Diagnostic Value of Aberrant Methylation of Genes in Stool for Colorectal Tumor: A Meta-Analysis_Chinese Journal of Evidence-Based Medicine

Authors：

ZHANG Hu ^1,2 ,  ZHU Youqing ^1,2 , WU Yaqiong ³ , GUO Yi ⁴ , QI Jian ^1,2

1. Department of Digestive Disease, Zhongnan Hospital of Wuhan University, Wuhan 430071, China;2. Clinical Center of Intestinal and Colorectal Diseases of Hubei Province, Key Laboratory of Intestinal and Colorectal Diseases of Hubei Province, Wuhan 430071, China;3. Yijishan Hospital of Wannan Medical College, Wuhu 241001, China;4. Department of Epidemiology, College of Public Health, Wuhan University, Wuhan 430071, China;

Corresponding author：

ZHU Youqing, Email: uqing_zhu@sina.com

Keywords：

Colorectal tumor; Colorectal cancer; Stool; Methylation; Systematic review; Meta-analysis; Diagnostic test

DOI：

10.7507/1672-2531.20130027

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective 　To evaluate the diagnostic accuracy of the aberrant methylation of genes in stool for colorectal tumor.
Methods 　Databases including The Cochrane Library, PubMed, EMbase, CBM, Web of Science, CNKI and WanFang Data were searched to collect the diagnostic trials on the aberrant methylation of genes in stool for colorectal tumor published from January 1990 to February 2012. QUADAS items were used to evaluate the quality of the included studies, and the meta-analysis was conducted using Meta-Disc 1.4 software.
Results 　A total of 32 studies involving 3 951 patients were included. The results of meta-analysis showed that, for detecting the colorectal tumor, the weighted sensitivity, specificity, diagnostic odds ratio (DOR), area under the summary receiver operating characteristic (SROC) curve and Q were 92% (95%CI 91% to 93%), 63% (95%CI 61% to 65%), 20.79 (95%CI 15.13 to 28.57), 0.861 9 (SE=0.020 4), and 0.792 6 (SE=0.019 8), respectively. For detecting the colorectal cancer, the weighted sensitivity, specificity and area under the curve (AUC) were 91% (95%CI 89% to 92%), 75% (95%CI 73% to 77%), and 0.900 7, respectively. For detecting the colorectal adenoma, the weighted sensitivity, specificity and AUC were 79% (95%CI 76% to 83%), 75% (95%CI 73% to 77%), and 0.845 7, respectively.
Conclusion 　With high sensitivity (92%) and moderate specificity (63%), aberrant methylation of genes in stool can be used as an optional noninvasive method for the diagnosis of colorectal tumor.

Citation： ZHANG Hu,ZHU Youqing,WU Yaqiong,GUO Yi,QI Jian. Diagnostic Value of Aberrant Methylation of Genes in Stool for Colorectal Tumor: A Meta-Analysis. Chinese Journal of Evidence-Based Medicine, 2013, 13(2): 149-159. doi: 10.7507/1672-2531.20130027 Copy

1. Center MM, Jemal A, Ward E. International trends in colorectal cancer incidence rates. Cancer Epidemiol Biomarkers Prev, 2009, 18(6): 1688-1694.

2. Kohler BA, Ward E, Mccarthy BJ, et al. Annual report to the nation on the status of cancer, 1975-2007, featuring tumors of the brain and other nervous system. J Natl Cancer Inst, 2011, 103(9): 714-736.

3. Jemal A, Siegel R, Xu J, et al. Cancer statistics, 2010. CA Cancer J Clin, 2010, 60(5): 277-300.

4. 中华医学会消化病学分会. 中国结直肠肿瘤筛查、早诊早治和综合预防共识意见. 胃肠病学, 2011, 16(11): 666-675.

5. Gumaste VV. CT colonography can be an adjunct to optical colonoscopy in CRC screening. Dig Dis Sci, 2009, 54(2): 212-217.

6. Chen WD, Han ZJ, Skoletsky J, et al. Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. Journal of the National Cancer Institute, 2005, 97(15): 1124-1132.

7. Olson J, Whitney DH, Durkee K, et al. DNA stabilization is critical for maximizing performance of fecal DNA-based colorectal cancer tests. Diagnostic Molecular Pathology, 2005, 14(3): 183-191.

8. Altekruse SF, Kosary CL, Krapcho M, et al. SEER Cancer Statistics Review 2009, 2009.

9. Whiting P, Rutjes AW, Reitsma JB, et al. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodology, 2003, 3: 25.

10. Ahlquist DA, Taylor WR, Mahoney DW, et al. The stool DNA test is more accurate than the plasma septin 9 test in detecting colorectal neoplasia. Clin Gastroenterol Hepatol, 2012, 10(3): 272-277.

11. Bosch L, Oort FA, Neerincx M, et al. DNA methylation of phosphatase and actin regulator 3 detects colorectal cancer in stool and complements FIT. Cancer Prevention Research, 2012, 5(3): 464-472.

12. Ahlquist DA, Zou HZ, Domanico M, et al. Next generation stool DNA test accurately detects colorectal cancer and large adenomas. Gastroenterology, 2012, 142(2): 248-256.

13. Azuara D, Rodriguez-Moranta F, Biondo S, et al. Novel methylation panel for the early detection of colorectal tumors in stool DNA. Clin Colorectal Cancer, 2010, 9(3): 168-176.

14. Tang D, Liu J, Wang DR, et al. Diagnostic and prognostic value of the methylation status of secreted frizzled-related protein 2 in colorectal cancer. Clin Invest Med, 2011, 34(2): E88-E95.

15. Baek YH, Chang E, Kim YJ, et al. Stool methylation specific polymerase chain reaction assay for the detection of colorectal neoplasia in Korean patients. Dis Colon Rectum, 2009, 52(8): 1452-1463.

16. Li M, Chen WD, Papadopoulos N, et al. Sensitive digital quantification of DNA methylation in clinical samples. Nat Biotechnol, 2009, 27(9): 858-863.

17. Melotte V, Lentjes MH, Bosch SM, et al. N-Myc downstream-regulated gene 4 (NDRG4): a candidate tumor suppressor gene and potential biomarker for colorectal cancer. J Natl Cancer Inst, 2009, 101(13): 916-927.

18. Ausch C, Kim YH, Tsuchiya KD, et al. Comparative analysis of PCR based biomarker assay methods for colorectal polyp detection from fecal DNA. Clinical Chemistry, 2009, 55(8): 1559-1563.

19. Hellebrekers DM, Lentjes MH, Bosch SM, et al. GATA4 and GATA5 are potential tumor suppressors and biomarkers in colorectal cancer. Clin Cancer Res, 2009, 15(12): 3990-3997.

20. Mayor R, Casadome L, Azuara D, et al. Long range epigenetic silencing at 2q14.2 affects most human colorectal cancers and may have application as a non-invasive biomarker of disease. Br J Cancer, 2009, 100(10): 1534-1539.

21. Kim MS, Louwagie J, Carvalho B, et al. Promoter DNA methylation of oncostatin M receptor-beta as a novel diagnostic and therapeutic marker in ccolon cancer. Plos One, 2009, 4(e65558).

22. Nagasaka T, Tanaka N, Cullings HM, et al. Analysis of fecal DNA methylation to detect gastrointestinal neoplasia. Journal of the National Cancer Institute, 2009, 101(18): 1244-1258.

23. Glockner SC, Dhir M, Yi JM, et al. Methylation of TFPI2 in stool DNA: a potential novel biomarker for the detection of colorectal cancer. Cancer Res, 2009, 69(11): 4691-4699.

24. Wang DR, Tang D. Hypermethylated SFRP2 gene in fecal DNA is a high potential biomarker for colorectal cancer noninvasive screening. World J Gastroenterol, 2008, 14(4): 524-531.

25. Oberwalder M, Zitt M, Wontner C, et al. SFRP2 methylation in fecal DNA--a marker for colorectal polyps. Int J Colorectal Dis, 2008, 23(1): 15-19.

26. Itzkowitz S, Brand R, Jandorf L, et al. A simplified, noninvasive stool DNA test for colorectal cancer detection. Am J Gastroenterol, 2008, 103(11): 2862-2870.

27. Huang ZH, Li LH, Yang F, et al. Detection of aberrant methylation in fecal DNA as a molecular screening tool for colorectal cancer and precancerous lesions. World J Gastroenterol, 2007, 13(6): 950-954.

28. Itzkowitz SH, Jandorf L, Brand R, et al. Improved fecal DNA test for colorectal cancer screening. Clin Gastroenterol Hepatol, 2007, 5(1): 111-117.

29. Abbaszadegan MR, Tavasoli A, Velayati A, et al. Stool-based DNA testing, a new noninvasive method for colorectal cancer screening, the first report from Iran. World J Gastroenterol, 2007, 13(10): 1528-1533.

30. Zhang W, Bauer M, Croner R S, et al. DNA stool test for colorectal cancer: hypermethylation of the secreted frizzled-related protein-1 gene. Dis Colon Rectum, 2007, 50(10): 1618-1627.

31. Leung WK, To KF, Man EP, et al. Detection of hypermethylated DNA or cyclooxygenase-2 messenger RNA in fecal samples of patients with colorectal cancer or polyps. Am J Gastroenterol, 2007, 102(5): 1070-1076.

32. Petko Z, Ghiassi M, Shuber A, et al. Aberrantly methylated CDKN2A, MGMT, and MLH1 in colon polyps and in fecal DNA from patients with colorectal polyps. Clin Cancer Res, 2005, 11(3): 1203-1209.

33. Lenhard K, Bommer GT, Asutay S, et al. Analysis of promoter methylation in stool: a novel method for the detection of colorectal cancer. Clin Gastroenterol Hepatol, 2005, 3(2): 142-149.

34. Chen WD, Han ZJ, Skoletsky J, et al. Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. J Natl Cancer Inst, 2005, 97(15): 1124-1132.

35. Muller HM, Oberwalder M, Fiegl H, et al. Methylation changes in faecal DNA: a marker for colorectal cancer screening? Lancet, 2004, 363(9417): 1283-1285.

36. 徐梅华, 蔡克银, 涂颖. 粪便基因甲基化分析对大肠癌的早期诊断价值. 临床消化病杂志, 2012, 24(1): 17-19.

37. 康燕平, 曹付傲, 常文军, 等. 粪便基因甲基化检测在结直肠癌及其癌前病变筛查中的作用. 中华胃肠外科杂志, 2011, 14(1): 52-56.

38. 张金平, 王静, 桂银莉, 等. 人粪便中基因甲基化分析在大肠癌早期筛查中的意义. 中华医学杂志, 2011, 91(35): 2482-2484.

39. 付蕾, 盛剑秋, 孟晓明, 等. 粪便DNA的Vimentin基因甲基化检测在结直肠癌患者早期诊断中的意义. 胃肠病学和肝病学杂志, 2010, 19(7): 601-603.

40. 凌志安, 陈利生, 何纯刚. 粪便p16基因甲基化状态在结直肠癌早期诊断的意义. 结直肠肛门外科, 2009, 15(3): 144-148.

41. 黄朝晖, 李莉华, 杨帆, 等. 粪便DNA甲基化分析在结直肠癌诊断中的应用价值. 中华检验医学杂志, 2007, 30(6): 617-620.

42. 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(1): 62-68.

43. Tagore KS, Levin TR, Lawson MJ. The evolution to stool DNA testing for colorectal cancer. Alimentary Pharmacology and Therapeutics, 2004, 19(12): 1225-1233,.

44. Bourke MJ. Making every colonoscopy count: Ensuring quality in endoscopy. J Gastroenterol Hepatol, 2009, 24(Suppl 3): S43-50.

45. Ahlquist DA. Molecular detection of colorectal neoplasia. Gastroenterology, 2010, 138(6): 2127-2139.

46. 齐健, 朱尤庆, 李霞, 等. 不同阶段结直肠肿瘤分泌型卷曲相关蛋白基因甲基化及表达. 中华消化杂志, 2007, 27(4): 251-254.

47. Qi J, Zhu YQ, Luo J, et al. Hypermethylation and expression regulation of secreted frizzled-related protein genes in colorectal tumor. World J Gastroenterology, 2006, 12(44): 7113-7117.

48. Qi J, Zhu YQ. Targeting the most upstream site of Wnt signaling pathway provides a strategic advantage for therapy in colorectal cancer. Curr Drug Targets, 2008, 9(7): 548-557.

49. Issa JP, Ahuja N, Toyota M, et al. Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Res, 2001, 61(9): 3573-3577.

50. Lichtenstein P, Holm NV, Verkasalo PK, et al. Environmental and heritable factors in the causation of cancer--analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med, 2000, 343(2): 78-85.

51. Hsieh CJ, Klump B, Holzmann K, et al. Hypermethylation of the p16INK4a promoter in colectomy specimens of patients with long-standing and extensive ulcerative colitis. Cancer Res, 1998, 58(17): 3942-3945.

52. Issa JP, Ottaviano YL, Celano P, et al. Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet, 1994, 7(4): 536-540.

53. Suzuki K, Suzuki I, Leodolter A, et al. Global DNA demethylation in gastrointestinal cancer is age dependent and precedes genomic damage. Cancer Cell, 2006, 9(3): 199-207.

1. Center MM, Jemal A, Ward E. International trends in colorectal cancer incidence rates. Cancer Epidemiol Biomarkers Prev, 2009, 18(6): 1688-1694.

2. Kohler BA, Ward E, Mccarthy BJ, et al. Annual report to the nation on the status of cancer, 1975-2007, featuring tumors of the brain and other nervous system. J Natl Cancer Inst, 2011, 103(9): 714-736.

3. Jemal A, Siegel R, Xu J, et al. Cancer statistics, 2010. CA Cancer J Clin, 2010, 60(5): 277-300.

4. 中华医学会消化病学分会. 中国结直肠肿瘤筛查、早诊早治和综合预防共识意见. 胃肠病学, 2011, 16(11): 666-675.

5. Gumaste VV. CT colonography can be an adjunct to optical colonoscopy in CRC screening. Dig Dis Sci, 2009, 54(2): 212-217.

6. Chen WD, Han ZJ, Skoletsky J, et al. Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. Journal of the National Cancer Institute, 2005, 97(15): 1124-1132.

7. Olson J, Whitney DH, Durkee K, et al. DNA stabilization is critical for maximizing performance of fecal DNA-based colorectal cancer tests. Diagnostic Molecular Pathology, 2005, 14(3): 183-191.

8. Altekruse SF, Kosary CL, Krapcho M, et al. SEER Cancer Statistics Review 2009, 2009.

9. Whiting P, Rutjes AW, Reitsma JB, et al. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodology, 2003, 3: 25.

10. Ahlquist DA, Taylor WR, Mahoney DW, et al. The stool DNA test is more accurate than the plasma septin 9 test in detecting colorectal neoplasia. Clin Gastroenterol Hepatol, 2012, 10(3): 272-277.

11. Bosch L, Oort FA, Neerincx M, et al. DNA methylation of phosphatase and actin regulator 3 detects colorectal cancer in stool and complements FIT. Cancer Prevention Research, 2012, 5(3): 464-472.

12. Ahlquist DA, Zou HZ, Domanico M, et al. Next generation stool DNA test accurately detects colorectal cancer and large adenomas. Gastroenterology, 2012, 142(2): 248-256.

13. Azuara D, Rodriguez-Moranta F, Biondo S, et al. Novel methylation panel for the early detection of colorectal tumors in stool DNA. Clin Colorectal Cancer, 2010, 9(3): 168-176.

14. Tang D, Liu J, Wang DR, et al. Diagnostic and prognostic value of the methylation status of secreted frizzled-related protein 2 in colorectal cancer. Clin Invest Med, 2011, 34(2): E88-E95.

15. Baek YH, Chang E, Kim YJ, et al. Stool methylation specific polymerase chain reaction assay for the detection of colorectal neoplasia in Korean patients. Dis Colon Rectum, 2009, 52(8): 1452-1463.

16. Li M, Chen WD, Papadopoulos N, et al. Sensitive digital quantification of DNA methylation in clinical samples. Nat Biotechnol, 2009, 27(9): 858-863.

17. Melotte V, Lentjes MH, Bosch SM, et al. N-Myc downstream-regulated gene 4 (NDRG4): a candidate tumor suppressor gene and potential biomarker for colorectal cancer. J Natl Cancer Inst, 2009, 101(13): 916-927.

18. Ausch C, Kim YH, Tsuchiya KD, et al. Comparative analysis of PCR based biomarker assay methods for colorectal polyp detection from fecal DNA. Clinical Chemistry, 2009, 55(8): 1559-1563.

19. Hellebrekers DM, Lentjes MH, Bosch SM, et al. GATA4 and GATA5 are potential tumor suppressors and biomarkers in colorectal cancer. Clin Cancer Res, 2009, 15(12): 3990-3997.

20. Mayor R, Casadome L, Azuara D, et al. Long range epigenetic silencing at 2q14.2 affects most human colorectal cancers and may have application as a non-invasive biomarker of disease. Br J Cancer, 2009, 100(10): 1534-1539.

21. Kim MS, Louwagie J, Carvalho B, et al. Promoter DNA methylation of oncostatin M receptor-beta as a novel diagnostic and therapeutic marker in ccolon cancer. Plos One, 2009, 4(e65558).

22. Nagasaka T, Tanaka N, Cullings HM, et al. Analysis of fecal DNA methylation to detect gastrointestinal neoplasia. Journal of the National Cancer Institute, 2009, 101(18): 1244-1258.

23. Glockner SC, Dhir M, Yi JM, et al. Methylation of TFPI2 in stool DNA: a potential novel biomarker for the detection of colorectal cancer. Cancer Res, 2009, 69(11): 4691-4699.

24. Wang DR, Tang D. Hypermethylated SFRP2 gene in fecal DNA is a high potential biomarker for colorectal cancer noninvasive screening. World J Gastroenterol, 2008, 14(4): 524-531.

25. Oberwalder M, Zitt M, Wontner C, et al. SFRP2 methylation in fecal DNA--a marker for colorectal polyps. Int J Colorectal Dis, 2008, 23(1): 15-19.

26. Itzkowitz S, Brand R, Jandorf L, et al. A simplified, noninvasive stool DNA test for colorectal cancer detection. Am J Gastroenterol, 2008, 103(11): 2862-2870.

27. Huang ZH, Li LH, Yang F, et al. Detection of aberrant methylation in fecal DNA as a molecular screening tool for colorectal cancer and precancerous lesions. World J Gastroenterol, 2007, 13(6): 950-954.

28. Itzkowitz SH, Jandorf L, Brand R, et al. Improved fecal DNA test for colorectal cancer screening. Clin Gastroenterol Hepatol, 2007, 5(1): 111-117.

29. Abbaszadegan MR, Tavasoli A, Velayati A, et al. Stool-based DNA testing, a new noninvasive method for colorectal cancer screening, the first report from Iran. World J Gastroenterol, 2007, 13(10): 1528-1533.

30. Zhang W, Bauer M, Croner R S, et al. DNA stool test for colorectal cancer: hypermethylation of the secreted frizzled-related protein-1 gene. Dis Colon Rectum, 2007, 50(10): 1618-1627.

31. Leung WK, To KF, Man EP, et al. Detection of hypermethylated DNA or cyclooxygenase-2 messenger RNA in fecal samples of patients with colorectal cancer or polyps. Am J Gastroenterol, 2007, 102(5): 1070-1076.

32. Petko Z, Ghiassi M, Shuber A, et al. Aberrantly methylated CDKN2A, MGMT, and MLH1 in colon polyps and in fecal DNA from patients with colorectal polyps. Clin Cancer Res, 2005, 11(3): 1203-1209.

33. Lenhard K, Bommer GT, Asutay S, et al. Analysis of promoter methylation in stool: a novel method for the detection of colorectal cancer. Clin Gastroenterol Hepatol, 2005, 3(2): 142-149.

34. Chen WD, Han ZJ, Skoletsky J, et al. Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. J Natl Cancer Inst, 2005, 97(15): 1124-1132.

35. Muller HM, Oberwalder M, Fiegl H, et al. Methylation changes in faecal DNA: a marker for colorectal cancer screening? Lancet, 2004, 363(9417): 1283-1285.

36. 徐梅华, 蔡克银, 涂颖. 粪便基因甲基化分析对大肠癌的早期诊断价值. 临床消化病杂志, 2012, 24(1): 17-19.

37. 康燕平, 曹付傲, 常文军, 等. 粪便基因甲基化检测在结直肠癌及其癌前病变筛查中的作用. 中华胃肠外科杂志, 2011, 14(1): 52-56.

38. 张金平, 王静, 桂银莉, 等. 人粪便中基因甲基化分析在大肠癌早期筛查中的意义. 中华医学杂志, 2011, 91(35): 2482-2484.

39. 付蕾, 盛剑秋, 孟晓明, 等. 粪便DNA的Vimentin基因甲基化检测在结直肠癌患者早期诊断中的意义. 胃肠病学和肝病学杂志, 2010, 19(7): 601-603.

40. 凌志安, 陈利生, 何纯刚. 粪便p16基因甲基化状态在结直肠癌早期诊断的意义. 结直肠肛门外科, 2009, 15(3): 144-148.

41. 黄朝晖, 李莉华, 杨帆, 等. 粪便DNA甲基化分析在结直肠癌诊断中的应用价值. 中华检验医学杂志, 2007, 30(6): 617-620.

42. 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(1): 62-68.

43. Tagore KS, Levin TR, Lawson MJ. The evolution to stool DNA testing for colorectal cancer. Alimentary Pharmacology and Therapeutics, 2004, 19(12): 1225-1233,.

44. Bourke MJ. Making every colonoscopy count: Ensuring quality in endoscopy. J Gastroenterol Hepatol, 2009, 24(Suppl 3): S43-50.

45. Ahlquist DA. Molecular detection of colorectal neoplasia. Gastroenterology, 2010, 138(6): 2127-2139.

46. 齐健, 朱尤庆, 李霞, 等. 不同阶段结直肠肿瘤分泌型卷曲相关蛋白基因甲基化及表达. 中华消化杂志, 2007, 27(4): 251-254.

47. Qi J, Zhu YQ, Luo J, et al. Hypermethylation and expression regulation of secreted frizzled-related protein genes in colorectal tumor. World J Gastroenterology, 2006, 12(44): 7113-7117.

48. Qi J, Zhu YQ. Targeting the most upstream site of Wnt signaling pathway provides a strategic advantage for therapy in colorectal cancer. Curr Drug Targets, 2008, 9(7): 548-557.

49. Issa JP, Ahuja N, Toyota M, et al. Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Res, 2001, 61(9): 3573-3577.

50. Lichtenstein P, Holm NV, Verkasalo PK, et al. Environmental and heritable factors in the causation of cancer--analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med, 2000, 343(2): 78-85.

51. Hsieh CJ, Klump B, Holzmann K, et al. Hypermethylation of the p16INK4a promoter in colectomy specimens of patients with long-standing and extensive ulcerative colitis. Cancer Res, 1998, 58(17): 3942-3945.

52. Issa JP, Ottaviano YL, Celano P, et al. Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet, 1994, 7(4): 536-540.

53. Suzuki K, Suzuki I, Leodolter A, et al. Global DNA demethylation in gastrointestinal cancer is age dependent and precedes genomic damage. Cancer Cell, 2006, 9(3): 199-207.

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Diagnostic Value of Aberrant Methylation of Genes in Stool for Colorectal Tumor: A Meta-Analysis

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1.	Center MM, Jemal A, Ward E. International trends in colorectal cancer incidence rates. Cancer Epidemiol Biomarkers Prev, 2009, 18(6): 1688-1694.
2.	Kohler BA, Ward E, Mccarthy BJ, et al. Annual report to the nation on the status of cancer, 1975-2007, featuring tumors of the brain and other nervous system. J Natl Cancer Inst, 2011, 103(9): 714-736.
3.	Jemal A, Siegel R, Xu J, et al. Cancer statistics, 2010. CA Cancer J Clin, 2010, 60(5): 277-300.
4.	中华医学会消化病学分会. 中国结直肠肿瘤筛查、早诊早治和综合预防共识意见. 胃肠病学, 2011, 16(11): 666-675.
5.	Gumaste VV. CT colonography can be an adjunct to optical colonoscopy in CRC screening. Dig Dis Sci, 2009, 54(2): 212-217.
6.	Chen WD, Han ZJ, Skoletsky J, et al. Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. Journal of the National Cancer Institute, 2005, 97(15): 1124-1132.
7.	Olson J, Whitney DH, Durkee K, et al. DNA stabilization is critical for maximizing performance of fecal DNA-based colorectal cancer tests. Diagnostic Molecular Pathology, 2005, 14(3): 183-191.
8.	Altekruse SF, Kosary CL, Krapcho M, et al. SEER Cancer Statistics Review 2009, 2009.
9.	Whiting P, Rutjes AW, Reitsma JB, et al. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodology, 2003, 3: 25.
10.	Ahlquist DA, Taylor WR, Mahoney DW, et al. The stool DNA test is more accurate than the plasma septin 9 test in detecting colorectal neoplasia. Clin Gastroenterol Hepatol, 2012, 10(3): 272-277.
11.	Bosch L, Oort FA, Neerincx M, et al. DNA methylation of phosphatase and actin regulator 3 detects colorectal cancer in stool and complements FIT. Cancer Prevention Research, 2012, 5(3): 464-472.
12.	Ahlquist DA, Zou HZ, Domanico M, et al. Next generation stool DNA test accurately detects colorectal cancer and large adenomas. Gastroenterology, 2012, 142(2): 248-256.
13.	Azuara D, Rodriguez-Moranta F, Biondo S, et al. Novel methylation panel for the early detection of colorectal tumors in stool DNA. Clin Colorectal Cancer, 2010, 9(3): 168-176.
14.	Tang D, Liu J, Wang DR, et al. Diagnostic and prognostic value of the methylation status of secreted frizzled-related protein 2 in colorectal cancer. Clin Invest Med, 2011, 34(2): E88-E95.
15.	Baek YH, Chang E, Kim YJ, et al. Stool methylation specific polymerase chain reaction assay for the detection of colorectal neoplasia in Korean patients. Dis Colon Rectum, 2009, 52(8): 1452-1463.
16.	Li M, Chen WD, Papadopoulos N, et al. Sensitive digital quantification of DNA methylation in clinical samples. Nat Biotechnol, 2009, 27(9): 858-863.
17.	Melotte V, Lentjes MH, Bosch SM, et al. N-Myc downstream-regulated gene 4 (NDRG4): a candidate tumor suppressor gene and potential biomarker for colorectal cancer. J Natl Cancer Inst, 2009, 101(13): 916-927.
18.	Ausch C, Kim YH, Tsuchiya KD, et al. Comparative analysis of PCR based biomarker assay methods for colorectal polyp detection from fecal DNA. Clinical Chemistry, 2009, 55(8): 1559-1563.
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