Screening for colorectal cancer: Established and emerging modalities

Nature Reviews Gastroenterology and Hepatology

Volumn 8, Issue 12, 2011, Pages 711-722

  Pawa, Nikhil ^a   Arulampalam, Tan ^b   Norton, John D ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b IPSWICH HOSPITAL NHS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CA 19-9 ANTIGEN; CALGRANULIN A; CALGRANULIN B; CARCINOEMBRYONIC ANTIGEN; GELATINASE B; GENOMIC DNA; HEMOGLOBIN; MICRORNA;

AGE DISTRIBUTION; CANCER RISK; CANCER SCREENING; CANCER STAGING; COLONOSCOPY; COLORECTAL CANCER; COMPUTED TOMOGRAPHIC COLONOGRAPHY; COST EFFECTIVENESS ANALYSIS; CYTODIAGNOSIS; DIAGNOSTIC ACCURACY; DNA MICROARRAY; FECES ANALYSIS; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; HEALTH CARE COST; HEMOGLOBIN ANALYSIS; HUMAN; MASS SCREENING; MOLECULAR DIAGNOSIS; OCCULT BLOOD TEST; PRACTICE GUIDELINE; PRECANCER; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REVIEW; RISK ASSESSMENT; SIGMOIDOSCOPY;

COLONOSCOPY; COLORECTAL NEOPLASMS; DNA, NEOPLASM; HUMANS; INCIDENCE; MASS SCREENING; REPRODUCIBILITY OF RESULTS; SURVIVAL RATE; WORLD HEALTH;

EID: 82955195715     PISSN: 17595045     EISSN: 17595053     Source Type: Journal    
DOI: 10.1038/nrgastro.2011.205     Document Type: Review

References (145)

1. Weitz, J. et al. Colorectal cancer. Lancet 365, 153-165 (2005). (Pubitemid 40091806)
2. Cancer Research UK. Bowel cancer statistics-UK. Cancer Research UK [online], http://info.cancerresearchuk.org/cancerstats/types/bowel/ symptomsandtreatment/ (2011).
3. Kim, H. J., Yu, M. H., Kim, H., Byun, J. & Lee, C. Noninvasive molecular biomarkers for the detection of colorectal cancer. BMB Rep. 41, 685-692 (2008).
4. Verdecchia, A. et al. Recent cancer survival in Europe: a 2000-2002 period analysis of EUROCARE-4data. Lancet Oncol. 8, 784-796 (2007). (Pubitemid 47321601)
5. Gupta, A. K., Brenner, D. E. & Turgeon, D. K. Early detection of colon cancer: new tests on the horizon. Mol. Diag. Ther. 12, 77-85 (2008). (Pubitemid 351570863)
6. Burt, R. W. Colorectal cancer screening. Curr. Opin. Gastroenterol. 26, 466-470 (2010).
7. Hofstad, B. in Colonoscopy: Principles and Practice 1st edn (eds Waye, J. D., Rex, D. K., Williams, C. B.) 358-376 (Wiley-Blackwell, Oxford, 2003).
8. Ahlquist, D. A. Molecular detection of colorectal neoplasia. Gastroenterology 138, 2127-2139 (2010).
9. Lieberman, D. Progress and challenges in colorectal cancer screening and surveillance. Gastroenterology 138, 2115-2126 (2010).
10. Regula, J. et al. Colonoscopy in colorectal cancer screening for detection of advanced neoplasia. N. Engl. J. Med. 355, 1863-1872 (2006). (Pubitemid 44664644)
11. Kahi, C. J., Imperiale, T. F., Juliar, B. E. & Rex, D. K. Effect of screening colonoscopy on colorectal cancer incidence and mortality. Clin. Gastroenterol. Hepatol. 7, 770-775 (2009).
12. Rabeneck, L., Paszat, L. F., Saskin, R. & Stukel, T. A. Association between colonoscopy rates and colorectal cancer mortality. Am. J. Gastroenterol. 105, 1627-1632 (2010).
13. Baxter, N. N. et al. Association of colonoscopy and death from colorectal cancer. Ann. Intern. Med. 150, 1-8 (2009).
14. Brenner, H. et al. Protection from right- and left-sided colorectal neoplasms after colonoscopy: population-based study. J. Natl Cancer Inst. 102, 89-95 (2010).
15. The Northern-European Initiative on Colorectal Cancer (NordICC). ClinicalTrials.gov [online], http://clinicaltrials.gov/ct2/show/NCT00883792 (2011).
16. Nelson, S. R. & Thorson, A. G. Colorectal cancer screening. Curr. Oncol. Rep. 11, 482-489 (2009).
17. Ransohoff, A. F. How much does colonoscopy reduce colon cancer mortality? Ann. Intern. Med. 150, 50-52 (2009).
18. Ward, N., Wright, J., Marsh, S. & Norton, J. Fast track referrals for colorectal cancer: impact of the faecal occult blood test screening programme. Colorectal Dis. 9, 258-261 (2007). (Pubitemid 46477030)
19. Glick, S., Wagner, J. L. & Johnson, C. D. Cost-effectiveness of double contrast barium enema in screening for colorectal cancer. AJR Am. J. Roentgenol. 170, 629-636 (1998). (Pubitemid 28106650)
20. Toma, J., Paszat, L. F., Gunraj, N. & Rabeneck, L. Rates of new or missed colorectal cancer after barium enema and their risk factors: a population based study. Am. J. Gastroenterol. 103, 3142-3148 (2008).
21. Sosna, J. et al. CT colonography of colorectal polyps: a metaanalysis. AJR Am. J. Roentgenol. 181, 1593-1598 (2003). (Pubitemid 37466537)
22. Rosman, A. S. & Korsten, M. A. Meta-analysis comparing CT colonography, air contrast barium enema, and colonoscopy. Am. J. Med. 120, 203-210 (2007).
23. Vu, H. T. & Burke, C. A. Advances in colorectal cancer screening. Curr. Gastroenterol. Rep. 11, 406-412 (2009).
24. Knudsen, A. B. et al. Cost-effectiveness of computed tomographic colonography screening for colorectal cancer in the medicare population. J. Natl Cancer Inst. 102, 1238-1252 (2010).
25. Sweet, A. et al. The impact of CT colonography for colorectal cancer screening on the UK NHS: costs, healthcare resources and health outcomes. Appl. Health Econ. Health Policy 9, 51-64 (2011).
26. Hoff, G., Grotmol, T., Skovlund, E. & Bretthauer, M. & Norwegian Colorectal Cancer Prevention Study Group. Risk of colorectal cancer seven years after flexible sigmoidoscopy screening: randomised controlled trial. BMJ 338, b1846 (2009).
27. Atkin, W. S. et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet 375, 1624-1633 (2010).
28. Segnan, N. et al. Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian randomized controlled trial-SCORE. J. Natl Cancer Inst. 103, 1310-1322 (2011).
29. Tappenden, P. et al. Option appraisal of population-based colorectal cancer screening programmes in England. Gut 56, 677-684 (2007). (Pubitemid 46662935)
30. Towler, B. et al. A systematic review of the effects of screening for colorectal cancer using the faecal occult blood test, hemoccult. BMJ 317, 559-565 (1998). (Pubitemid 28395924)
31. Zavoral, M. et al. Colorectal cancer screening in Europe. World J. Gastroenterol. 15, 5907-5915 (2009).
32. West, N. J., Boustiere, C., Fischbach, W., Parente, F. & Leicester, R. Colorectal cancer screening in Europe: differences in approach; similar barriers to overcome. Int. J. Colorectal Dis. 24, 731-740 (2009).
33. Vilkin, A. et al. Performance characteristics and evaluation of an automated-developed and quantitative, immunochemical, fecal occult blood screening test. Am. J. Gastroenterol. 100, 2519-2525 (2005).
34. Grazzini, G. et al. Influence of seasonal variations in ambient temperature on performance of immunochemical faecal occult blood test for colorectal cancer: observational study from the Florence district. Gut 59, 1511-1515 (2010).
35. Guittet, L. et al. Comparison of a guaiac based and an immunochemical faecal occult blood test in screening for colorectal cancer in a general average risk population. Gut 56, 210-214 (2007).
36. Van Rossum, L. G. et al. Random comparison of guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population. Gastroenterology 135, 82-90 (2008).
37. Parra-Blanco, A. et al. Diagnostic accuracy of immunochemical versus guaiac faecal occult blood tests for colorectal cancer. J. Gastroenterol. 45, 703-712 (2010).
38. Li, S. et al. New immunochemical fecal occult blood test with two-consecutive stool sample testing is a cost-effective approach for colon cancer screening: results of a prospective multicenter study in Chinese patients. Int. J. Cancer 118, 3078-3083 (2006).
39. Parekh, M., Fendrick, A. M. & Ladabaum, U. As tests evolve and costs of cancer care rise: reappraising stool-based screening for colorectal neoplasia. Aliment. Pharmacol. Ther. 27, 697-712 (2008). (Pubitemid 351406306)
40. Zheng, S. et al. Cluster randomization trial of sequence mass screening for colorectal cancer. Dis. Colon Rectum 46, 51-58 (2003). (Pubitemid 36105831)
41. Potack, J. & Itzkowitz, S. H. Practical advances in stool screening for colorectal cancer. J. Natl Comp. Canc. Netw. 8, 81-92 (2010).
42. Imperiale, T. F. et al. Fecal DNA versus fecal occult blood for colorectal cancer screening in an average risk population. N. Engl. J. Med. 351, 2704-2714 (2004). (Pubitemid 39665324)
43. Ahlquist, D. A. et al. Stool DNA and occult blood testing for screen detection of colorectal neoplasia. Ann. Intern. Med. 149, 441-450 (2008).
44. Goel, A. DNA methylation-based fecal biomarkers for non-invasive screening of GI cancers. Future Oncol. 6, 333-336 (2010).
45. Song, K., Fendrick, A. M. & Ladabaum, U. Fecal DNA testing compared with conventional colorectal cancer screening methods: a decision analysis. Gastroenterology 126, 1270-1279 (2004). (Pubitemid 38552791)
46. Itzkowitz, S. et al. A simplified, noninvasive stool DNA test for colorectal cancer detection. Am. J. Gastroenterol. 103, 2862-2870 (2008).
47. Paterlini-Brechot, P. & Benali, N. L. Circulating tumor cells (CTC): detection, clinical impact and future directions. Cancer Lett. 253, 180-204 (2007). (Pubitemid 47017533)
48. Sleijfer, S. et al. Circulating tumour cell detection on its way to routine diagnostic implementation. Eur. J. Cancer 43, 2645-2650 (2007). (Pubitemid 350151847)
49. Pantel, K., Brakenhoff, R. H. & Brandt, B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat. Rev. Cancer 8, 329-340 (2008). (Pubitemid 351596394)
50. Sastre, J. et al. Circulating tumor cells in colorectal cancer: correlation with clinical and pathological variables. Ann. Oncol. 19, 935-938 (2008). (Pubitemid 351627310)
51. Wong, S. C. et al. Clinical significance of cytokeratin 20-positive circulating tumor cells detected by a refined immunomagnetic enrichment assay in colorectal cancer patients. Clin. Cancer Res. 15, 1005-1012 (2009).
52. Negin, B. P. & Cohen, S. J. Circulating tumor cells in colorectal cancer: past, present and future challenges. Curr. Treat. Options Oncol. 11, 1-13 (2010).
53. Allen, J. E. & El-Deiry, W. S. Circulating tumor cells and colorectal cancer. Curr. Colorectal Cancer Rep. 6, 212-220 (2010).
54. Cohen, S. J. et al. Relationship of circulating tumor cells to tumor response, progression-free survival and overall survival in patients with metastatic colorectal cancer. J. Clin. Oncol. 26, 3213-3221 (2008).
55. Tol, J. et al. Circulating tumour cells early predict progression-free and overall survival in advanced colorectal cancer patients treated with chemotherapy and targeted agents. Ann. Oncol. 21, 1006-1012 (2010).
56. Antolovic, D. et al. Heterogenous detection of circulating tumor cells in patients with colorectal cancer by immunomagnetic enrichment using different EpCAM-specific antibodies. BMC Biotechnol. 10, 35 (2010).
57. Krivacic, R. T. et al. A rare-cell detector for cancer. Proc. Natl Acad. Sci. USA 101, 10501-10504 (2004). (Pubitemid 38955770)
58. Kraeft, S. K. et al. Reliable and sensitive identification of occult tumor cells using the improved rare event imaging system. Clin. Cancer Res. 10, 3020-3028 (2004).
59. Marrinucci, D. et al. Cytomorphology of circulating colorectal tumor cells: a small case series. J. Oncol. 861341 (2010).
60. Nagrath, S. et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450, 1235-1239 (2007).
61. Stott, S. L. et al. Isolation and characterization of circulating tumor cells from patients with localized and metastatic prostate cancer. Sci. Transl. Med. 2, 25ra23 (2010).
62. Huerta, S. Recent advances in the molecular diagnosis and prognosis of colorectal cancer. Expert Rev. Mol. Diagn. 8, 277-288 (2008). (Pubitemid 351724707)
63. Wanebo, H. J. et al. Preoperative carcinoembryonic antigen level as a prognostic indicator in colorectal cancer. N. Engl. J. Med. 299, 448-451 (1978). (Pubitemid 9011330)
64. Posner, M. R. & Mayer, R. J. The use of serologic tumor markers in gastrointestinal malignancies. Hematol. Oncol. Clin. North Am. 8, 533-553 (1994). (Pubitemid 24188443)
65. Fletcher, R. H. Carcinoembryonic antigen. Ann. Intern. Med. 104, 66-73 (1986). (Pubitemid 16182780)
66. Hundt, S., Haug, U. & Brenner, H. Blood markers for early detection of colorectal cancer: a systematic review. Cancer Epidemiol. Biomarkers Prev. 16, 1935-1953 (2007). (Pubitemid 47621167)
67. Tjalsma, H. Identification of biomarkers for colorectal cancer through proteomics-based approaches. Expert Rev. Proteomics 7, 879-895 (2010).
68. Leman, E. S. et al. Initial analysis of colon cancer-specific antigen CCSA 3 and CCSA 4 as colorectal cancer-associated serum markers. Cancer Res. 67, 5600-5605 (2007). (Pubitemid 46984988)
69. Walgenbach-Brunagel, G. et al. The use of a colon cancer associated nuclear antigen CCSA 2 for the blood-based detection of colon cancer. J. Cell. Biochem. 104, 286-294 (2008).
70. Hurst, N. G. et al. Elevated serum matrix metalloproteinase 9 (MMP 9) concentration predicts the presence of colorectal cancer in symptomatic patients. Br. J. Cancer 97, 971-977 (2007). (Pubitemid 47519304)
71. Kim, H. J. et al. Identification of S100A8 and S100A9 as serological markers for colorectal cancer. J. Proteome Res. 8, 1368-1379 (2009).
72. Kobold, S., Luetkens, T., Cao, Y., Bokemeyer, C. & Atanackovic, D. Prognostic and diagnostic value of spontaneous tumor-related antibodies. Clin. Dev. Immunol. 721531 (2010).
73. Casal, J. I. & Barderas, R. Identification of cancer autoantigens in serum: toward diagnostic/prognostic testing? Mol. Diagn. Ther. 14, 149-154 (2010).
74. Leidinger, P. et al. Identification of lung cancer with high sensitivity and specificity by blood testing. Respir. Res. 11, 18 (2010).
75. Gnjatic, S. et al. Seromic profiling of ovarian and pancreatic cancer. Proc. Natl Acad. Sci. USA 107, 5088-5093 (2010).
76. Babel, I. et al. Identification of tumor-associated autoantigens for the diagnosis of colorectal cancer in serum using high density protein microarrays. Mol. Cell. Proteomics 8, 2382-2395 (2009).
77. Babel, I. et al. Identification of MST1/STK4 and SULF1 proteins as autoantibody targets for the diagnosis of colorectal cancer by using phage microarrays. Mol. Cell. Proteomics 10, M110.001784 (2011).
78. De Bock, M. et al. Challenges for biomarker discovery in body fluids using SELDI-TOF MS. J. Biomed. Biotechnol. 2010, 9606082 (2010).
79. Adam, B. L. et al. Serum protein fingerprinting coupled with a pattern-matching algorithm distinguishes prostate cancer from benign prostate hyperplasia and healthy men. Cancer Res. 62, 3609-3614 (2002).
80. Petricoin, E. F. et al. Use of proteomic patterns in serum to identify ovarian cancer. Lancet 359, 572-575 (2002).
81. Li, J., Zhang, Z., Rosenzweig, J., Wang, Y. Y. & Chan, D. W. Proteomics and bioinformatics approaches for identification of serum biomarkers to detect breast cancer. Clin. Chem. 48, 1296-1304 (2002). (Pubitemid 34809839)
82. Honda, K. et al. Possible detection of pancreatic cancer by plasma protein profiling. Cancer Res. 65, 10613-10622 (2005). (Pubitemid 41743757)
83. McHugh, S. M., O'Donnell, J. & Gillen, P. Genomic and oncoproteomic advances in detection and treatment of colorectal cancer. World J. Surg. Oncol. 7, 36 (2009).
84. Huijbers, A. et al. Proteomic serum biomarkers and their potential application in cancer Screening Programs. Int. J. Mol. Sci. 11, 4175-4193 (2010).
85. Engwegen, J. Y. et al. Identification of serum proteins discriminating colorectal cancer patients and healthy controls using surface-enhanced laser desorption ionisation-time of flight mass spectrometry. World J. Gastroenterol. 12, 1536-1544 (2006).
86. Wang, Q. et al. Limitations in SELDI-TOF MS whole serum proteomic profiling with IMAC surface to specifically detect colorectal cancer. BMC Cancer 9, 287 (2009).
87. De Noo, M. E. et al. Detection of colorectal cancer using MALDI-TOF serum protein profiling. Eur. J. Cancer 42, 1068-1076 (2006).
88. Ward, D. G. et al. Proteomic profiling of urine for the detection of colon cancer. Proteome Sci. 6, 19 (2008).
89. Smith, F. M. et al. Combination of SELDI-TOF MS and data mining provides early-stage response prediction for rectal tumors undergoing multimodal neoadjuvant therapy. Ann. Surg. 245, 259-266 (2007). (Pubitemid 46151655)
90. Liao, C. C. et al. Analysis of post-operative changes in serum protein expression profiles from colorectal cancer patients by MALDI-TOF mass spectrometry: a pilot methodological study. World J. Surg. Oncol. 8, 33 (2010).
91. Petricoin, E. F., Belluco, C., Araujo, R. P. & Liotta, L. A. The blood peptidome: a higher dimension of information content for cancer biomarker discovery. Nat. Rev. Cancer 6, 961-967 (2006). (Pubitemid 44862680)
92. Albrethsen, J. Reproducibility in protein profiling by MALDI-TOF mass spectrometry. Clin. Chem. 53, 852-858 (2007). (Pubitemid 46744240)
93. Karsan, A. et al. Analytical and pre-analytical biases in serum proteomic pattern analysis for breast cancer diagnosis. Clin. Chem. 51, 1525-1528 (2005). (Pubitemid 41060893)
94. Omenn, G. S., Aebersold, R. & Paik, Y. K. 7(th) HUPO World Congress of Proteomics: launching the second phase of the HUPOPlasma Proteome Project (PPP 2) 16-20 August 2008, Amsterdam, The Netherlands. Proteomics 9, 4-6 (2009).
95. Vogel, C. & Marcotte, E. M. Absolute abundance for the masses. Nat. Biotechnol. 27, 825-826 (2009).
96. Whiteaker, J. R. et al. A targeted proteomics-based pipeline for verification of biomarkers in plasma. Nat. Biotechnol. 29, 625-634 (2011).
97. Fan, R. et al. Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood. Nat. Biotechnol. 26, 1373-1378 (2008).
98. Rissin, D. M. et al. Single-molecule enzyme-linked immunosorbent assay detects serum proteins at subfemtomolar concentrations. Nat. Biotechnol. 28, 595-599 (2010).
99. Gaster, R. S. et al. Matrix-insensitive protein assays push the limits of biosensors in medicine. Nat. Med. 15, 1327-1332 (2009).
100. Fleischhacker, M. & Schmidt, B. Circulating nucleic acids (CNAs) and cancer-a survey. Biochim. Biophys. Acta 1775, 181-232 (2007). (Pubitemid 44911084)
101. Vlassov, V. V., Laktionov, P. P. & Rykova, E. Y. Circulating nucleic acids as a potential source for cancer biomarkers. Curr. Mol. Med. 10, 142-165 (2010).
102. Schwarzenbach, H., Hoon, D. S. & Pantel, K. Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer 11, 426-437 (2011).
103. Diehl, F. et al. Circulating mutant DNA to assess tumor dynamics. Nat. Med. 14, 985-990 (2008).
104. Leary, R. J. et al. Development of personalized tumor biomarkers using massively parallel sequencing. Sci. Transl. Med. 2, 20ra14 (2010).
105. He, Y. et al. Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature 464, 610-614 (2010).
106. Holdhoff, M., Schmidt, K., Donehower, R. & Diaz, L. A. Jr. Analysis of circulating tumor DNA to confirm somatic KRAS mutations. J. Natl Cancer Inst. 101, 1284-1285 (2009).
107. Lofton-Day, C. et al. DNA methylation biomarkers for blood-based colorectal cancer screening. Clin. Chem. 54, 414-423 (2008). (Pubitemid 351302625)
108. deVos, T. et al. Circulating methylated SEPT9 DNA in plasma is a biomarker for colorectal cancer. Clin. Chem. 55, 1337-1346 (2009).
109. Mullard, A. Epigenomic colon cancer kit. Nat. Biotechnol. 27, 1066 (2009).
110. Tänzer, M. et al. Performance of epigenetic markers, SEPT9 and ALX4 in plasma for detection of colorectal precancerous lesions. PLoS ONE 5, e9061 (2010).
111. Liew, C. C., Ma, J., Tang, H. C., Zheng, R. & Dempsey, A. A. The peripheral blood transcriptome dynamically reflects system wide biology: a potential diagnostic tool. J. Lab. Clin. Med. 147, 126-132 (2006). (Pubitemid 43288168)
112. Han, M. et al. Novel blood-based five gene biomarker set for the detection of colorectal cancer. Clin. Cancer Res. 14, 455-460 (2008). (Pubitemid 351226113)
113. Marshall, K. W. et al. A blood-based biomarker panel for stratifying current risk for colorectal cancer. Int. J. Cancer 126, 1177-1186 (2010).
114. Yip, K. T. et al. A case-controlled validation study of a blood-based seven-gene biomarker panel for colorectal cancer in Malaysia. J. Exp. Clin. Cancer Res. 29, 128 (2010).
115. Song, B. & Ju, J. Impact of miRNAs in gastrointestinal cancer diagnosis and prognosis. Expert Rev. Mol. Med. 12, e33 (2010).
116. Dong, Y. et al. MicroRNA dysregulation in colorectal cancer: a clinical perspective. Br. J. Cancer 104, 893-898 (2011).
117. Aslam, M. I., Taylor, K., Pringle, J. H. & Jameson, J. S. MicroRNAs are novel biomarkers for colorectal cancer. Br. J. Surg. 96, 702-710 (2009).
118. Mostert, B., Sieuwerts, A. M., Martens, J. W. & Sleijer, S. Diagnostic applications of cell-free and circulating tumor cell associated miRNAs in cancer patients. Expert Rev. Mol. Diagn. 11, 259-275 (2011).
119. Tsujiura, M. et al. Circulating microRNAs in plasma of patients with gastric cancers. Br. J. Cancer 102, 1174-1179 (2010).
120. Huang, Z. et al. Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. Int. J. Cancer 127, 118-126 (2010).
121. Ng, E. K. et al. Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut 58, 1375-1381 (2009).
122. Link, A. et al. Fecal MicroRNAs as novel biomarkers for colon cancer screening. Cancer Epidemiol. Biomarkers Prev. 19, 1766-1774 (2010).
123. Diamandis, E. P. Cancer biomarkers: can we turn recent failures into success? J. Natl Cancer Inst. 102, 1462-1467 (2010).
124. Hanash, S. M., Baik, C. S. & Kallioniemi, O. Emerging molecular biomarkers-blood-based strategies to detect and monitor cancer. Nat. Rev. Clin. Oncol. 8, 142-150 (2011).
125. European Commission. European guidelines for quality assurance in colorectal cancer screening and diagnosis 1st edition. UEGF [online], http://www.uegf.org/eu-affairs/eu-news/CRC-guidelines-publication%20EU-2011.pdf (2010).
126. American Cancer Society. American Cancer Society recommendations for colorectal cancer early detection (People at increased or high risk). American Cancer Society [online], http://www.cancer.org/Cancer/ColonandRectumCancer/ MoreInformation/ColonandRectumCancerEarlyDetection/colorectal-cancer-early- detection-acs-recommendations (2011).
127. Pignone, M., Rich, M., Teutsch, S. M., Berg, A. O. & Lohr, K. N. Screening for colorectal cancer in adults at average risk: a summary of the evidence for the US preventative services task force. Ann. Intern. Med. 137, 132-141 (2002). (Pubitemid 34779159)
128. Sung, J. J. et al. Screening for colorectal cancer in Chinese: comparison of fecal occult blood test, flexible sigmoidoscopy, and colonoscopy. Gastroenterology 124, 608-614 (2003). (Pubitemid 36268479)
129. Levi, Z. et al. A quantitative immunochemical fecal occult blood test for colorectal neoplasia. Ann. Intern. Med. 146, 244-255 (2007). (Pubitemid 351650610)
130. Fernandes, L. C., Kim, S. B. & Matos, D. Cytokeratins and carcinoembryonic antigen in diagnosis, staging and prognosis of colorectal adenocarcinoma. World J. Gastroenterol. 11, 645-648 (2005). (Pubitemid 40227373)
131. Carpelan-Holmstrom, M. et al. Estimating the probability of cancer with several tumor markers in patients with colorectal disease. Oncology 66, 296-302 (2004). (Pubitemid 38822799)
132. Ahlquist, D. A. et al. Colorectal cancer screening by detection of altered human DNA in stool: feasibility of a multitarget assay panel. Gastroenterology 119, 1219-1227 (2000).
133. Calistri, D. et al. Fecal multiple molecular tests to detect colorectal cancer in stool. Clin. Gastroenterol. Hepatol. 1, 377-383 (2003). (Pubitemid 37248057)
134. Itzkowitz, S. H. et al. Improved fecal DNA test for colorectal cancer screening. Clin. Gastroenterol. Hepatol. 5, 111-117 (2007). (Pubitemid 46096834)
135. Wang, J. Y. et al. Development and evaluation of a colorimetric membrane-array method for the detection of circulating tumor cells in the peripheral blood of Taiwanese patients with colorectal cancer. Int. J. Mol. Med. 17, 737-747 (2006).
136. Chen, Y. D., Zheng, S., Yu, J. K. & Hu, X. Artificial neural networks analysis of surface enhanced laser desorption/ionisation mass spectra of serum protein pattern distinguishes colorectal cancer from healthy population. Clin. Cancer Res. 10, 8380-8385 (2004). (Pubitemid 40053400)
137. Yu, J. K., Chen, Y. D. & Zheng, S. An integrated approach to the detection of colorectal cancer utilizing proteomics and bioinformatics. World J. Gastroenterol. 10, 3127-3131 (2004). (Pubitemid 39419872)
138. Ward, D. G. et al. Identification of serum biomarkers for colon cancer by proteomic analysis. Br. J. Cancer 94, 1898-1905 (2006). (Pubitemid 43882582)
139. Chen, Y. D., Xie, P. P., Yu, J. W., Zhou, J. & Zheng, S. Classification and diagnostic prediction of colorectal cancer using protein profiling of serum and bioinformatics [Chinese]. Zhejiang Da Xue Xue Bao Yi Xue Ban 38, 470-477 (2009).
140. Alexandrov, T. et al. Biomarker discovery in MALDI-TOF serum protein profiles using discrete wavelet transformation. Bioinformatics 25, 643-649 (2009).
141. Grutzmann, R. et al. Sensitive detection of colorectal cancer in peripheral blood by septin 9 DNA methylation assay. PLoS ONE 3, e3759 (2008).
142. Wang, J. Y. et al. Molecular detection of APC, K ras and p53 mutations in the serum of colorectal cancer patients as circulating biomarkers. World J. Surg. 28, 721-726 (2004).
143. Leung, W. K. et al. Quantitative detection of promoter hypermethylation in multiple genes in the serum of patients with colorectal cancer. Am. J. Gastroenterol. 100, 2274-2279 (2005).
144. Schiedeck, T. H., Wellm, C., Roblick, U. J., Broll, R. & Bruch, H. P. Diagnosis and monitoring of colorectal cancer by L6 blood serum polymerase chain reaction is superior to carcinoembryonic antigen enzyme linked immunosorbent assay. Dis. Colon Rectum 46, 818-825 (2003). (Pubitemid 36693403)
145. Ng, E. K. et al. Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut 58, 1375-1381 (2009)