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Canadian Journal of Gastroenterology and Hepatology
Volume 2016, Article ID 2878149, 18 pages
http://dx.doi.org/10.1155/2016/2878149
Review Article

Colorectal Cancer Screening in Average Risk Populations: Evidence Summary

1Prevention and Cancer Control, Cancer Care Ontario, Toronto, ON, Canada
2Department of Medicine, Sunnybrook Health Sciences Centre, Toronto, ON, Canada
3Institute for Clinical Evaluative Sciences, Toronto, ON, Canada
4Institute of Health Policy, Management and Evaluation, Dalla Lana School of Public Health, University of Toronto, Toronto, ON, Canada
5Department of Medicine, University of Toronto, Toronto, ON, Canada
6Program in Evidence-Based Care, Cancer Care Ontario, Hamilton, ON, Canada
7Department of Surgery, St. Michael’s Hospital, Toronto, ON, Canada
8Li Ka Shing Knowledge Institute, St. Michael’s Hospital, Toronto, ON, Canada
9Department of Medicine, Division of Gastroenterology, University of Ottawa, The Ottawa Hospital, Ottawa, ON, Canada
10William Osler Health Centre, Etobicoke, ON, Canada
11Vaughan Endoscopy Clinic, Vaughan, ON, Canada
12Northeast Cancer Centre Health Sciences North/Horizon Santé-Nord, Sudbury Outpatient Centre, Sudbury, ON, Canada
13American Society of Clinical Oncology, Alexandria, VA, USA

Received 1 April 2016; Accepted 29 June 2016

Academic Editor: Mark Borgaonkar

Copyright © 2016 Jill Tinmouth et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Colorectal Cancer Association of Canada, 2016, http://www.colorectal-cancer.ca/en/just-the-facts/colorectal/.
  2. World Cancer Research Fund International website, 2016, http://www.wcrf.org/int/cancer-facts-figures/data-specific-cancers/colorectal-cancer-statistics.
  3. H. Brenner, J. Chang-Claude, C. M. Seiler, and M. Hoffmeister, “Interval cancers after negative colonoscopy: population-based case-control study,” Gut, vol. 61, no. 11, pp. 1576–1582, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. O. Kronborg, C. Fenger, J. Olsen, O. D. Jørgensen, and O. Søndergaard, “Randomised study of screening for colorectal cancer with faecal-occult-blood test,” The Lancet, vol. 348, no. 9040, pp. 1467–1471, 1996. View at Publisher · View at Google Scholar · View at Scopus
  5. E. J. A. Morris, L. E. Whitehouse, T. Farrell et al., “A retrospective observational study examining the characteristics and outcomes of tumours diagnosed within and without of the English NHS Bowel Cancer Screening Programme,” British Journal of Cancer, vol. 107, no. 5, pp. 757–764, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Segnan, P. Armaroli, L. Bonelli et al., “Once-only sigmoidoscopy in colorectal cancer screening: Follow-up findings of the italian randomized controlled trial - SCORE,” Journal of the National Cancer Institute, vol. 103, no. 17, pp. 1310–1322, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. Canadian Quality Cancer of Ontario, 2016, http://www.csqi.on.ca/by_patient_journey/screening/colorectal_screening_participation.
  8. J. Tinmouth, E. Vella, NN. Baxter et al., “Colorectal cancer screening in average risk populations: evidence summary,” Program in Evidence-Based Care Evidence Summary 15-14, CCO, Toronto, Canada, 2015, https://www.cancercare.on.ca/toolbox/qualityguidelines/clin-program/screening-ebs/. View at Google Scholar
  9. G. Guyatt, A. D. Oxman, E. A. Akl et al., “GRADE guidelines: 1. Introduction—GRADE evidence profiles and summary of findings tables,” Journal of Clinical Epidemiology, vol. 64, no. 4, pp. 383–394, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. Ø. Holme, M. Bretthauer, A. Fretheim, J. Odgaard-Jensen, and G. Hoff, “Flexible sigmoidoscopy versus faecal occult blood testing for colorectal cancer screening in asymptomatic individuals,” Cochrane Database of Systematic Reviews, vol. 9, Article ID CD009259, 2013. View at Google Scholar · View at Scopus
  11. J. Kewenter and H. Brevinge, “Endoscopic and surgical complications of work-up in screening for colorectal cancer,” Diseases of the Colon and Rectum, vol. 39, no. 6, pp. 676–680, 1996. View at Publisher · View at Google Scholar · View at Scopus
  12. O. Kronborg, O. D. Jørgensen, C. Fenger, and M. Rasmussen, “Randomized study of biennial screening with a faecal occult blood test: results after nine screening rounds,” Scandinavian Journal of Gastroenterology, vol. 39, no. 9, pp. 846–851, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Lindholm, H. Brevinge, and E. Haglind, “Survival benefit in a randomized clinical trial of faecal occult blood screening for colorectal cancer,” British Journal of Surgery, vol. 95, no. 8, pp. 1029–1036, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. J. S. Mandel, J. H. Bond, T. R. Church et al., “Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study,” The New England Journal of Medicine, vol. 328, no. 19, pp. 1365–1371, 1993. View at Publisher · View at Google Scholar · View at Scopus
  15. J. S. Mandel, T. R. Church, J. H. Bond et al., “The effect of fecal occult-blood screening on the incidence of colorectal cancer,” The New England Journal of Medicine, vol. 343, no. 22, pp. 1603–1607, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. J. S. Mandel, T. R. Church, F. Ederer, and J. H. Bond, “Colorectal cancer mortality: effectiveness of biennial screening for fecal occult blood,” Journal of the National Cancer Institute, vol. 91, no. 5, pp. 434–437, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Paimela, N. Malila, T. Palva, T. Hakulinen, H. Vertio, and H. Järvinen, “Early detection of colorectal cancer with faecal occult blood test screening,” British Journal of Surgery, vol. 97, no. 10, pp. 1567–1571, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. M. H. E. Robinson, J. D. Hardcastle, S. M. Moss et al., “The risks of screening: data from the Nottingham randomised controlled trial of faecal occult blood screening for colorectal cancer,” Gut, vol. 45, no. 4, pp. 588–592, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. J. H. Scholefield, S. M. Moss, C. M. Mangham, D. K. Whynes, and J. D. Hardcastle, “Nottingham trial of faecal occult blood testing for colorectal cancer: a 20-year follow-up,” Gut, vol. 61, no. 7, pp. 1036–1040, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Shaukat, S. J. Mongin, M. S. Geisser et al., “Long-term mortality after screening for colorectal cancer,” The New England Journal of Medicine, vol. 369, no. 12, pp. 1106–1114, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. Ø. Holme, M. Løberg, M. Kalager et al., “Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial,” The Journal of the American Medical Association, vol. 312, no. 6, pp. 606–615, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. W. S. Atkin, C. F. Cook, J. Cuzick et al., “Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial,” The Lancet, vol. 359, no. 9314, pp. 1291–300, 2002. View at Publisher · View at Google Scholar
  23. W. S. Atkin, R. Edwards, I. Kralj-Hans et al., “Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial,” The Lancet, vol. 375, no. 9726, pp. 1624–1633, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Hoff, J. Sauar, M. H. Vatn et al., “Polypectomy of adenomas in the prevention of colorectal cancer: 10 years' follow-up of the Telemark Polyp Study I. A prospective, controlled population study,” Scandinavian Journal of Gastroenterology, vol. 31, no. 10, pp. 1006–1010, 1996. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Hoff, T. Grotmol, E. Skovlund, and M. Bretthauer, “Risk of colorectal cancer seven years after flexible sigmoidoscopy screening: randomised controlled trial,” British Medical Journal, vol. 338, Article ID b1846, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. R. E. Schoen, P. F. Pinsky, J. L. Weissfeld et al., “Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy,” The New England Journal of Medicine, vol. 366, no. 25, pp. 2345–2357, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Segnan, C. Senore, B. Andreoni et al., “Baseline findings of the Italian multicenter randomized controlled trial of ‘once-only sigmoidoscopy’—SCORE,” Journal of the National Cancer Institute, vol. 94, no. 23, pp. 1763–1772, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Thiis-Evensen, G. S. Hoff, J. Sauar, F. Langmark, B. M. Majak, and M. H. Vatn, “Population-based surveillance by colonoscopy: effect on the incidence of colorectal cancer: Telemark Polyp Study I,” Scandinavian Journal of Gastroenterology, vol. 34, no. 4, pp. 414–420, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Brenner, C. Stock, and M. Hoffmeister, “Effect of screening sigmoidoscopy and screening colonoscopy on colorectal cancer incidence and mortality: systematic review and meta-analysis of randomised controlled trials and observational studies,” British Medical Journal, vol. 348, article g2467, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Niv, R. Hazazi, Z. Levi, and G. Fraser, “Screening colonoscopy for colorectal cancer in asymptomatic people: a meta-analysis,” Digestive Diseases and Sciences, vol. 53, no. 12, pp. 3049–3054, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. H.-M. Chiu, H.-P. Wang, Y.-C. Lee et al., “A prospective study of the frequency and the topographical distribution of colon neoplasia in asymptomatic average-risk Chinese adults as determined by colonoscopic screening,” Gastrointestinal Endoscopy, vol. 61, no. 4, pp. 547–553, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. J. A. DiSario, P. G. Foutch, H. D. Mai, K. Pardy, and R. K. Manne, “Prevalence and malignant potential of colorectal polyps in asymptomatic, average-risk men,” The American Journal of Gastroenterology, vol. 86, no. 8, pp. 941–945, 1991. View at Google Scholar · View at Scopus
  33. T. F. Imperiale, D. R. Wagner, C. Y. Lin, G. N. Larkin, J. D. Rogge, and D. F. Ransohoff, “Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings,” The New England Journal of Medicine, vol. 343, no. 3, pp. 169–174, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. D. A. Johnson, M. S. Gurney, R. J. Volpe et al., “A prospective study of the prevalence of colonic neoplasms in asymptomatic patients with an age-related risk,” The American Journal of Gastroenterology, vol. 85, no. 8, pp. 969–974, 1990. View at Google Scholar · View at Scopus
  35. C. J. Kahi, T. F. Imperiale, B. E. Juliar, and D. K. Rex, “Effect of screening colonoscopy on colorectal cancer incidence and mortality,” Clinical Gastroenterology and Hepatology, vol. 7, no. 7, pp. 770–775, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. D. H. Kim, S. Y. Lee, K. S. Choi et al., “The usefulness of colonoscopy as a screening test for detecting colorectal polyps,” Hepatogastroenterology, vol. 54, no. 80, pp. 2240–2242, 2007. View at Google Scholar
  37. D. H. Kim, P. J. Pickhardt, A. J. Taylor et al., “CT colonography versus colonoscopy for the detection of advanced neoplasia,” The New England Journal of Medicine, vol. 357, no. 14, pp. 1403–1412, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. D. A. Lieberman, D. G. Weiss, J. H. Bond, D. J. Ahnen, H. Garewal, and G. Chejfec, “Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380,” The New England Journal of Medicine, vol. 343, no. 3, pp. 162–168, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. C. N. Manser, L. M. Bachmann, J. Brunner, F. Hunold, P. Bauerfeind, and U. A. Marbet, “Colonoscopy screening markedly reduces the occurrence of colon carcinomas and carcinoma-related death: a closed cohort study,” Gastrointestinal Endoscopy, vol. 76, no. 1, pp. 110–117, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Regula, M. Rupinski, E. Kraszewska et al., “Colonoscopy in colorectal-cancer screening for detection of advanced neoplasia,” The New England Journal of Medicine, vol. 355, no. 18, pp. 1863–1872, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. J. D. Rogge, M. F. Elmore, S. J. Mahoney et al., “Low-cost, office-based, screening colonoscopy,” The American Journal of Gastroenterology, vol. 89, no. 10, pp. 1775–1780, 1994. View at Google Scholar · View at Scopus
  42. P. Schoenfeld, B. Cash, A. Flood et al., “Colonoscopic screening of average-risk women for colorectal neoplasia,” The New England Journal of Medicine, vol. 352, no. 20, pp. 2061–2068, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. M.-S. Soon, R. A. Kozarek, K. Ayub, A. Soon, T.-Y. Lin, and O. S. Lin, “Screening colonoscopy in Chinese and Western patients: a comparative study,” The American Journal of Gastroenterology, vol. 100, no. 12, pp. 2749–2755, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. J. W. Choe, H.-S. Chang, S.-K. Yang et al., “Screening colonoscopy in asymptomatic average-risk Koreans: analysis in relation to age and sex,” Journal of Gastroenterology and Hepatology, vol. 22, no. 7, pp. 1003–1008, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. S. J. Chung, Y. S. Kim, S. Y. Yang et al., “Prevalence and risk of colorectal adenoma in asymptomatic Koreans aged 40–49 years undergoing screening colonoscopy,” Journal of Gastroenterology and Hepatology, vol. 25, no. 3, pp. 519–525, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Nishihara, K. Wu, P. Lochhead et al., “Long-term colorectal-cancer incidence and mortality after lower endoscopy,” The New England Journal of Medicine, vol. 369, no. 12, pp. 1095–1105, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. D. N. Prajapati, K. Saeian, D. G. Binion et al., “Volume and yield of screening colonoscopy at a tertiary medical center after change in medicare reimbursement,” The American Journal of Gastroenterology, vol. 98, no. 1, pp. 194–199, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Strul, R. Kariv, M. Leshno et al., “The prevalence rate and anatomic location of colorectal adenoma and cancer detected by colonoscopy in average-risk individuals aged 40-80 years,” American Journal of Gastroenterology, vol. 101, no. 2, pp. 255–262, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. H. Brenner, J. Chang-Claude, L. Jansen, P. Knebel, C. Stock, and M. Hoffmeister, “Reduced risk of colorectal cancer up to 10 years after screening, surveillance, or diagnostic colonoscopy,” Gastroenterology, vol. 146, no. 3, pp. 709–717, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Cotterchio, M. Manno, N. Klar, J. McLaughlin, and S. Gallinger, “Colorectal screening is associated with reduced colorectal cancer risk: a case-control study within the population-based Ontario Familial Colorectal Cancer Registry,” Cancer Causes and Control, vol. 16, no. 7, pp. 865–875, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. C. A. Doubeni, S. Weinmann, K. Adams et al., “Screening colonoscopy and risk for incident late-stage colorectal cancer diagnosis in average-risk adults: a nested case-control study,” Annals of Internal Medicine, vol. 5, part 1, pp. 312–320, 2013. View at Publisher · View at Google Scholar
  52. T. R. Church, M. Wandell, C. Lofton-Day et al., “Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer,” Gut, vol. 63, no. 2, pp. 317–325, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. U. Haug, S. Hundt, and H. Brenner, “Sensitivity and specificity of faecal tumour M2 pyruvate kinase for detection of colorectal adenomas in a large screening study,” British Journal of Cancer, vol. 99, no. 1, pp. 133–135, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Tonus, G. Neupert, and M. Sellinger, “Colorectal cancer screening by non-invasive metabolic biomarker fecal tumor M2-PK,” World Journal of Gastroenterology, vol. 12, no. 43, pp. 7007–7011, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. D. A. Ahlquist, D. J. Sargent, C. L. Loprinzi et al., “Stool DNA and occult blood testing for screen detection of colorectal neoplasia,” Annals of Internal Medicine, vol. 149, no. 7, pp. 441–450, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. T. F. Imperiale, D. F. Ransohoff, S. H. Itzkowitz et al., “Multitarget stool DNA testing for colorectal-cancer screening,” The New England Journal of Medicine, vol. 370, no. 14, pp. 1287–1297, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. T. F. Imperiale, D. F. Ransohoff, S. H. Itzkowitz, B. A. Turnbull, and M. E. Ross, “Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population,” The New England Journal of Medicine, vol. 351, no. 26, pp. 2704–2714, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. Koga, N. Yamazaki, S. Takizawa et al., “Gene expression analysis using a highly sensitive DNA microarray for colorectal cancer screening,” Anticancer Research, vol. 34, no. 1, pp. 169–176, 2014. View at Google Scholar · View at Scopus
  59. C. Hassan, P. Giorgi Rossi, L. Camilloni et al., “Meta-analysis: adherence to colorectal cancer screening and the detection rate for advanced neoplasia, according to the type of screening test,” Alimentary Pharmacology and Therapeutics, vol. 36, no. 10, pp. 929–940, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Chubak, A. Bogart, S. Fuller, S. S. Laing, and B. B. Green, “Uptake and positive predictive value of fecal occult blood tests: a randomized controlled trial,” Preventive Medicine, vol. 57, no. 5, pp. 671–678, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Federici, P. G. Rossi, P. Borgia, F. Bartolozzi, S. Farchi, and G. Gausticchi, “The immunochemical faecal occult blood test leads to higher compliance than the guaiac for colorectal cancer screening programmes: a cluster randomized controlled trial,” Journal of Medical Screening, vol. 12, no. 2, pp. 83–88, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. R. M. Hoffman, S. Steel, E. F. T. Yee, L. Massie, R. M. Schrader, and G. H. Murata, “Colorectal cancer screening adherence is higher with fecal immunochemical tests than guaiac-based fecal occult blood tests: a randomized, controlled trial,” Preventive Medicine, vol. 50, no. 5-6, pp. 297–299, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. L. Hol, M. E. Van Leerdam, M. Van Ballegooijen et al., “Screening for colorectal cancer: randomised trial comparing guaiac-based and immunochemical faecal occult blood testing and flexible sigmoidoscopy,” Gut, vol. 59, no. 1, pp. 62–68, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. Z. Levi, S. Birkenfeld, A. Vilkin et al., “A higher detection rate for colorectal cancer and advanced adenomatous polyp for screening with immunochemical fecal occult blood test than guaiac fecal occult blood test, despite lower compliance rate. A prospective, controlled, feasibility study,” International Journal of Cancer, vol. 128, no. 10, pp. 2415–2424, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. L. G. van Rossum, A. F. van Rijn, R. J. Laheij et al., “Random comparison of guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population,” Gastroenterology, vol. 135, no. 1, pp. 82–90, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. E. M. Stoop, M. C. de Haan, T. R. de Wijkerslooth et al., “Participation and yield of colonoscopy versus non-cathartic CT colonography in population-based screening for colorectal cancer: a randomised controlled trial,” The Lancet Oncology, vol. 13, no. 1, pp. 55–64, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Groth, H. Krause, R. Behrendt et al., “Capsule colonoscopy increases uptake of colorectal cancer screening,” BMC Gastroenterology, vol. 12, article 80, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. C. Littlejohn, S. Hilton, G. J. MacFarlane, and P. Phull, “Systematic review and meta-analysis of the evidence for flexible sigmoidoscopy as a screening method for the prevention of colorectal cancer,” British Journal of Surgery, vol. 99, no. 11, pp. 1488–1500, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. D. P. Berry, P. Clarke, J. D. Hardcastle, and K. D. Vellacott, “Randomized trial of the addition of flexible sigmoidoscopy to faecal occult blood testing for colorectal neoplasia population screening,” British Journal of Surgery, vol. 84, no. 9, pp. 1274–1276, 1997. View at Publisher · View at Google Scholar · View at Scopus
  70. H. Brevinge, E. Lindholm, S. Buntzen, and J. Kewenter, “Screening for colorectal neoplasia with faecal occult blood testing compared with flexible sigmoidoscopy directly in a 55-56 years' old population,” International Journal of Colorectal Disease, vol. 12, no. 5, pp. 291–295, 1997. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Federici, C. Marinacci, M. Mangia, P. Borgia, P. Giorgi Rossi, and G. Guasticchi, “Is the type of test used for mass colorectal cancer screening a determinant of compliance?. A cluster-randomized controlled trial comparing fecal occult blood testing with flexible sigmoidoscopy,” Cancer Detection and Prevention, vol. 30, no. 4, pp. 347–353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. G. Gondal, T. Grotmol, B. Hofstad, M. Bretthauer, T. J. Eide, and G. Hoff, “The Norwegian Colorectal Cancer Prevention (NORCCAP) screening study: baseline findings and implementations for clinical work-up in age groups 50–64 years,” Scandinavian Journal of Gastroenterology, vol. 38, no. 6, pp. 635–642, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Lisi, C. Hassan, M. Crespi, and A. S. Group, “Participation in colorectal cancer screening with FOBT and colonoscopy: an Italian, multicentre, randomized population study. [Erratum appears in Dig Liver Dis. 2012 Feb;44(2):182 Note: Hassan, C Cesare [corrected to Hassan, Cesare]],” Digestive and Liver Disease, vol. 42, no. 5, pp. 371–376, 2012. View at Google Scholar
  74. Multicentre Australian Colorectal-neoplasia Screening (MACS) Group, “A comparison of colorectal neoplasia screening tests: a multicentre community-based study of the impact of consumer choice,” Medical Journal of Australia, vol. 184, no. 11, pp. 546–550, 2006. View at Google Scholar
  75. E. Quintero, A. Castells, L. Bujanda et al., “Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening,” The New England Journal of Medicine, vol. 366, no. 8, pp. 697–706, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Rasmussen, O. Kronborg, C. Fenger, and O. D. Jørgensen, “Possible advantages and drawbacks of adding flexible sigmoidoscopy to hemoccult-II in screening for colorectal cancer. A randomized study,” Scandinavian Journal of Gastroenterology, vol. 34, no. 1, pp. 73–78, 1999. View at Publisher · View at Google Scholar · View at Scopus
  77. N. Segnan, C. Senore, B. Andreoni et al., “Randomized trial of different screening strategies for colorectal cancer: patient response and detection rates,” Journal of the National Cancer Institute, vol. 97, no. 5, pp. 347–357, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Segnan, C. Senore, B. Andreoni et al., “Comparing attendance and detection rate of colonoscopy with sigmoidoscopy and FIT for colorectal cancer screening,” Gastroenterology, vol. 132, no. 7, pp. 2304–2312, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. J. E. C. W. Verne, R. Aubrey, S. B. Love, I. C. Talbot, and J. M. A. Northover, “Population based randomised study of uptake and yield of screening by flexible sigmoidoscopy compared with screening by faecal occult blood testing,” British Medical Journal, vol. 317, no. 7152, pp. 182–185, 1998. View at Publisher · View at Google Scholar · View at Scopus
  80. A. G. Zauber, S. J. Winawer, G. M. Mills et al., “Adherence to screening in a randomized controlled trial of a one-time screening colonoscopy versus program of annual fecal occult blood test (gFOBt): implications of lower gFOBt adherence to screening on colorectal cancer mortality reduction,” Gastroenterology, vol. 142, no. 5, pp. S82–S83, 2012. View at Publisher · View at Google Scholar
  81. A. H. C. van Roon, S. L. Goede, M. van Ballegooijen et al., “Random comparison of repeated faecal immunochemical testing at different intervals for population-based colorectal cancer screening,” Gut, vol. 62, no. 3, pp. 409–415, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. B. J. Shea, J. M. Grimshaw, G. A. Wells et al., “Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews,” BMC Medical Research Methodology, vol. 7, article 10, 7 pages, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. G. A. Wells, B. Shea, D. O'Connell et al., The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses, Ottawa Hospital Research Institute, Ottawa, Canada, 2012, http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm.
  84. P. Whiting, A. W. S. Rutjes, J. B. Reitsma, P. M. M. Bossuyt, and J. Kleijnen, “The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews,” BMC Medical Research Methodology, vol. 3, article 25, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Brożek, A. Nowak, P. Kunstman, and H. J. Schünemann, GRADEpro Guideline Development Tool (G2DT), (Computer Program) Version 2.xx, 2014, http://www.guidelinedevelopment.org.
  86. Review Manager (Rev Man). 4.2 for Windows, The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark, 2003.
  87. B. J. Elmunzer, R. A. Hayward, P. S. Schoenfeld, S. D. Saini, A. Deshpande, and A. K. Waljee, “Effect of flexible sigmoidoscopy-based screening on incidence and mortality of colorectal cancer: a systematic review and meta-analysis of randomized controlled trials,” PLoS Medicine, vol. 9, no. 12, Article ID e1001352, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. P. Hewitson, P. Glasziou, L. Irwig, B. Towler, and E. Watson, “Screening for colorectal cancer using the faecal occult blood test, Hemoccult,” Cochrane Database of Systematic Reviews, no. 1, Article ID CD001216, 2011. View at Google Scholar
  89. N. J. Massat, S. M. Moss, S. P. Halloran, and S. W. Duffy, “Screening and primary prevention of colorectal cancer: a review of sex-specific and site-specific differences,” Journal of Medical Screening, vol. 20, no. 3, pp. 125–148, 2013. View at Publisher · View at Google Scholar · View at Scopus
  90. Canadian Task Force on Preventive Health Care, “Recommendations on screening for breast cancer in average-risk women aged 40–74 years,” Canadian Medical Association Journal, vol. 183, no. 17, pp. 1991–2001, 2011. View at Publisher · View at Google Scholar
  91. R. Sankaranarayanan, B. M. Nene, S. S. Shastri et al., “HPV screening for cervical cancer in rural India,” The New England Journal of Medicine, vol. 360, no. 14, pp. 1385–1394, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. T. André, C. Boni, M. Navarro et al., “Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial,” Journal of Clinical Oncology, vol. 27, no. 19, pp. 3109–3116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. B. Levin, D. A. Lieberman, B. McFarland et al., “Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American cancer society, the US multi-society task force on colorectal cancer, and the American college of radiology,” Gastroenterology, vol. 134, no. 5, pp. 1570–1595, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. Scottish Intercollegiate Guidelines Network (SIGN), Diagnosis and Management of Colorectal Cancer. A National Clinical Guideline, SIGN Publication no. 126, Scottish Intercollegiate Guidelines Network (SIGN), Edinburgh, UK, 2011.
  95. European Commission, European Guidelines for Quality Assurance in Colorectal Cancer Screening and Diagnosis, Edited by N. Segnan, J. Patnick, L. von Karsa, Publications Office of the European Union, Rue Mercier, Luxembourg, 1st edition, 2010.
  96. U.S. Preventive Services Task Force, “Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement,” Annals of Internal Medicine, vol. 149, no. 9, pp. 627–637, 2008. View at Publisher · View at Google Scholar
  97. D. Leddin, “The Canadian Association of Gastroenterology position on colon cancer screening,” Canadian Journal of Gastroenterology, vol. 17, no. 2, p. 133, 2003. View at Publisher · View at Google Scholar
  98. D. K. Rex, D. A. Johnson, J. C. Anderson et al., “American College of Gastroenterology guidelines for colorectal cancer screening,” The American Journal of Gastroenterology, vol. 104, no. 3, pp. 739–750, 2009. View at Google Scholar
  99. Canadian Task Force on Preventive Health C, “Recommendations on screening for colorectal cancer in primary care,” Canadian Medical Association Journal, vol. 188, no. 5, pp. 340–348, 2016. View at Publisher · View at Google Scholar
  100. US Preventive Services Task Force, “Screening for colorectal cancer: us preventive services task force recommendation statement,” The Journal of the American Medical Association, vol. 315, no. 23, pp. 2564–2575, 2016. View at Publisher · View at Google Scholar
  101. C. Dubé, “Tackling colorectal cancer as a public health issue: what can the gastroenterologist do?” Canadian Journal of Gastroenterology, vol. 26, no. 7, pp. 417–418, 2012. View at Publisher · View at Google Scholar · View at Scopus