Advertisement

Metachronous colorectal cancers result from missed lesions and non-compliance with surveillance

  • Chantal M.C. le Clercq
    Affiliations
    Division of Gastroenterology and Hepatology, Department of Internal Medicine, Maastricht University Medical Center, Maastricht, The Netherlands

    GROW, School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, The Netherlands
    Search for articles by this author
  • Bjorn Winkens
    Affiliations
    Department of Methodology and Statistics, Maastricht University Medical Center, Maastricht, The Netherlands

    CAPHRI, School for Public Health and Primary Care, Maastricht University Medical Center, Maastricht, The Netherlands
    Search for articles by this author
  • C. Minke Bakker
    Affiliations
    Department of Internal Medicine and Gastroenterology, Atrium Medical Center Heerlen, Heerlen, The Netherlands
    Search for articles by this author
  • Eric T.P. Keulen
    Affiliations
    Department of Internal Medicine and Gastroenterology, Orbis Medical Center Sittard, Sittard, The Netherlands
    Search for articles by this author
  • Geerard L. Beets
    Affiliations
    GROW, School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, The Netherlands

    Department of Surgery, Maastricht University Medical Center, Maastricht, The Netherlands
    Search for articles by this author
  • Ad A.M. Masclee
    Affiliations
    Division of Gastroenterology and Hepatology, Department of Internal Medicine, Maastricht University Medical Center, Maastricht, The Netherlands

    NUTRIM, School for Nutrition, Toxicology and Metabolism, Maastricht University Medical Center, Maastricht, The Netherlands
    Search for articles by this author
  • Silvia Sanduleanu
    Correspondence
    Reprint requests: Silvia Sanduleanu, MD, PhD, Division of Gastroenterology and Hepatology, Department of Internal Medicine, GROW, School for Oncology and Developmental Biology, Maastricht University Medical Center, Postbox 5800, 6202 AZ, Maastricht, The Netherlands.
    Affiliations
    Division of Gastroenterology and Hepatology, Department of Internal Medicine, Maastricht University Medical Center, Maastricht, The Netherlands

    GROW, School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, The Netherlands
    Search for articles by this author
Published:April 02, 2015DOI:https://doi.org/10.1016/j.gie.2014.12.052

      Background

      Several studies examined the rate of colorectal cancer (CRC) developed during colonoscopy surveillance after CRC resection (ie, metachronous CRC [mCRC]), yet the underlying etiology is unclear.

      Objective

      To examine the rate and likely etiology of mCRCs.

      Design

      Population-based, multicenter study. Review of clinical and histopathologic records, including data of the national pathology database and The Netherlands Cancer Registry.

      Setting

      National cancer databases reviewed at 3 hospitals in South-Limburg, The Netherlands.

      Patients

      Total CRC population diagnosed in South-Limburg from January 2001 to December 2010.

      Interventions

      Colonoscopy.

      Main Outcome Measurements

      We defined an mCRC as a second primary CRC, diagnosed >6 months after the primary CRC. By using a modified algorithm to ascribe likely etiology, we classified the mCRCs into cancers caused by non-compliance with surveillance recommendations, inadequate examination, incomplete resection of precursor lesions (CRC in same segment as previous advanced adenoma), missed lesions, or newly developed cancers.

      Results

      We included a total of 5157 patients with CRC, of whom 93 (1.8%) had mCRCs, which were diagnosed on an average of 81 months (range 7-356 months) after the initial CRC diagnosis. Of all mCRCs, 43.0% were attributable to non-compliance with surveillance advice, 43.0% to missed lesions, 5.4% to incompletely resected lesions, 5.4% to newly developed cancers, and 3.2% to inadequate examination. Age-adjusted and sex-adjusted logistic regression analyses showed that mCRCs were significantly smaller in size (odds ratio [OR] 0.8; 95% confidence interval [CI], 0.7-0.9) and more often poorly differentiated (OR 1.7; 95% CI, 1.0-2.8) than were solitary CRCs.

      Limitations

      Retrospective evaluation of clinical data.

      Conclusion

      In this study, 1.8% of all patients with CRC developed mCRCs, and the vast majority were attributable to missed lesions or non-compliance with surveillance advice. Our findings underscore the importance of high-quality colonoscopy to maximize the benefit of post-CRC surveillance.

      Abbreviations:

      CRC (colorectal cancer), mCRC (metachronous CRC), PALGA (national pathology database), TNM (tumor, node, metastasis)
      To read this article in full you will need to make a payment

      Subscribe:

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

      References

        • Ferlay J.
        • Parkin D.M.
        • Steliarova-Foucher E.
        Estimates of cancer incidence and mortality in Europe in 2008.
        Eur J Cancer. 2010; 46: 765-781
        • Soerjomataram I.
        • Lortet-Tieulent J.
        • Parkin D.M.
        • et al.
        Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions.
        Lancet. 2012; 380: 1840-1850
        • Renehan A.G.
        • Egger M.
        • Saunders M.P.
        • et al.
        Impact on survival of intensive follow up after curative resection for colorectal cancer: systematic review and meta-analysis of randomised trials.
        BMJ. 2002; 324: 813
        • Rodriguez-Moranta F.
        • Salo J.
        • Arcusa A.
        • et al.
        Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial.
        J Clin Oncol. 2006; 24: 386-393
        • Bouvier A.M.
        • Latournerie M.
        • Jooste V.
        • et al.
        The lifelong risk of metachronous colorectal cancer justifies long-term colonoscopic follow-up.
        Eur J Cancer. 2008; 44: 522-527
        • Wang T.
        • Cui Y.
        • Huang W.S.
        • et al.
        The role of postoperative colonoscopic surveillance after radical surgery for colorectal cancer: a prospective, randomized clinical study.
        Gastrointest Endosc. 2009; 69: 609-615
        • Figueredo A.
        • Rumble R.B.
        • Maroun J.
        • et al.
        Follow-up of patients with curatively resected colorectal cancer: a practice guideline.
        BMC Cancer. 2003; 3: 26
        • Rex D.K.
        • Kahi C.J.
        • Levin B.
        • et al.
        Guidelines for colonoscopy surveillance after cancer resection: a consensus update by the American Cancer Society and the US Multi-Society Task Force on Colorectal Cancer.
        Gastroenterology. 2006; 130: 1865-1871
        • Cairns S.R.
        • Scholefield J.H.
        • Steele R.J.
        • et al.
        Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002).
        Gut. 2010; 59: 666-689
        • Labianca R.
        • Nordlinger B.
        • Beretta G.D.
        • et al.
        Primary colon cancer: ESMO Clinical Practice Guidelines for diagnosis, adjuvant treatment and follow-up.
        Ann Oncol. 2010; 21: v70-v77
        • Tornqvist A.
        • Ekelund G.
        • Leandoer L.
        Early diagnosis of metachronous colorectal carcinoma.
        ANZ J Surg. 1981; 51: 442-445
        • Green R.J.
        • Metlay J.P.
        • Propert K.
        • et al.
        Surveillance for second primary colorectal cancer after adjuvant chemotherapy: an analysis of Intergroup 0089.
        Ann Intern Med. 2002; 136: 261-269
        • Liu L.
        • Lemmens V.E.
        • De Hingh I.H.
        • et al.
        Second primary cancers in subsites of colon and rectum in patients with previous colorectal cancer.
        Dis Colon Rectum. 2013; 56: 158-168
        • Nava H.R.
        • Pagana T.J.
        Postoperative surveillance of colorectal carcinoma.
        Cancer. 1982; 49: 1043-1047
        • Kronborg O.
        • Hage E.
        • Deichgraeber E.
        The remaining colon after radical surgery for colorectal cancer. The first three years of a prospective study.
        Dis Colon Rectum. 1983; 26: 172-176
        • Luchtefeld M.A.
        • Ross D.S.
        • Zander J.D.
        • et al.
        Late development of metachronous colorectal cancer.
        Dis Colon Rectum. 1987; 30: 180-184
        • Hollington P.
        • Tiong L.
        • Young G.
        Timing and detection of metachronous colorectal cancer.
        ANZ J Surg. 2011; 81: 272-274
        • Chen T.A.
        • Horng J.T.
        • Lin W.C.
        Metachronous colorectal cancer in Taiwan: analyzing 20 years of data from Taiwan Cancer Registry.
        Int J Clin Oncol. 2013; 18: 267-272
        • Mulder S.A.
        • Kranse R.
        • Damhuis R.A.
        • et al.
        The incidence and risk factors of metachronous colorectal cancer: an indication for follow-up.
        Dis Colon Rectum. 2012; 55: 522-531
        • Samadder N.J.
        • Curtin K.
        • Wong J.
        • et al.
        Epidemiology and familial risk of synchronous and metachronous colorectal cancer: a population-based study in Utah.
        Clin Gastroenterol Hepatol. 2014; 12: 2078-2084
        • le Clercq C.M.
        • Bouwens M.W.
        • Rondagh E.J.
        • et al.
        Postcolonoscopy colorectal cancers are preventable: a population-based study.
        Gut. 2014; 63: 957-963
        • Pabby A.
        • Schoen R.E.
        • Weissfeld J.L.
        • et al.
        Analysis of colorectal cancer occurrence during surveillance colonoscopy in the dietary Polyp Prevention Trial.
        Gastrointest Endosc. 2005; 61: 385-391
        • 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
        • le Clercq C.M.
        • Sanduleanu S.
        Interval colorectal cancers: what and why.
        Curr Gastroenterol Rep. 2014; 16: 375
        • Schouten L.J.
        • Jager J.J.
        • van den Brandt P.A.
        Quality of cancer registry data: a comparison of data provided by clinicians with those of registration personnel.
        Br J Cancer. 1993; 68: 974-977
        • Casparie M.
        • Tiebosch A.T.
        • Burger G.
        • et al.
        Pathology databanking and biobanking in The Netherlands, a central role for PALGA, the nationwide histopathology and cytopathology data network and archive.
        Cell Oncol. 2007; 29: 19-24
      1. StatLine CBS. Bevolkingsontwikkeling; levendgeborenen, overledenen en migratie per regio [Dutch]. 2011. http://statline.cbs.nl/statweb/

        • Moertel C.G.
        • Bargen J.A.
        • Dockerty M.B.
        Multiple carcinomas of the large intestine: a review of the literature and a study of 261 cases.
        Gastroenterology. 1958; 34: 85-98
      2. Dutch Institute for Healthcare Improvement. Herziene richtlijn: Follow-up na poliepectomie. Utrecht: Kwaliteitsinstituut voor de Gezondheidszorg CBO, 2002.

      3. Integraal Kankercentrum Nederland (IKNL) [Comprehensive Cancer Center of The Netherlands]. Richtlijn ‘Coloncarcinoom’ 2008;14:29-35 [Dutch]. Oncoline: Cancer Clinical Practice Guidelines. http://www.oncoline.nl/

        • Aronchick C.A.
        • Lipshutz W.H.
        • Wright S.H.
        • et al.
        Validation of an instrument to assess colon cleansing [abstract].
        Am J Gastroenterol. 1999; 94: 2667
        • Kaminski M.F.
        • Regula J.
        • Kraszewska E.
        • et al.
        Quality indicators for colonoscopy and the risk of interval cancer.
        N Engl J Med. 2010; 362: 1795-1803
        • Borrmann R.
        Geschwülste des Magens und Duodenums.
        in: Henke F. Lubarsch O. Handbuch der speziellen pathologischen anatomie und histologie. Springer, Vienna1926: 812-1054
        • Vittinghoff E.
        • McCulloch C.E.
        Relaxing the rule of ten events per variable in logistic and Cox regression.
        Am J Epidemiol. 2007; 165: 710-718
        • Liang K.-Y.
        • Zeger S.L.
        Longitudinal data analysis using generalized linear models.
        Biometrika. 1986; 73: 13-22
        • Zeger S.L.
        • Liang K.Y.
        Longitudinal data analysis for discrete and continuous outcomes.
        Biometrics. 1986; 42: 121-130
        • Huang Y.
        • Gong W.
        • Su B.
        • et al.
        Risk and cause of interval colorectal cancer after colonoscopic polypectomy.
        Digestion. 2012; 86: 148-154
        • Chen T.A.
        Is metachronous colorectal cancer really metachronous?.
        Dis Colon Rectum. 2012; 55: e382
        • Lam A.K.
        • Gopalan V.
        • Carmichael R.
        • et al.
        Metachronous carcinomas in colorectum and its clinicopathological significance.
        Int J Colorectal Dis. 2012; 27: 1303-1310
        • Mulder S.A.
        • Ouwendijk R.J.
        • van Leerdam M.E.
        • et al.
        A nationwide survey evaluating adherence to guidelines for follow-up after polypectomy or treatment for colorectal cancer.
        J Clin Gastroenterol. 2008; 42: 487-492
        • Cone M.M.
        • Beck D.E.
        • Hicks T.E.
        • et al.
        Timing of colonoscopy after resection for colorectal cancer: Are we looking too soon?.
        Dis Colon Rectum. 2013; 56: 1233-1236
        • Battersby N.J.
        • Coupland A.
        • Bouliotis G.
        • et al.
        Metachronous colorectal cancer: a competing risks analysis with consideration for a stratified approach to surveillance colonoscopy.
        J Surg Oncol. 2014; 109: 445-450
        • Couch D.G.
        • Bullen N.
        • Ward-Booth S.E.
        • et al.
        What interval between colorectal cancer resection and first surveillance colonoscopy? An audit of practice and yield.
        Colorectal Dis. 2013; 15: 317-322
        • Baxter N.N.
        • Sutradhar R.
        • Forbes S.S.
        • et al.
        Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer.
        Gastroenterology. 2011; 140: 65-72
        • Bielawska B.
        • Day A.G.
        • Lieberman D.A.
        • et al.
        Risk factors for early colonoscopic perforation include non-gastroenterologist endoscopists: a multivariable analysis.
        Clin Gastroenterol Hepatol. 2014; 12: 85-92
        • Jiang M.
        • Sewitch M.J.
        • Barkun A.N.
        • et al.
        Endoscopist specialty is associated with colonoscopy quality.
        BMC Gastroenterol. 2013; 13: 78
        • de Jonge V.
        • Sint Nicolaas J.
        • Cahen D.L.
        • et al.
        Quality evaluation of colonoscopy reporting and colonoscopy performance in daily clinical practice.
        Gastrointest Endosc. 2012; 75: 98-106
        • Sweetser S.
        • Smyrk T.C.
        • Sugumar A.
        Serrated polyps: critical precursors to colorectal cancer.
        Expert Rev Gastroenterol Hepatol. 2011; 5: 627-635
        • Cali R.L.
        • Pitsch R.M.
        • Thorson A.G.
        • et al.
        Cumulative incidence of metachronous colorectal cancer.
        Dis Colon Rectum. 1993; 36: 388-393
        • 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