Current noninvasive tests for colorectal cancer screening: An overview of colorectal cancer screening tests

Le-Le Song, Yue-Min Li, Le-Le Song, Yue-Min Li

Abstract

Colorectal cancer (CRC) has become the third most common cancer in the world. Screening has been shown to be an effective way to identify early CRC and precancerous lesions, and to reduce its morbidity and mortality. Several types of noninvasive tests have been developed for CRC screening, including the fecal occult blood test (FOBT), the fecal immunochemical test (FIT), the fecal-based DNA test and the blood-based DNA test (the SEPT9 assay). FIT has replaced FOBT and become the major screening test due to high sensitivity, specificity and low costs. The fecal DNA test exhibited higher sensitivity than FIT but its current cost is high for a screening assay. The SEPT9 assay showed good compliance while its performance in screening needs further improvements. These tests exhibited distinct sensitivity and specificity in screening for CRC and adenoma. This article will focus on the performance of the current noninvasive in vitro diagnostic tests that have been used for CRC screening. The merits and drawbacks for these screening methods will also be compared regarding the techniques, usage and costs. We hope this review can provide suggestions for both the public and clinicians in choosing the appropriate method for CRC screening.

Keywords: Adenoma; Colorectal cancer; Fecal DNA; Fecal immunochemical test; SEPT9; Septin 9.

Conflict of interest statement

Conflict-of-interest statement: There is no conflict of interest associated with any of the senior author or other coauthors contributed their efforts in this manuscript.

References

    1. American Cancer Society. Cancer Facts & Figures 2013. American Cancer Society, GA, United States. Available from: .
    1. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D, Bray F. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49:1374–1403.
    1. The National Cancer Center and Disease Prevention and Control Bureau: The 2012 Annual Cancer Report of China. National Cancer Center and Disease Prevention and Control Bureau, Beijing, China.
    1. American Cancer Society. Colorectal Cancer Facts & Figures 2011-2013. American Cancer Society, GA, United States. Available from: .
    1. National Cancer Institute, PDQ, Treatment, Health Professionals. Survival Rate for Colorectal Cancer by Stage 1999. National Cancer Institute, Bethesda, MD, United States.
    1. Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM, Ederer F. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med. 1993;328:1365–1371.
    1. Hardcastle JD, Chamberlain JO, Robinson MH, Moss SM, Amar SS, Balfour TW, James PD, Mangham CM. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet. 1996;348:1472–1477.
    1. Kronborg O, Fenger C, Olsen J, Jørgensen OD, Søndergaard O. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet. 1996;348:1467–1471.
    1. Lieberman DA. Clinical practice. Screening for colorectal cancer. N Engl J Med. 2009;361:1179–1187.
    1. Ahlquist DA, Wieand HS, Moertel CG, McGill DB, Loprinzi CL, O’Connell MJ, Mailliard JA, Gerstner JB, Pandya K, Ellefson RD. Accuracy of fecal occult blood screening for colorectal neoplasia. A prospective study using Hemoccult and HemoQuant tests. JAMA. 1993;269:1262–1267.
    1. Ahlquist DA, Shuber AP. Stool screening for colorectal cancer: evolution from occult blood to molecular markers. Clin Chim Acta. 2002;315:157–168.
    1. Allison JE, Tekawa IS, Ransom LJ, Adrain AL. A comparison of fecal occult-blood tests for colorectal-cancer screening. N Engl J Med. 1996;334:155–159.
    1. Imperiale TF, Ransohoff DF, Itzkowitz SH, Turnbull BA, Ross ME. Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population. N Engl J Med. 2004;351:2704–2714.
    1. Lee JK, Liles EG, Bent S, Levin TR, Corley DA. Accuracy of fecal immunochemical tests for colorectal cancer: systematic review and meta-analysis. Ann Intern Med. 2014;160:171.
    1. Allison JE, Sakoda LC, Levin TR, Tucker JP, Tekawa IS, Cuff T, Pauly MP, Shlager L, Palitz AM, Zhao WK, et al. Screening for colorectal neoplasms with new fecal occult blood tests: update on performance characteristics. J Natl Cancer Inst. 2007;99:1462–1470.
    1. Cheng TI, Wong JM, Hong CF, Cheng SH, Cheng TJ, Shieh MJ, Lin YM, Tso CY, Huang AT. Colorectal cancer screening in asymptomaic adults: comparison of colonoscopy, sigmoidoscopy and fecal occult blood tests. J Formos Med Assoc. 2002;101:685–690.
    1. Nakama H, Yamamoto M, Kamijo N, Li T, Wei N, Fattah AS, Zhang B. Colonoscopic evaluation of immunochemical fecal occult blood test for detection of colorectal neoplasia. Hepatogastroenterology. 1999;46:228–231.
    1. Nakama H, Kamijo N, Abdul Fattah AS, Zhang B. Validity of immunological faecal occult blood screening for colorectal cancer: a follow up study. J Med Screen. 1996;3:63–65.
    1. Parra-Blanco A, Gimeno-García AZ, Quintero E, Nicolás D, Moreno SG, Jiménez A, Hernández-Guerra M, Carrillo-Palau M, Eishi Y, López-Bastida J. Diagnostic accuracy of immunochemical versus guaiac faecal occult blood tests for colorectal cancer screening. J Gastroenterol. 2010;45:703–712.
    1. Chiu HM, Lee YC, Tu CH, Chen CC, Tseng PH, Liang JT, Shun CT, Lin JT, Wu MS. Association between early stage colon neoplasms and false-negative results from the fecal immunochemical test. Clin Gastroenterol Hepatol. 2013;11:832–8.e1-832-8.e2.
    1. Chiang TH, Lee YC, Tu CH, Chiu HM, Wu MS. Performance of the immunochemical fecal occult blood test in predicting lesions in the lower gastrointestinal tract. CMAJ. 2011;183:1474–1481.
    1. Sohn DK, Jeong SY, Choi HS, Lim SB, Huh JM, Kim DH, Kim DY, Kim YH, Chang HJ, Jung KH, et al. Single immunochemical fecal occult blood test for detection of colorectal neoplasia. Cancer Res Treat. 2005;37:20–23.
    1. Levi Z, Birkenfeld S, Vilkin A, Bar-Chana M, Lifshitz I, Chared M, Maoz E, Niv Y. 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;128:2415–2424.
    1. Levi Z, Rozen P, Hazazi R, Vilkin A, Waked A, Maoz E, Birkenfeld S, Leshno M, Niv Y. A quantitative immunochemical fecal occult blood test for colorectal neoplasia. Ann Intern Med. 2007;146:244–255.
    1. Morikawa T, Kato J, Yamaji Y, Wada R, Mitsushima T, Shiratori Y. A comparison of the immunochemical fecal occult blood test and total colonoscopy in the asymptomatic population. Gastroenterology. 2005;129:422–428.
    1. Launoy GD, Bertrand HJ, Berchi C, Talbourdet VY, Guizard AV, Bouvier VM, Caces ER. Evaluation of an immunochemical fecal occult blood test with automated reading in screening for colorectal cancer in a general average-risk population. Int J Cancer. 2005;115:493–496.
    1. Itoh M, Takahashi K, Nishida H, Sakagami K, Okubo T. Estimation of the optimal cut off point in a new immunological faecal occult blood test in a corporate colorectal cancer screening programme. J Med Screen. 1996;3:66–71.
    1. Nakazato M, Yamano HO, Matsushita HO, Sato K, Fujita K, Yamanaka Y, Imai Y. Immunologic fecal occult blood test for colorectal cancer screening. JMAJ. 2006;49:203–207.
    1. Park DI, Ryu S, Kim YH, Lee SH, Lee CK, Eun CS, Han DS. Comparison of guaiac-based and quantitative immunochemical fecal occult blood testing in a population at average risk undergoing colorectal cancer screening. Am J Gastroenterol. 2010;105:2017–2025.
    1. de Wijkerslooth TR, Stoop EM, Bossuyt PM, Meijer GA, van Ballegooijen M, van Roon AH, Stegeman I, Kraaijenhagen RA, Fockens P, van Leerdam ME, et al. Immunochemical fecal occult blood testing is equally sensitive for proximal and distal advanced neoplasia. Am J Gastroenterol. 2012;107:1570–1578.
    1. Brenner H, Tao S. Superior diagnostic performance of faecal immunochemical tests for haemoglobin in a head-to-head comparison with guaiac based faecal occult blood test among 2235 participants of screening colonoscopy. Eur J Cancer. 2013;49:3049–3054.
    1. Imperiale TF, Ransohoff DF, Itzkowitz SH, Levin TR, Lavin P, Lidgard GP, Ahlquist DA, Berger BM. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 2014;370:1287–1297.
    1. Church TR, Wandell M, Lofton-Day C, Mongin SJ, Burger M, Payne SR, Castaños-Vélez E, Blumenstein BA, Rösch T, Osborn N, et al. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut. 2014;63:317–325.
    1. Binefa G, Rodríguez-Moranta F, Teule A, Medina-Hayas M. Colorectal cancer: from prevention to personalized medicine. World J Gastroenterol. 2014;20:6786–6808.
    1. Dhaliwal A, Vlachostergios PJ, Oikonomou KG, Moshenyat Y. Fecal DNA testing for colorectal cancer screening: Molecular targets and perspectives. World J Gastrointest Oncol. 2015;7:178–183.
    1. Lofton-Day C, Model F, Devos T, Tetzner R, Distler J, Schuster M, Song X, Lesche R, Liebenberg V, Ebert M, et al. DNA methylation biomarkers for blood-based colorectal cancer screening. Clin Chem. 2008;54:414–423.
    1. Grützmann R, Molnar B, Pilarsky C, Habermann JK, Schlag PM, Saeger HD, Miehlke S, Stolz T, Model F, Roblick UJ, et al. Sensitive detection of colorectal cancer in peripheral blood by septin 9 DNA methylation assay. PLoS One. 2008;3:e3759.
    1. deVos T, Tetzner R, Model F, Weiss G, Schuster M, Distler J, Steiger KV, Grützmann R, Pilarsky C, Habermann JK, et al. Circulating methylated SEPT9 DNA in plasma is a biomarker for colorectal cancer. Clin Chem. 2009;55:1337–1346.
    1. Tänzer M, Balluff B, Distler J, Hale K, Leodolter A, Röcken C, Molnar B, Schmid R, Lofton-Day C, Schuster T, et al. Performance of epigenetic markers SEPT9 and ALX4 in plasma for detection of colorectal precancerous lesions. PLoS One. 2010;5:e9061.
    1. Warren JD, Xiong W, Bunker AM, Vaughn CP, Furtado LV, Roberts WL, Fang JC, Samowitz WS, Heichman KA. Septin 9 methylated DNA is a sensitive and specific blood test for colorectal cancer. BMC Med. 2011;9:133.
    1. Tóth K, Sipos F, Kalmár A, Patai AV, Wichmann B, Stoehr R, Golcher H, Schellerer V, Tulassay Z, Molnár B. Detection of methylated SEPT9 in plasma is a reliable screening method for both left- and right-sided colon cancers. PLoS One. 2012;7:e46000.
    1. Weiss G, Rösch T. Potential of a new blood test for colorectal cancer screening - the Septin 9 gene biomarker. Eur Oncol. 2010;6:51–54.
    1. Potter NT, Hurban P, White MN, Whitlock KD, Lofton-Day CE, Tetzner R, Koenig T, Quigley NB, Weiss G. Validation of a real-time PCR-based qualitative assay for the detection of methylated SEPT9 DNA in human plasma. Clin Chem. 2014;60:1183–1191.
    1. Johnson DA, Barclay RL, Mergener K, Weiss G, König T, Beck J, Potter NT. Plasma Septin9 versus fecal immunochemical testing for colorectal cancer screening: a prospective multicenter study. PLoS One. 2014;9:e98238.
    1. Tóth K, Wasserkort R, Sipos F, Kalmár A, Wichmann B, Leiszter K, Valcz G, Juhász M, Miheller P, Patai ÁV, Tulassay Z, Molnár B. Detection of methylated septin 9 in tissue and plasma of colorectal patients with neoplasia and the relationship to the amount of circulating cell-free DNA. PLoS One. 2014;9:e115415.
    1. Jin P, Kang Q, Wang X, Yang L, Yu Y, Li N, He YQ, Han X, Hang J, Zhang J, et al. Performance of a second-generation methylated SEPT9 test in detecting colorectal neoplasm. J Gastroenterol Hepatol. 2015;30:830–833.
    1. Lee HS, Hwang SM, Kim TS, Kim DW, Park DJ, Kang SB, Kim HH, Park KU. Circulating methylated septin 9 nucleic Acid in the plasma of patients with gastrointestinal cancer in the stomach and colon. Transl Oncol. 2013;6:290–296.
    1. Li Y, Song L, Gong Y, He B. Detection of colorectal cancer by DNA methylation biomarker SEPT9: past, present and future. Biomark Med. 2014;8:755–769.
    1. Song L, Li Y. SEPT9: A Specific Circulating Biomarker for Colorectal Cancer. Adv Clin Chem. 2015;72:171–204.
    1. Adler A, Geiger S, Keil A, Bias H, Schatz P, deVos T, Dhein J, Zimmermann M, Tauber R, Wiedenmann B. Improving compliance to colorectal cancer screening using blood and stool based tests in patients refusing screening colonoscopy in Germany. BMC Gastroenterol. 2014;14:183.
    1. Wild N, Andres H, Rollinger W, Krause F, Dilba P, Tacke M, Karl J. A combination of serum markers for the early detection of colorectal cancer. Clin Cancer Res. 2010;16:6111–6121.
    1. Chen JS, Chen KT, Fan WC, Yu JS, Chang YS, Chan EC. Combined analysis of survivin autoantibody and carcinoembryonic antigen biomarkers for improved detection of colorectal cancer. Clin Chem Lab Med. 2010;48:719–725.
    1. Yu H, Son GM, Joh YG. The clinical significance of preoperative serum levels of carbohydrate antigen 19-9 in colorectal cancer. J Korean Surg Soc. 2013;84:231–237.
    1. Fu H, Wang W, Cai Q. The application of combined detection of serum tumor markers levels of patients with colon cancer. Chin J Clin. 2012;6:5087–5090.
    1. Wu D, Zhou G, Jin P, Zhu J, Li S, Wu Q, Wang G, Sheng J, Wang J, Song L, et al. Detection of Colorectal Cancer Using a Simplified SEPT9 Gene Methylation Assay Is a Reliable Method for Opportunistic Screening. J Mol Diagn. 2016;18:535–545.

Source: PubMed

Sponzoři a spolupracovníci

Zdravotní podmínky

Drogové intervence

3
Předplatit