, 2019)
      3. Palga Dutch Foundation of the Pathological Anatomy National Automated Archive.
        Protocol colorectum., February 2015 (Available at: Accessed August 13, 2019)
        • Webber C.
        • Gospodarowicz M.
        • Sobin L.H.
        • et al.
        Improving the TNM classification: findings from a 10-year continuous literature review.
        Int J Cancer. 2014; 135: 371-378
        • Shin J.W.
        • Han K.S.
        • Hyun J.H.
        • et al.
        Risk of recurrence after endoscopic resection of early colorectal cancer with positive margins.
        Endoscopy. 2018; 50: 241-247
        • Backes Y.
        • de Vos Tot Nederveen Cappel W.H.
        • van Bergeijk J.
        • et al.
        Risk for incomplete resection after macroscopic radical endoscopic resection of t1 colorectal cancer: a multicenter cohort study.
        Am J Gastroenterol. 2017; 112: 785-796
        • Ueno H.
        • Mochizuki H.
        • Hashiguchi Y.
        • et al.
        Risk factors for an adverse outcome in early invasive colorectal carcinoma.
        Gastroenterology. 2004; 127: 385-394
        • Kessels K.
        • Backes Y.
        • Elias S.G.
        • et al.
        Pedunculated morphology of T1 colorectal tumors associates with reduced risk of adverse outcome.
        Clin Gastroenterol Hepatol. 2019; 17 (e1111): 1112-1120
        • Vermeer N.C.A.
        • Backes Y.
        • Snijders H.S.
        • et al.
        National cohort study on postoperative risks after surgery for submucosal invasive colorectal cancer.
        BJS Open. 2019; 3: 210-217
        • Desomer L.
        • Tutticci N.
        • Tate D.J.
        • et al.
        A standardized imaging protocol is accurate in detecting recurrence after EMR.
        Gastrointest Endosc. 2017; 85: 518-526