Interval post-colonoscopy colorectal cancer following a negative colonoscopy in a fecal immunochemical test-based screening program

Abstract

Background In the Dutch colorectal (CRC) screening program, fecal immunochemical test (FIT)-positive individuals are referred for colonoscopy. If no relevant findings are detected at colonoscopy, individuals are reinvited for FIT screening after 10 years. We aimed to assess CRC risk after a negative colonoscopy in FIT-positive individuals.

Methods In this cross-sectional cohort study, data were extracted from the Dutch national screening information system. Participants with a positive FIT followed by a negative colonoscopy between 2014 and 2018 were included. A negative colonoscopy was defined as a colonoscopy during which no more than one nonvillous, nonproximal adenoma < 10 mm or serrated polyp < 10 mm was found. The main outcome was interval post-colonoscopy CRC (iPCCRC) risk. iPCCRC risk was reviewed against the risk of interval CRC after a negative FIT (FIT IC) with a 2-year screening interval.

Results 35 052 FIT-positive participants had a negative colonoscopy and 24 iPCCRCs were diagnosed, resulting in an iPCCRC risk of 6.85 (95 %CI 4.60–10.19) per 10 000 individuals after a median follow-up of 1.4 years. After 2.5 years of follow-up, age-adjusted iPCCRC risk was approximately equal to FIT IC risk at 2 years.

Conclusion Risk of iPCCRC within a FIT-based CRC screening program was low during the first years after colonos-copy but, after 2.5 years, was the same as the risk in FIT-negative individuals at 2 years, when they are reinvited for screening. Colonoscopy quality may therefore require further improvement and FIT screening interval may need to be reduced after negative colonoscopy.

^‡ Authors contributed equally

Publication History

Received: 02 September 2022

Accepted after revision: 07 July 2023

Article published online:
04 October 2023

• References

• 1 Sung H, Ferlay J, Siegel RL. et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71: 209-249
• 2 Chiu HM, Chen SL, Yen AM. et al. Effectiveness of fecal immunochemical testing in reducing colorectal cancer mortality from the One Million Taiwanese Screening Program. Cancer 2015; 121: 3221-3229
• 3 Giorgi RossiP, Vicentini M, Sacchettini C. et al. Impact of screening program on incidence of colorectal cancer: a cohort study in Italy. Am J Gastroenterol 2015; 110: 1359-1366
• 4 Levin TR, Corley DA, Jensen CD. et al. Effects of organized colorectal cancer screening on cancer incidence and mortality in a large community-based population. Gastroenterology 2018; 155: 1383-1391.e1385
• 5 Schreuders EH, Ruco A, Rabeneck L. et al. Colorectal cancer screening: a global overview of existing programmes. Gut 2015; 64: 1637-1649
• 6 Zorzi M, Hassan C, Capodaglio G. et al. Long-term performance of colorectal cancer screening programmes based on the faecal immunochemical test. Gut 2018; 67: 2124-2130
• 7 Hassan C, Quintero E, Dumonceau JM. et al. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2013; 45: 842-851
• 8 Brenner H, Chang-Claude J, Seiler CM. et al. Does a negative screening colonoscopy ever need to be repeated?. Gut 2006; 55: 1145-1150
• 9 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
• 10 Lakoff J, Paszat LF, Saskin R. et al. Risk of developing proximal versus distal colorectal cancer after a negative colonoscopy: a population-based study. Clin Gastroenterol Hepatol 2008; 6: 1117-1121
• 11 Nishihara R, Wu K, Lochhead P. et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med 2013; 369: 1095-1105
• 12 Pilonis ND, Bugajski M, Wieszczy P. et al. Long-term colorectal cancer incidence and mortality after a single negative screening colonoscopy. Ann Intern Med 2020; 173: 81-91
• 13 Singh H, Turner D, Xue L. et al. Risk of developing colorectal cancer following a negative colonoscopy examination: evidence for a 10-year interval between colonoscopies. JAMA 2006; 295: 2366-2373
• 14 Brenner H, Chang-Claude J, Seiler CM. et al. Interval cancers after negative colonoscopy: population-based case-control study. Gut 2012; 61: 1576-1582
• 15 Munoz Garcia-Borruel M, Hervas Molina AJ, Rodriguez Peralvarez ML. et al. Post-colonoscopy colorectal cancer: characteristics and predictive factors. Med Clin (Barc) 2018; 150: 1-7
• 16 le Clercq CM, Bouwens MW, Rondagh EJ. et al. Postcolonoscopy colorectal cancers are preventable: a population-based study. Gut 2014; 63: 957-963
• 17 Peng SM, Hsu WF, Wang YW. et al. Faecal immunochemical test after negative colonoscopy may reduce the risk of incident colorectal cancer in a population-based screening programme. Gut 2021; 70: 1318-1324
• 18 Adler J, Robertson DJ. Interval colorectal cancer after colonoscopy: exploring explanations and solutions. Am J Gastroenterol 2015; 110: 1657-1664
• 19 Rivero-Sanchez L, Grau J, Auge JM. et al. Colorectal cancer after negative colonoscopy in fecal immunochemical test-positive participants from a colorectal cancer screening program. Endosc Int Open 2018; 6: E1140-E1148
• 20 Unanue-Arza S, Idigoras-Rubio I, Fernandez-Landa MJ. et al. Analysis of post-colonoscopy colorectal cancer and its subtypes in a screening programme. Cancers (Basel) 2021; 13: 5105
• 21 Toes-Zoutendijk E, van Leerdam ME, Dekker E. et al. Real-time monitoring of results during first year of Dutch colorectal cancer screening program and optimization by altering fecal immunochemical test cut-off levels. Gastroenterology 2017; 152: 767-775.e762
• 22 Toes-Zoutendijk E, Bonfrer JMG, Ramakers C. et al. Quality monitoring of a FIT-based colorectal cancer screening program. Clin Chem 2019; 65: 419-426
• 23 van Heijningen EM, Lansdorp-Vogelaar I, van Hees F. et al. Developing a score chart to improve risk stratification of patients with colorectal adenoma. Endoscopy 2016; 48: 563-570
• 24 Casparie M, Tiebosch AT, 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
• 25 Rutter MD, Beintaris I, Valori R. et al. World Endoscopy Organization consensus statements on post-colonoscopy and post-imaging colorectal cancer. Gastroenterology 2018; 155: 909-925.e903
• 26 Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 2010; 17: 1471-1474
• 27 Toes-Zoutendijk E, Kooyker AI, Dekker E. et al. Incidence of interval colorectal cancer after negative results from first-round fecal immunochemical screening tests, by cutoff value and participant sex and age. Clin Gastroenterol Hepatol 2020; 18: 1493-1500
• 28 Portillo I, Idigoras I, Bilbao I. et al. Colorectal cancer screening program using FIT: quality of colonoscopy varies according to hospital type. Endosc Int Open 2018; 6: E1149-E1156
• 29 Lee JK, Jensen CD, Levin TR. et al. Long-term risk of colorectal cancer and related deaths after a colonoscopy with normal findings. JAMA Intern Med 2019; 179: 153-160
• 30 Morris EJ, 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
• 31 Sanduleanu S, le Clercq CM, Dekker E. et al. Definition and taxonomy of interval colorectal cancers: a proposal for standardising nomenclature. Gut 2015; 64: 1257-1267
• 32 van Toledo D, JEG IJ, Bossuyt PMM. et al. Serrated polyp detection and risk of interval post-colonoscopy colorectal cancer: a population-based study. Lancet Gastroenterol Hepatol 2022; 7: 747-754
• 33 Wisse PHA, Erler NS, de Boer SY. et al. Adenoma detection rate and risk for interval postcolonoscopy colorectal cancer in fecal immunochemical test-based screening: a population-based cohort study. Ann Intern Med 2022; 175: 1366-1373
• 34 Sweetser S, Smyrk TC, Sinicrope FA. Serrated colon polyps as precursors to colorectal cancer. Clin Gastroenterol Hepatol 2013; 11: 760-767
• 35 Pohl H, Srivastava A, Bensen SP. et al. Incomplete polyp resection during colonoscopy – results of the complete adenoma resection (CARE) study. Gastroenterology 2013; 144: 74-80.e71
• 36 Sanduleanu S, Dube C. Monitoring postcolonoscopy colorectal cancers: dangerous crossroads?. Gut 2015; 64: 1188-1190
• 37 Vanaclocha-Espi M, Ibanez J, Molina-Barcelo A. et al. Optimal cut-off value for detecting colorectal cancer with fecal immunochemical tests according to age and sex. PLoS One 2021; 16: e0254021
• 38 Bronzwaer MES, Depla A, van Lelyveld N. et al. Quality assurance of colonoscopy within the Dutch national colorectal cancer screening program. Gastrointest Endosc 2019; 89: 1-13
• 39 National Institute for Public Health and the Environment. Protocol for the authorization and auditing of colonoscopy centers and endoscopists. National screening programme for bowel cancer, 9th version. Bilthoven, The Netherlands: National Institute for Public Health and the Environment; 2020