Stool Investigations for Colorectal Cancer Screening: From Occult Blood Test to DNA Analysis

Journal of Gastrointestinal Cancer

Volumn 47, Issue 2, 2016, Pages 143-151

  Iannone, Andrea ^a   Losurdo, Giuseppe ^a   Pricci, Maria ^a   Girardi, Bruna ^a   Massaro, Antonio ^a   Principi, Mariabeatrice ^a   Barone, Michele ^a   Ierardi, Enzo ^a   Di Leo, Alfredo ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Adenoma; Colorectal cancer; Fecal DNA; Fecal immunochemical test; Fecal occult blood test; Screening

Indexed keywords

BIOLOGICAL MARKER; CELL DNA; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR BETA; MICRORNA; MICRORNA 106A; MICRORNA 134; MICRORNA 135; MICRORNA 135B; MICRORNA 17; MICRORNA 17 92; MICRORNA 183; MICRORNA 196A; MICRORNA 199A; MICRORNA 199A 3P; MICRORNA 20A; MICRORNA 21; MICRORNA 214; MICRORNA 29B; MICRORNA 7; MICRORNA 9; MICRORNA 92A; MICRORNA 96; UNCLASSIFIED DRUG; UNTRANSLATED RNA; DNA;

BETA ACTIN GENE; CANCER SCREENING; COLORECTAL CANCER; COST EFFECTIVENESS ANALYSIS; DNA DETERMINATION; DNA METHYLATION; DOWN REGULATION; FECAL IMMUNOCHEMICAL TEST; FECAL OCCULT BLOOD TEST; FECES ANALYSIS; GENE EXPRESSION; GENE MUTATION; HEALTH ECONOMICS; HUMAN; META ANALYSIS; OCCULT BLOOD TEST; ONCOGENE; ONCOGENE K RAS; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SENSITIVITY AND SPECIFICITY; SYSTEMATIC REVIEW; UPREGULATION; COLORECTAL NEOPLASMS; CYTOLOGY; EARLY CANCER DIAGNOSIS; FECES; MASS SCREENING; OCCULT BLOOD; PROCEDURES;

COLORECTAL NEOPLASMS; DNA; EARLY DETECTION OF CANCER; FECES; HUMANS; MASS SCREENING; OCCULT BLOOD;

EID: 84991931178     PISSN: 19416628     EISSN: 19416636     Source Type: Journal    
DOI: 10.1007/s12029-016-9810-z     Document Type: Review

References (76)

1. Ferlay J, Shin HR, Bray F, et al. GLOBOCAN 2008 v2.0, cancer incidence and mortality worldwide: IARC cancer base no. 10 [internet]. Lyon, France: International Agency for Research on Cancer; 2010.
2. Lofano K, Principi M, Scavo MP, Pricci M, Ierardi E, Di Leo A. Dietary lifestyle and colorectal cancer onset, recurrence, and survival: myth or reality? J Gastrointest Cancer. 2013;44(1):1–11.
3. Barone M, Lofano K, De Tullio N, Licinio R, Albano F, Di Leo A. Dietary, endocrine, and metabolic factors in the development of colorectal cancer. J Gastrointest Cancer. 2012;43(1):13–9.
4. Loughrey MB, Shepherd NA. The pathology of bowel cancer screening. Histopathology. 2015;66(1):66–77.
5. Kaemmerer E, Klaus C, Jeon MK, Gassler N. Molecular classification of colorectal carcinomas: the genotype-to-phenotype relation. World J Gastroenterol. 2013;19(45):8163–7.
6. Garborg K, Holme Ø, Løberg M, Kalager M, Adami HO, Bretthauer M. Current status of screening for colorectal cancer. Ann Oncol. 2013;24(8):1963–72.
7. Young GP. Population-based screening for colorectal cancer: Australian research and implementation. J Gastroenterol Hepatol. 2009;24 Suppl 3:S33–42.
8. Sinatra MA, St John DJ, Young GP. Interference of plant peroxidases with guaiac-based fecal occult blood tests is avoidable. Clin Chem. 1999;45:123–6.
9. Ciatto S, Martinelli F, Castiglione G, et al. Association of FOBT-assessed faecal Hb content with colonic lesions detected in the Florence screening programme. Br J Cancer. 2007;96(2):218–21.
10. Parente F, Bargiggia S, Boemo C, et al. Anatomic distribution of cancers and colorectal adenomas according to age and sex and relationship between proximal and distal neoplasms in an i-FOBT-positive average-risk Italian screening cohort. Int J Colorectal Dis. 2014;29(1):57–64.
11. Levin B, Lieberman DA, McFarland B, 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. 2008;134(5):1570–95.
12. Hardcastle JD, Chamberlain JO, Robinson MH, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet. 1996;348:1472–7.
13. Kronborg O, Fenger C, Olsen J, et al. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet. 1996;348:1467–71.
14. Lindholm E, Brevinge H, Haglind E. Survival benefit in a randomized clinical trial of faecal occult blood screening for colorectal cancer. Br J Surg. 2008;95:1029–36.
15. Mandel JS, Church TR, Ederer F, et al. Colorectal cancer mortality: effectiveness of biennial screening for fecal occult blood. J Natl Cancer Inst. 1999;91:434–7.
16. Scholefield JH, Moss SM, Mangham CM, et al. Nottingham trial of faecal occult blood testing for colorectal cancer: a 20-year follow-up. Gut. 2012;61:1036–40.
17. Mandel JS, Church TR, Bond JH, et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med. 2000;343:1603–7.
18. Kronborg O, Jorgensen OD, Fenger C, et al. Randomized study of biennial screening with a faecal occult blood test: results after nine screening rounds. Scand J Gastroenterol. 2004;39:846–51.
19. Hewitson P, Glasziou P, Irwig L, et al. Screening for colorectal cancer using the faecal occult blood test, Hemoccult. Cochrane Database Syst Rev. 2007;1, CD001216.
20. Segnan N, Patnick J, Karsa L. European guidelines for quality assurance in colorectal cancer screening and diagnosis. Luxembourg: Office for Official Publications of the European Communities; 2010.
21. Hundt S, Haug U, Brenner H. Comparative evaluation of immunochemical fecal occult blood tests for colorectal adenoma detection. Ann Intern Med. 2009;150:162–9.
22. Guittet L, Bouvier V, Mariotte N, et al. Comparison of a guaiac and an immunochemical faecal occult blood test for the detection of colonic lesions according to lesion type and location. Br J Cancer. 2009;100:1230–5.
23. Grazzini G, Visioli CB, Zorzi M, et al. Immunochemical faecal occult blood test: number of samples and positivity cutoff. What is the best strategy for colo-rectal cancer screening? Br J Cancer. 2009;100:259–65.
24. Levi Z, Rozen P, Hazazi R, et al. A quantitative immunochemical fecal occult blood test for colorectal neoplasia. Ann Intern Med. 2007;146:244–55.
25. Whitlock EP, Lin JS, Liles E, et al. Screening for colorectal cancer: a targeted, updated systematic review for the U.S. Preventive Services Task Force. Ann Intern Med. 2008;149:638–58.
26. Hol L, van Leerdam ME, van Ballegooijen M, et al. Screening for colorectal cancer: randomised trial comparing guaiac-based and immunochemical faecal occult blood testing and flexible sigmoidoscopy. Gut. 2010;59:62–8.
27. Levi Z, Birkenfeld S, Vilkin A, 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. Int J Cancer. 2011;128:2415–24.
28. Levi Z, Hazazi R, Rozen P, et al. A quantitative immunochemical faecal occult blood test is more efficient for detecting significant colorectal neoplasia than a sensitive guaiac test. Aliment Pharmacol Ther. 2006;23:1359–64.
29. Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell. 2012;150:12–27.
30. Sidransky D, Tokino T, Hamilton SR, et al. Identification of ras oncogene mutations in the stool of patients with curable colorectal tumors. Science. 1992;256:102–5.
31. Robertson DJ, Imperiale TF. Stool testing for colorectal cancer. Gastroenterology. 2015. doi:10.1053/j.gastro.2015.05.045 [article in press].
32. Villa E, Dugani A, Rebecchi AM, et al. Identification of subjects at risk for colorectal carcinoma through a test based on K-ras determination in the stool. Gastroenterology. 1996;110:1346–53.
33. Ratto C, Flamini G, Sofo L, et al. Detection of oncogene mutation from neoplastic colonic cells exfoliated in feces. Dis Colon Rectum. 1996;39(11):1238–44.
34. Traverso G, Shuber A, Levin B, et al. Detection of APC mutations in fecal DNA from patients with colorectal tumors. N Engl J Med. 2002;346(5):311–20.
35. Notarnicola M, Cavallini A, Cardone R, Pezzolla F, Demma I, Di Leo A. K-ras and p53 mutations in DNA extracted from colonic epithelial cells exfoliated in faeces of patients with colorectal cancer. Dig Liver Dis. 2000;32(2):131–6.
36. Coppedè F, Lopomo A, Spisni R, Migliore L. Genetic and epigenetic biomarkers for diagnosis, prognosis and treatment of colorectal cancer. World J Gastroenterol. 2014;20(4):943–56.
37. Luo YX, Chen DK, Song SX, Wang L, Wang JP. Aberrant methylation of genes in stool samples as diagnostic biomarkers for colorectal cancer or adenomas: a meta-analysis. Int J Clin Pract. 2011;65:1313–20.
38. Yang H, Xia BQ, Jiang B, et al. Diagnostic value of stool DNA testing for multiple markers of colorectal cancer and advanced adenoma: a meta-analysis. Can J Gastroenterol. 2013;27(8):467–75.
39. Guo Q, Song Y, Zhang H, Wu X, Xia P, Dang C. Detection of hypermethylated fibrillin-1 in the stool samples of colorectal cancer patients. Med Oncol. 2013;30:695.
40. Toyota M, Suzuki H. Epigenetic drivers of genetic alterations. Adv Genet. 2010;70:309–23.
41. You JS, Jones PA. Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell. 2012;22:9–20.
42. Imperiale TF, Ransohoff DF, Itzkowitz SH, et al. Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population. N Engl J Med. 2004;351:2704–14.
43. Ahlquist DA, Sargent DJ, Loprinzi CL, et al. Stool DNA and occult blood testing for screen detection of colorectal neoplasia. Ann Intern Med. 2008;149:441–50. w81.
44. Ahlquist DA, Zou H, Domanico M, et al. Next-generation stool DNA test accurately detects colorectal cancer and large adenomas. Gastroenterology. 2012;142:248–56.
45. Imperiale TF, Ransohoff DF, Itzkowitz SH, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 2014;370(14):1287–97.
46. Smith RA, Manassaram-Baptiste D, Brooks D, et al. Cancer screening in the United States, 2015: a review of current American cancer society guidelines and current issues in cancer screening. CA Cancer J Clin. 2015;65(1):30–54.
47. Bartel DP, Lee R, Feinbaum. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–97.
48. Ren A, Dong Y, Tsoi H, et al. Detection of miRNA as non-invasive biomarkers of colorectal cancer. Int J Mol Sci. 2015;16:2810–23.
49. Wu CW, Ng SC, Dong Y, et al. Identification of microRNA-135b in stool as a potential noninvasive biomarker for colorectal cancer and adenoma. Clin Cancer Res. 2014;20:2994–3002.
50. Wu CW, Ng SSM, Dong YJ, et al. Detection of miR-92a and miR-21 in stool samples as potential screening biomarkers for colorectal cancer and polyps. Gut. 2012;61:739–45.
51. Koga Y, Yasunaga M, Takahashi A, et al. MicroRNA expression profiling of exfoliated colonocytes isolated from feces for colorectal cancer screening. Cancer Prev Res. 2010;3:1435–42.
52. Ahmed FE, Ahmed NC, Vos PW, et al. Diagnostic microRNA markers to screen for sporadic human colon cancer in stool: I. Proof of principle. Cancer Genomics Proteomics. 2013;10:93–113.
53. Hoff G, Grotmol T, Thiis-Evensen E, et al. Testing for faecal calprotectin (PhiCal) in the Norwegian Colorectal Cancer Prevention trial on flexible sigmoidoscopy screening: comparison with an immunochemical test for occult blood (FlexSure OBT). Gut. 2004;53:1329–33.
54. Uppara M, Adaba F, Askari A, Clark S, Hanna G, Athanasiou T, et al. A systematic review and meta-analysis of the diagnostic accuracy of pyruvate kinase M2 isoenzymatic assay in diagnosing colorectal cancer. World J Surg Oncol. 2015;13:48.
55. Huang JX, Zhou Y, Wang CH, Yuan WW, Zhang ZD, Zhang XF. Tumor M2-pyruvate kinase in stool as a biomarker for diagnosis of colorectal cancer: a meta-analysis. J Cancer Res Ther. 2014;10(Suppl):C225–8.
56. Leen R, Seng-Lee C, Holleran G, O’Morain C, McNamara D. Comparison of faecal M2-PK and FIT in a population-based bowel cancer screening cohort. Eur J Gastroenterol Hepatol. 2014;26(5):514–8.
57. Karl J, Wild N, Tacke M, et al. Improved diagnosis of colorectal cancer using a combination of fecal occult blood and novel fecal protein markers. Clin Gastroenterol Hepatol. 2008;6:1122–8.
58. Olson J, Whitney DH, Durkee K, Shuber AP. DNA stabilization is critical for maximizing performance of fecal DNA-based colorectal cancer tests. Diagn Mol Pathol. 2005;14(3):183–91.
59. Zauber AG, Lansdorp-Vogelaar I, Wilschut J, Knudsen AB, van Ballegooijen M, Kuntz KM. Cost-effectiveness of DNA stool testing to screen for colorectal cancer [Internet]. Rockville: Agency for Healthcare Research and Quality (US); 2007.
60. Special report: fecal DNA analysis for colon cancer screening. Technol Eval Cent Asses Program Exec Summ. 2006;21(6):1–2.
61. Pignone M, Saha S, Hoerger T, Mandelblatt J. Cost-effectiveness analyses of colorectal cancer screening: a systematic review for the U.S. preventive services task force. Ann Int Med. 2002;137(2):96–104.
62. Fernandez E, La Vecchia C, Balducci A, Chatenoud L, Franceschi S, Negri E. Oral contraceptives and colorectal cancer risk: a meta-analysis. Br J Cancer. 2001;84:722–7.
63. Chlebowski RT, Wactawski-Wende J, Ritenbaugh C, et al. Women’s health initiative investigators. Estrogen plus progestin and colorectal cancer in postmenopausal women. N Engl J Med. 2004;350:991–1004.
64. Hendifar A, Yang D, Lenz F, Lurje G, Pohl A, Lenz C, et al. Gender disparities in metastatic colorectal cancer survival. Clin Cancer Res. 2009;15:6391–7.
65. Long MD, Martin CF, Galanko JA, Sandler RS. Hormone replacement therapy, oral contraceptive use, and distal large bowel cancer: a population-based case-control study. Am J Gastroenterol. 2010;105:1843–50.
66. Principi M, Scavo MP, Piscitelli D, et al. The sharp decline of beta estrogen receptors expression in long-lasting ulcerative-associated carcinoma. Scand J Gastroenterol. 2015;50(8):1002–10.
67. Principi M, Barone M, Pricci M, De Tullio N, Losurdo G, Ierardi E, et al. Ulcerative colitis: from inflammation to cancer. Do estrogen receptors have a role? World J Gastroenterol. 2014;20(33):11496–504.
68. Di Leo A, Barone M, Maiorano E, et al. ER-beta expression in large bowel adenomas: implications in colon carcinogenesis. Dig Liver Dis. 2008;40:260–6.
69. Weige CC, Allred KF, Allred CD. Estradiol alters cell growth in nonmalignant colonocytes and reduces the formation of preneoplastic lesions in the colon. Cancer Res. 2009;69:9118–24.
70. Bringiotti R, Ierardi E, De Tullio N, et al. Education and imaging. Gastroenterology: video capsule endoscopy disclosure of unprecedented therapeutic effect of Eviendep on small bowel polyposis in Lynch syndrome. J Gastroenterol Hepatol. 2015;30(5):801.
71. Calabrese C, Praticò C, Calafiore A, et al. Eviendep(R) reduces number and size of duodenal polyps in familial adenomatous polyposis patients with ileal pouch-anal anastomosis. World J Gastroenterol. 2013;19:5671–7.
72. Barone M, Tanzi S, Lofano K, et al. Dietary induced ERbeta upregulation counteracts intestinal neoplasia development in intact male ApcMin/+ mice. Carcinogenesis. 2010;31:269–74.
73. Principi M, Di Leo A, Pricci M, Barone M, et al. Phytoestrogens/insoluble fibers and colonic estrogen receptor β: randomized, double-blind, placebo-controlled study. World J Gastroenterol. 2013;19:4325–33.
74. Tu Z, Ma Y, Tian J, Li H, Akers W, Achilefu S, et al. Estrogen receptor β potentiates the antiproliferative effect of raloxifene and affects the cell migration and invasion in HCT-116 colon cancer cells. J Cancer Res Clin Oncol. 2012;138:1091–103.
75. Edvardsson K, Ström A, Jonsson P, Gustafsson JÅ, Williams C. Estrogen receptor beta induces anti-inflammatory and anti-tumorigenic networks in colon cancer cells. Mol Endocrinol. 2011;25:969–79.
76. Berner C, Aumüller E, Gnauck A, Nestelberger M, Just A, Haslberger AG. Epigenetic control of estrogen receptor expression and tumor suppressor genes is modulated by bioactive food compounds. Ann Nutr Metab. 2010;57(3–4):183–9.