Stool DNA testing for cancer surveillance in inflammatory bowel disease: An early view

Therapeutic Advances in Gastroenterology

Volumn 6, Issue 5, 2013, Pages 371-380

  Kisiel, John B ^a   Ahlquist, David A ^a  

^a MAYO CLINIC   (United States)

Author keywords

colorectal neoplasms; DNA methylation; early detection of cancer; inflammatory bowel disease; stool DNA

Indexed keywords

CANCER EPIDEMIOLOGY; CARCINOGENESIS; COLONOSCOPY; COLORECTAL CANCER; DNA DETERMINATION; ENTERITIS; FECES ANALYSIS; HETEROZYGOSITY LOSS; HIGH RISK PATIENT; HUMAN; MEDICAL TECHNOLOGY; PRIORITY JOURNAL; RECEIVER OPERATING CHARACTERISTIC; REVIEW; SENSITIVITY AND SPECIFICITY;

EID: 84883428731     PISSN: 1756283X     EISSN: 17562648     Source Type: Journal    
DOI: 10.1177/1756283X13487941     Document Type: Article

References (77)

1. Ahlquist D. Sargent D. Loprinzi C. Levin T. Rex D. Ahnen D. et al. (2008) Stool DNA and occult blood testing for screen detection of colorectal neoplasia. Ann Intern Med 149: 441–450, W481.
2. Ahlquist D. Taylor W. Mahoney D. Zou H. Domanico M. Thibodeau S. et al. (2012 a) The stool DNA test is more accurate than the plasma septin 9 test in detecting colorectal neoplasia. Clin Gastroenterol Hepatol 10: 272–277.
3. Ahlquist D. Zou H. Domanico M. Mahoney D. Yab T. Taylor W. et al. (2012 b) Next-generation stool DNA test accurately detects colorectal cancer and large adenomas. Gastroenterology 142: 248–256.
4. Berg M. Soreide K. (2012) EGFR and downstream genetic alterations in Kras/Braf and Pi3k/Akt pathways in colorectal cancer: implications for targeted therapy. Discovery Med 14: 207–214.
5. Bergquist A. Ekbom A. Olsson R. Kornfeldt D. Loof L. Danielsson A. et al. (2002) Hepatic and extrahepatic malignancies in primary sclerosing cholangitis. J Hepatol 36: 321–327.
6. Bista R. Brentnall T. Bronner M. Langmead C. Brand R. Liu Y. (2011) Using optical markers of nondysplastic rectal epithelial cells to identify patients with ulcerative colitis-associated neoplasia. Inflammatory Bowel Dis 17: 2427–2435.
7. Blackstone M. Riddell R. Rogers B. Levin B. (1981) Dysplasia-associated lesion or mass (Dalm) detected by colonoscopy in long-standing ulcerative colitis: an indication for colectomy. Gastroenterology 80: 366–374.
8. Brentnall T. Crispin D. Rabinovitch P. Haggitt R. Rubin C. Stevens A. et al. (1994) Mutations in the P 53 gene: an early marker of neoplastic progression in ulcerative colitis. Gastroenterology 107: 369–378.
9. Burmer G. Rabinovitch P. Haggitt R. Crispin D. Brentnall T. Kolli V. et al. (1992) Neoplastic progression in ulcerative colitis: histology, DNA content, and loss of a P 53 Allele. Gastroenterology 103: 1602–1610.
10. Cairns S. Scholefield J. Steele R. Dunlop M. Thomas H. Evans G. et al. (2010) Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 59: 666–689.
11. Choi P. Nugent F. Schoetz D. Jr. Silverman M. Haggitt R. (1993) Colonoscopic surveillance reduces mortality from colorectal cancer in ulcerative colitis. Gastroenterology 105: 418–424.
12. Collins P. Mpofu C. Watson A. Rhodes J. (2006) Strategies for detecting colon cancer and/or dysplasia in patients with inflammatory bowel Disease. Cochrane Database Syst Rev: CD000279.
13. Connell W. Lennard-Jones J. Williams C. Talbot I. Price A. Wilkinson K. (1994) Factors affecting the outcome of endoscopic surveillance for cancer in ulcerative colitis. Gastroenterology 107: 934–944.
14. Delco F. Sonnenberg A. (2000) A decision analysis of surveillance for colorectal cancer in ulcerative colitis. Gut 46: 500–506.
15. Eaden J. Abrams K. Mayberry J. (2001) The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48: 526–535.
16. Farraye F. Odze R. Eaden J. Itzkowitz S. (2010) Aga technical review on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease. Gastroenterology 138: 746–774, e741–744; quiz e712–743.
17. Fearon E. Hamilton S. Vogelstein B. (1987) Clonal analysis of human colorectal tumors. Science 238: 193–197.
18. Fearon E. Vogelstein B. (1990) A genetic model for colorectal tumorigenesis. Cell 61: 759–767.
19. Finlay C. Hinds P. Levine A. (1989) The P 53 Proto-oncogene can act as a suppressor of transformation. Cell 57: 1083–1093.
20. Fogt F. Vortmeyer A. Goldman H. Giordano T. Merino M. Zhuang Z. (1998) Comparison of genetic alterations in colonic adenoma and ulcerative colitis-associated dysplasia and carcinoma. Hum Pathol 29: 131–136.
21. Gardiner-Garden M. Frommer M. (1987) Cpg islands in vertebrate genomes. J Mol Biol 196: 261–282.
22. Garrity-Park M. Loftus E. Jr. Sandborn W. Bryant S. Smyrk T. (2010) Methylation status of genes in non-neoplastic mucosa from patients with ulcerative colitis-associated colorectal cancer. Am J Gastroenterol 105: 1610–1619.
23. Goel A. Boland C. (2012) Epigenetics of colorectal cancer. Gastroenterology 143: 1442–1460, e1441.
24. Graff J. Herman J. Myohanen S. Baylin S. Vertino P. (1997) Mapping patterns of cpg island methylation in normal and neoplastic cells implicates both upstream and downstream regions in de novo methylation. J Biol Chem 272: 22322–22329.
25. Herman J. Umar A. Polyak K. Graff J. Ahuja N. Issa J. et al. (1998) Incidence and functional consequences of Hmlh 1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci U S A 95: 6870–6875.
26. Herrinton L. Liu L. Levin T. Allison J. Lewis J. Velayos F. (2012) Incidence and mortality of colorectal adenocarcinoma in persons with inflammatory bowel disease from 1998 to 2010. Gastroenterology 143: 382–389.
27. Issa J. Ahuja N. Toyota M. Bronner M. Brentnall T. (2001) Accelerated age-related Cpg island methylation in ulcerative colitis. Cancer Res 61: 3573–3577.
28. Itzkowitz S. Harpaz N. (2004) Diagnosis and management of dysplasia in patients with inflammatory bowel diseases. Gastroenterology 126: 1634–1648.
29. Jess T. Rungoe C. Peyrin-Biroulet L. (2012 a) Risk of colorectal cancer in patients with ulcerative colitis: a meta-analysis of population-based cohort studies. Clin Gastroenterol Hepatol 10: 639–645.
30. Jess T. Simonsen J. Jorgensen K. Pedersen B. Nielsen N. Frisch M. (2012 b) Decreasing risk of colorectal cancer in patients with inflammatory bowel disease over 30 years. Gastroenterology 143: 375–381, e371.
31. Jonsson B. Ahsgren L. Andersson L. Stenling R. Rutegard J. (1994) Colorectal cancer surveillance in patients with ulcerative colitis. Br J Surg 81: 689–691.
32. Karlen P. Kornfeld D. Brostrom O. Lofberg R. Persson P. Ekbom A. (1998) Is colonoscopic surveillance reducing colorectal cancer mortality in ulcerative colitis? A population based case control study. Gut 42: 711–714.
33. Kisiel J. Garrity-Park M. Taylor W. Smyrk T. Ahlquist D. (2011) Methylated Eya 4 gene in non-neoplastic mucosa of ulcerative colitis patients with colorectal cancer: evidence for a field effect. Gastroenterology 140: S348–S349.
34. Kisiel J. Loftus E. Jr. Harmsen W. Zinsmeister A. Sandborn W. (2012 a) Outcome of sporadic adenomas and adenoma-like dysplasia in patients with ulcerative colitis undergoing polypectomy. Inflammatory Bowel Dis 18: 226–235.
35. Kisiel J. Yab T. Nazer Hussain F. Taylor W. Garrity-Park M. Sandborn W. et al. (2013) Stool DNA testing for the detection of colorectal neoplasia in patients with inflammatory bowel disease. Aliment Pharmacol Ther 37: 546–554.
36. Kisiel J. Yab T. Simonson J. Devens M. Mahoney D. Ahlquist D. (2012 b) Su 1903 methylated gene markers in stool before and after colorectal cancer resection: biologic implications for surveillance. Gastroenterology 142: S531–S532.
37. Kisiel J. Yab T. Taylor W. Chari S. Petersen G. Mahoney D. et al. (2012 c) Stool DNA testing for the detection of pancreatic cancer: assessment of methylation marker candidates. Cancer 118: 2623–2631.
38. Lashner B. Bauer W. Rybicki L. Goldblum J. (2003) Abnormal P 53 immunohistochemistry is associated with an increased colorectal cancer-related mortality in patients with ulcerative colitis. Am J Gastroenterol 98: 1423–1427.
39. Lashner B. Kane S. Hanauer S. (1990) Colon cancer surveillance in chronic ulcerative colitis: historical cohort study. Am J Gastroenterol 85: 1083–1087.
40. Levin B. Lieberman D. Mcfarland B. Andrews K. Brooks D. Bond J. et al. (2008) 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 Ccancer, and the American College of Radiology. Gastroenterology 134: 1570–1595.
41. Lidgard G. Domanico M. Bruinsma J. Gagrat Z. Oldham-Haltom R. Fourrier K. et al. (2012 a) Tu1189, an optimized multi-marker stool test for colorectal cancer screening: initial clinical appraisal. Gastroenterology 142: S770.
42. Lidgard G. Domanico M. Bruinsma J. Light J. Gagrat Z. Oldham-Haltom R. et al. (2012 b) An optimized molecular stool test for colorectal cancer screening: evaluation of an automated analytic platform and logistic algorithm. Cancer Research 2012; 72(8, supplement 1).
43. Lim C. Dixon M. Vail A. Forman D. Lynch D. Axon A. (2003) Ten year follow up of ulcerative colitis patients with and without low grade dysplasia. Gut 52: 1127–1132.
44. Macdermott R. (1985) Review of clinical aspects of cancer of the colon in patients with ulcerative colitis. Dig Dis Sci 30: 114S–118S.
45. Miyakura Y. Sugano K. Konishi F. Ichikawa A. Maekawa M. Shitoh K. et al. (2001) Extensive methylation of Hmlh 1 promoter region predominates in proximal colon cancer with microsatellite instability. Gastroenterology 121: 1300–1309.
46. Moinova H. Leidner R. Ravi L. Lutterbaugh J. Barnholtz-Sloan J. Chen Y. et al. (2012) Aberrant vimentin methylation is characteristic of upper gastrointestinal pathologies. Cancer Epidemiol, Biomarkers Prev 21: 594–600.
47. National Institute for Health and Clinical Excellence (NICE) (2011) Colonoscopic surveillance for prevention of colorectal cancer in people with ulcerative colitis, Crohn's disease or adenomas. London: National Institute for Health and Clinical Excellence.
48. Nuako K. Ahlquist D. Mahoney D. Schaid D. Siems D. Lindor N. (1998) Familial predisposition for colorectal cancer in chronic ulcerative colitis: a case-control study. Gastroenterology 115: 1079–1083.
49. Nugent F. Haggitt R. Gilpin P. (1991) Cancer surveillance in ulcerative colitis. Gastroenterology 100: 1241–1248.
50. Odze R. Brown C. Hartmann C. Noffsinger A. Fogt F. (2000) Genetic alterations in chronic ulcerative colitis-associated adenoma-like dalms are similar to non-colitic sporadic adenomas. Am J Surg Pathol 24: 1209–1216.
51. Odze R. Farraye F. Hecht J. Hornick J. (2004) Long-term follow-up after polypectomy treatment for adenoma-like dysplastic lesions in ulcerative colitis. Clin Gastroenterol Hepatol 2: 534–541.
52. Olson J. Whitney D. Durkee K. Shuber A. (2005) DNA stabilization is critical for maximizing performance of fecal dna-based colorectal cancer tests. Diagn Mol Pathol 14: 183–191.
53. Osborn N. Zou H. Molina J. Lesche R. Lewin J. Lofton-Day C. et al. (2006) Aberrant methylation of the eyes absent 4 gene in ulcerative colitis-associated dysplasia. Clin Gastroenterol Hepatol 4: 212–218.
54. Pedersen N. Duricova D. Elkjaer M. Gamborg M. Munkholm P. Jess T. (2010) Risk of extra-intestinal cancer in inflammatory bowel disease: meta-analysis of population-based cohort studies. Am J Gastroenterol 105: 1480–1487.
55. Provenzale D. Wong J. Onken J. Lipscomb J. (1998) Performing a cost-effectiveness analysis: surveillance of patients with ulcerative colitis. Am J Gastroenterol 93: 872–880.
56. Rex D. Johnson D. Anderson J. Schoenfeld P. Burke C. Inadomi J. (2009) American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected]. Am J Gastroenterol 104: 739–750.
57. Risques R. Lai L. Himmetoglu C. Ebaee A. Li L. Feng Z. et al. (2011) Ulcerative colitis-associated colorectal cancer arises in a field of short telomeres, senescence, and inflammation. Cancer Res 71: 1669–1679.
58. Rubenstein J. Waljee A. Jeter J. Velayos F. Ladabaum U. Higgins P. (2009) Cost effectiveness of ulcerative colitis surveillance in the setting of 5-aminosalicylates. Am J Gastroenterol 104: 2222–2232.
59. Rubin P. Friedman S. Harpaz N. Goldstein E. Weiser J. Schiller J. et al. (1999) Colonoscopic polypectomy in chronic colitis: conservative management after endoscopic resection of dysplastic polyps. Gastroenterology 117: 1295–1300.
60. Sonnenberg A. Delco F. Inadomi J. (2000) Cost-effectiveness of colonoscopy in screening for colorectal cancer. Ann Intern Med 133: 573–584.
61. Subramanian V. Mannath J. Ragunath K. Hawkey C. (2011) Meta-analysis: the diagnostic yield of chromoendoscopy for detecting dysplasia in patients with colonic inflammatory bowel disease. Aliment Pharmacol Ther 33: 304–312.
62. Suehiro Y. Wong C. Chirieac L. Kondo Y. Shen L. Webb C. et al. (2008) Epigenetic-genetic interactions in the Apc/Wnt, Ras/Raf, and P 53 pathways in colorectal carcinoma. Clin Cancer Res 14: 2560–2569.
63. Syngal S. Stoffel E. Chung D. Willett C. Schoetz D. Schroy P. et al. (2006) Detection of stool DNA mutations before and after treatment of colorectal neoplasia. Cancer 106: 277–283.
64. Thomas T. Abrams K. Robinson R. Mayberry J. (2007) Meta-analysis: cancer risk of low-grade dysplasia in chronic ulcerative colitis. Aliment Pharmacol Ther 25: 657–668.
65. Toruner M. Harewood G. Loftus E. Jr. Sandborn W. Tremaine W. Faubion W. et al. (2005) Endoscopic factors in the diagnosis of colorectal dysplasia in chronic inflammatory bowel disease. Inflamm Bowel Dis 11: 428–434.
66. Toyota M. Ahuja N. Ohe-Toyota M. Herman J. Baylin S. Issa J. (1999) Cpg island methylator phenotype in colorectal cancer. Proc Natl Acad Sci U S A 96: 8681–8686.
67. Velayos F. Liu L. Lewis J. Allison J. Flowers N. Hutfless S. et al. (2010) Prevalence of colorectal cancer surveillance for ulcerative colitis in an integrated health care delivery system. Gastroenterology 139: 1511–1518.
68. Vienne A. Simon T. Cosnes J. Baudry C. Bouhnik Y. Soule J. et al. (2011) Low prevalence of colonoscopic surveillance of inflammatory bowel disease patients with longstanding extensive colitis: a clinical practice survey nested in the cesame cohort. Aliment Pharmacol Ther 34: 188–195.
69. Vogelstein B. Fearon E. Hamilton S. Kern S. Preisinger A. Leppert M. et al. (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319: 525–532.
70. Walsh S. Loda M. Torres C. Antonioli D. Odze R. (1999) P 53 and beta catenin expression in chronic ulcerative colitis–associated polypoid dysplasia and sporadic adenomas: an immunohistochemical study. Am J Surg Pathol 23: 963–969.
71. Yang Wu D. Yab T. Taylor W. Mahoney D. Kisiel J. Devens M. et al. (2011) Aberrant gene methylation in the neoplastic progression of barrett's esophagus: identification of candidate diagnostic markers. Gastroenterology 140: S222.
72. Xie J. Itzkowitz S. (2008) Cancer in inflammatory bowel disease. World J Gastroenterol 14: 378–389.
73. Zou H. Allawi H. Cao X. Domanico M. Harrington J. Taylor W. et al. (2010) Sensitive quantification of vimentin methylation with a novel methylation specific q Invader Technology. Clinical Chemistry 56(6S): A199.
74. Zou H. Harrington J. Klatt K. Ahlquist D. (2006) A Sensitive Method to quantify human long dna in stool: relevance to colorectal cancer screening. Cancer Epidemiol Biomarkers Prev 15: 1115–1119.
75. Zou H. Osborn N. Harrington J. Klatt K. Molina J. Burgart L. et al. (2005) Frequent methylation of eyes absent 4 gene in Barrett's esophagus and esophageal adenocarcinoma. Cancer Epidemiol Biomarkers Prev 14: 830–834.
76. Zou H. Taylor W. Harrington J. Devens M. Simonson J. Ahlquist D. (2008) A Sensitive method to scan gene mutations in stool: relevance to detection of gastrointestinal neoplasia. Gastroenterology 134: A484.
77. Zou H. Taylor W. Harrington J. Hussain F. Cao X. Loprinzi C. et al. (2009) High detection rates of colorectal neoplasia by stool DNA testing with a novel digital melt curve assay. Gastroenterology 136: 459–470.