CC BY-NC-ND 4.0 · Endosc Int Open 2018; 06(09): E1140-E1148
DOI: 10.1055/a-0650-4296
Original article
Owner and Copyright © Georg Thieme Verlag KG 2018

Colorectal cancer after negative colonoscopy in fecal immunochemical test-positive participants from a colorectal cancer screening program

Liseth Rivero-Sánchez
1   Gastroenterology Department, Hospital Clinic of Barcelona, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Universitat de Barcelona, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
,
Jaume Grau
2   Preventive Medicine and Hospital Epidemiology Department, Hospital Clínic, Barcelona, Spain
,
Josep María Augé
3   Biochemistry Department, Hospital Clinic of Barcelona, Barcelona, Spain
,
Lorena Moreno
4   Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Fundació Clínic per la Recerca Biomèdica, Barcelona, Spain
,
Angels Pozo
2   Preventive Medicine and Hospital Epidemiology Department, Hospital Clínic, Barcelona, Spain
,
Anna Serradesanferm
2   Preventive Medicine and Hospital Epidemiology Department, Hospital Clínic, Barcelona, Spain
,
Mireia Díaz
4   Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Fundació Clínic per la Recerca Biomèdica, Barcelona, Spain
,
Sabela Carballal
1   Gastroenterology Department, Hospital Clinic of Barcelona, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Universitat de Barcelona, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
,
Ariadna Sánchez
1   Gastroenterology Department, Hospital Clinic of Barcelona, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Universitat de Barcelona, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
,
Leticia Moreira
1   Gastroenterology Department, Hospital Clinic of Barcelona, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Universitat de Barcelona, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
,
Francesc Balaguer
1   Gastroenterology Department, Hospital Clinic of Barcelona, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Universitat de Barcelona, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
,
Maria Pellisé
1   Gastroenterology Department, Hospital Clinic of Barcelona, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Universitat de Barcelona, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
,
Antoni Castells
1   Gastroenterology Department, Hospital Clinic of Barcelona, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Universitat de Barcelona, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
,
on behalf of the PROCOLON group › Author Affiliations
Further Information

Publication History

submitted 27 February 2018

accepted after revision 14 May 2018

Publication Date:
11 September 2018 (online)

Abstract

Background and study aims Colorectal cancer (CRC) risk after a positive fecal immunochemical test (FIT) and negative colonoscopy is unknown. We aimed to ascertain the cumulative incidence of post-colonoscopy colorectal cancer (PCCRC) and the manifestation of other lesions that could explain the test positivity in individuals with a negative colonoscopy in a population screening program.

Patients and method Observational study in participants from the first round of a CRC screening program (2010 – 2012) with positive-FIT (≥ 20 μg/g of feces) and negative colonoscopy (without neoplasia). A 42- to 76-month follow-up was performed searching in the National Health Service database and by a brief structured telephonic interview.

Results Of 2659 FIT-positive individuals who underwent colonoscopy, 811 (30.5 %) had a negative colonoscopy. Three PCCRC (0.4 %) were detected within 11 – 28 months and accelerated carcinogenesis was ruled out. Among those with normal colonoscopy, 32 (5 %) relevant lesions were detected at follow-up. One-third of them (11/32) were significant neoplasias: a gastric cancer, a small-bowel lymphoma, six advanced colorectal adenomas, and the three PCCRC. The 21 remaining lesions were inflammatory, vascular disorders, or non-advanced colorectal adenomas.

Conclusions The vast majority (95 %) of individuals did not present any subsequent lesion that could explain the FIT positivity. The very low incidence (0.4 %) and characteristics of PCCRC observed in our cohort reinforce the concept that, although a positive FIT preselects high risk individuals, a high quality colonoscopy is the paramount factor in preventing PCCRC. Improving quality standards of colonoscopy are required to strengthen the current CRC screening strategies.

 
  • References

  • 1 Kahi CJ, Imperiale TF, Juliar BE. et al. Effect of screening colonoscopy on colorectal cancer incidence and mortality. Clin Gastroenterol Hepatol 2009; 7: 770-775
  • 2 Hardcastle JD, Chamberlain JO, Robinson MH. et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 1996; 348: 1472-1477
  • 3 Zorzi M, Fedeli U, Schievano E. et al. Impact on colorectal cancer mortality of screening programmes based on the faecal immunochemical test. Gut 2015; 64: 784-790
  • 4 Imperiale TF, Glowinski EA, Lin-Cooper C. et al. Five-year risk of colorectal neoplasia after negative screening colonoscopy. NEJM 2008; 359: 1218-1224
  • 5 Brenner H, Chang-Claude J, Seiler CM. et al. Long-term risk of colorectal cancer after negative colonoscopy. J Clin Oncol 2011; 29: 3761-3767
  • 6 Steele RJC, McClements P, Watling C. et al. Interval cancers in a FOBT-based colorectal cancer population screening programme: implications for stage, gender and tumour site. Gut 2012; 61: 576-581
  • 7 Morris EJA, Rutter MD, Finan PJ. et al. Post-colonoscopy colorectal cancer (PCCRC) rates vary considerably depending on the method used to calculate them: a retrospective observational population-based study of PCCRC in the English National Health Service. Gut 2015; 64: 1248-1256
  • 8 Sanduleanu S, le Clercq CMC, Dekker E. et al. Definition and taxonomy of interval colorectal cancers: a proposal for standardising nomenclature. Gut 2015; 64: 1257-1267
  • 9 Carroll MRR, Seaman HE, Halloran SP. Tests and investigations for colorectal cancer screening. Clin Biochem 2014; 47: 921-939
  • 10 Raginel T, Puvinel J, Ferrand O. et al. A population-based comparison of immunochemical fecal occult blood tests for colorectal cancer screening. Gastroenterology 2013; 144: 918-925
  • 11 Bjerrum A, Andersen O, Fischer A. et al. Long-term risk of colorectal cancer after negative colonoscopy in a Danish gFOBT screening cohort. Int J Cancer 2017; 141: 503-511
  • 12 Lieberman DA, Rex DK, Winawer SJ. et al. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2012; 143: 844-857
  • 13 van Rijn JC, Reitsma JB, Stoker J. et al. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol 2006; 101: 343-350
  • 14 Kaminski MF, Wieszczy P, Rupinski M. et al. Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death. Gastroenterology 2017; 153: 98-105
  • 15 Rivero-Sánchez L, Pellisé M. [Bowel preparation for colonoscopy. Any significant progress on the horizon?]. Gastroenterol Hepatol 2015; 38: 287-300
  • 16 Jover R, Herráiz M, Alarcón O. et al. Spanish Society of Gastroenterology (AEG) and Spanish Society of Gastrointestinal Endoscopy (SEED) Working Group. Clinical practice guidelines: quality of colonoscopy in colorectal cancer screening. Endoscopy 2012; 44: 444-451
  • 17 Quintero E, Castells A, Bujanda L. et al. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. NEJM 2012; 366: 697-706
  • 18 Jover R, Zapater P, Polanía E. et al. Modifiable endoscopic factors that influence the adenoma detection rate in colorectal cancer screening colonoscopies. Gastrointest Endosc 2013; 77: 381-389.e1
  • 19 Rex DK, Bond JH, Feld AD. Medical-legal risks of incident cancers after clearing colonoscopy. Am J Gastroenterol 2001; 96: 952-957
  • 20 Baxter NN, Sutradhar R, Forbes SS. et al. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology 2011; 140: 65-72
  • 21 Rembacken B, Hassan C, Riemann JF. et al. Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE). Endoscopy 2012; 44: 957-968
  • 22 Kaminski MF, Regula J, Kraszewska E. et al. Quality indicators for colonoscopy and the risk of interval cancer. NEJM 2010; 362: 1795-1803
  • 23 Zaanan A, Meunier K, Sangar F. et al. Microsatellite instability in colorectal cancer: from molecular oncogenic mechanisms to clinical implications. Cell Oncol (Dordr) 2011; 34: 155-176
  • 24 Singh S, Singh PP, Murad MH. et al. Prevalence, risk factors, and outcomes of interval colorectal cancers: A systematic review and meta-analysis. Am J Gastroenterol 2014; 109: 1375-1389
  • 25 Kahi CJ, Hewett DG, Norton DL. et al. Prevalence and variable detection of proximal colon serrated polyps during screening colonoscopy. Clin Gastroenterol Hepatol 2011; 9: 42-46
  • 26 Rockey DC. Occult gastrointestinal bleeding. NEJM 1999; 341: 38-46
  • 27 Samloff IM. Peptic ulcer: the many proteinases of aggression. Gastroenterology 1989; 96: 586-595
  • 28 Wang J, Barbuskaite D, Tozzi M. et al. Proton pump inhibitors inhibit pancreatic secretion: Role of gastric and non-gastric H+/K+-ATPases. PLoS One 2015; 10: e0126432
  • 29 Ibáñez-Sanz G, Garcia M, Rodríguez-Moranta F. et al. Prescription drugs associated with false-positive results when using faecal immunochemical tests for colorectal cancer screening. Dig Liver Dis 2016; 48: 1249-1254
  • 30 Saito H. Screening for colorectal cancer by immunochemical fecal occult blood testing. Jpn J Cancer Res 1996; 87: 1011-1024
  • 31 Ng JY, Chan DKH, Tan KK. Is gastroscopy for fecal immunochemical test positive patients worthwhile?. Int J Colorectal Dis 2017; 32: 95-98
  • 32 Chiang T-H, Lee Y-C, Tu C-H. et al. Performance of the immunochemical fecal occult blood test in predicting lesions in the lower gastrointestinal tract. Can Med Assoc J 2011; 183: 1474-1481
  • 33 Choi JS, Choi JY, Cho HG. et al. Is esophagogastroduodenoscopy necessary in patients with positive fecal occult blood tests and negative colonoscopy?. Scand J Gastroenterol 2013; 48: 657-662
  • 34 Stegeman I, de Wijkerslooth TR, Stoop EM. et al. Risk factors for false positive and for false negative test results in screening with fecal occult blood testing. Int J Cancer 2013; 133: 2408-2414
  • 35 Brenner H, Altenhofen L, Katalinic A. et al. Sojourn time of preclinical colorectal cancer by sex and age: Estimates from the German national screening colonoscopy database. Am J Epidemiol 2011; 174: 1140-1146