Serrated neoplasia of the colon: What do we really know?

Current Gastroenterology Reports

Volumn 16, Issue 4, 2014, Pages

  Haque, Tanvir ^a   Greene, Kevin G ^a   Crockett, Seth D ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Colonoscopy; Endoscopy; Epidemiology; Hyperplastic polyp; Natural history; Serrated pathway; Sessile serrated adenoma; Sessile serrated polyp; Traditional serrated adenoma

Indexed keywords

ARTICLE; CANCER RESEARCH; CLINICAL FEATURE; COLON ADENOMA; COLON POLYP; COLONOSCOPY; COLORECTAL CANCER; DISEASE SURVEILLANCE; HISTOPATHOLOGY; HISTORY; HUMAN; HYPERPLASTIC POLYP; MASS SCREENING; MOLECULAR BIOLOGY; POLYP; PRACTICE GUIDELINE; RECTUM ADENOMA; SERRATED POLYPOSIS SYNDROME; TRADITIONAL SERRATED ADENOMA; ADENOMA; COLON TUMOR; EARLY DIAGNOSIS; GENETICS; HYPERPLASIA; PATHOLOGY; PRECANCER; REVIEW;

ADENOMA; COLONIC NEOPLASMS; COLONIC POLYPS; COLONOSCOPY; EARLY DETECTION OF CANCER; HUMANS; HYPERPLASIA; PRACTICE GUIDELINES AS TOPIC; PRECANCEROUS CONDITIONS;

EID: 84894634008     PISSN: 15228037     EISSN: 1534312X     Source Type: Journal    
DOI: 10.1007/s11894-014-0380-6     Document Type: Article

References (96)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63(1):11-30.
2. Nishihara R, Wu K, Lochhead P, Morikawa T, Liao X, Qian ZR, et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med. 2013;369(12):1095-105.
3. Zauber AG, Winawer SJ, O'Brien MJ, Lansdorp-Vogelaar I, van Ballegooijen M, Hankey BF, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med. 2012;366(8):687-96.
4. Rex DK, Johnson DA, Anderson JC, Schoenfeld PS, Burke CA, Inadomi JM. American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected]. Am J Gastroenterol. 2009;104(3):739-50.
5. Farrar WD, Sawhney MS, Nelson DB, Lederle FA, Bond JH. Colorectal cancers found after a complete colonoscopy. Clin Gastroenterol Hepatol. 2006;4(10):1259-64.
6. Khalid O, Radaideh S, Cummings OW, O'Brien MJ, Goldblum JR, Rex DK. Reinterpretation of histology of proximal colon polyps called hyperplastic in 2001. World J Gastroenterol. 2009;15(30):3767-70.
7. Snover DC, Jass JR, Fenoglio-Preiser C, Batts KP. Serrated polyps of the large intestine: a morphologic and molecular review of an evolving concept. Am J Clin Pathol. 2005;124(3):380-91.
8. Leggett B, Whitehall V. Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology. 2010;138(6):2088-100.
9. Huang CS, Farraye FA, Yang S, O'Brien MJ. The clinical significance of serrated polyps. Am J Gastroenterol. 2011;106(2):229-40. quiz 41.
10. Snover DC. Update on the serrated pathway to colorectal carcinoma. Hum Pathol. 2011;42(1):1-10. This paper provides an excellent and comprehensive overview of serrated neoplasia, written by Dr. Dale Snover, a pathologist and international expert in the field.
11. Jass JR. Serrated adenoma of the colorectum and the DNA-methylator phenotype. Nature Clin Pract Oncol. 2005;2(8):398-405.
12. Rex DK, Ahnen DJ, Baron JA, Batts KP, Burke CA, Burt RW et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol. 2012;107(9):1315-29; quiz 4, 30. This is the recently published Expert Consensus Panel report that provides detailed surveillance guidelines for serrated polyps, as well as a comprehensive review of relevant evidence.
13. Longacre TA, Fenoglio-Preiser CM. Mixed hyperplastic adenomatous polyps/serrated adenomas. A distinct form of colorectal neoplasia. Am J Surg Pathol. 1990;14(6):524-37.
14. Torlakovic E, Snover DC. Serrated adenomatous polyposis in humans. Gastroenterology. 1996;110(3):748-55.
15. Torlakovic E, Skovlund E, Snover DC, Torlakovic G, Nesland JM. Morphologic reappraisal of serrated colorectal polyps. Am J Surg Pathol. 2003;27(1):65-81.
16. Torlakovic EE, Gomez JD, Driman DK, Parfitt JR, Wang C, Benerjee T, et al. Sessile serrated adenoma (SSA) vs. traditional serrated adenoma (TSA). Am J Surg Pathol. 2008;32(1):21-9. This report provides a comprehensive overview of the distinguishing pathologic features of TSAs and SSAs.
17. Snover D. Serrated adenomas. Am J Clin Pathol. 2005;124(4):611-2. author reply 2-5.
18. Bosman FTCF, Hruban RH, et al. WHO classification of tumours pathology and genetics tumours of the digestive system. 4th ed. Berlin: Springer-Verlag; 2010.
19. Weston AP, Campbell DR. Diminutive colonic polyps: histopathology, spatial distribution, concomitant significant lesions, and treatment complications. Am J Gastroenterol. 1995;90(1):24-8.
20. Lieberman DA, Prindiville S, Weiss DG, Willett W. Risk factors for advanced colonic neoplasia and hyperplastic polyps in asymptomatic individuals. JAMA. 2003;290(22):2959-67.
21. Sweetser S, Smyrk TC, Sinicrope FA. Serrated colon polyps as precursors to colorectal cancer. Clin Gastroenterol Hepatol. 2013;11(7):760-7. quiz e54-5.
22. Groff RJ, Nash R, Ahnen DJ. Significance of serrated polyps of the colon. Curr Gastroenterol Rep. 2008;10(5):490-8.
23. Lash RH, Genta RM, Schuler CM. Sessile serrated adenomas: prevalence of dysplasia and carcinoma in 2139 patients. J Clin Pathol. 2010;63(8):681-6. This report is the largest cross-sectional study of SSAs and TSAs yet published.
24. Higuchi T, Sugihara K, Jass JR. Demographic and pathological characteristics of serrated polyps of colorectum. Histopathology. 2005;47(1):32-40.
25. Fu Z, Shrubsole MJ, Smalley WE, Wu H, Chen Z, Shyr Y, et al. Lifestyle factors and their combined impact on the risk of colorectal polyps. Am J Epidemiol. 2012;176(9):766-76.
26. Carr NJ, Mahajan H, Tan KL, Hawkins NJ, Ward RL. Serrated and non-serrated polyps of the colorectum: their prevalence in an unselected case series and correlation of BRAF mutation analysis with the diagnosis of sessile serrated adenoma. J Clin Pathol. 2009;62(6):516-8.
27. Li SC, Burgart L. Histopathology of serrated adenoma, its variants, and differentiation from conventional adenomatous and hyperplastic polyps. Arch Pathol Lab Med. 2007;131(3):440-5.
28. Ha SY, Lee SM, Lee EJ, Kang SY, Jang KT, Park CK, et al. Filiform serrated adenoma is an unusual, less aggressive variant of traditional serrated adenoma. Pathology. 2012;44(1):18-23.
29. Yantiss RK, Oh KY, Chen YT, Redston M, Odze RD. Filiform serrated adenomas: a clinicopathologic and immunophenotypic study of 18 cases. Am J Surg Pathol. 2007;31(8):1238-45.
30. Boparai KS, Mathus-Vliegen EM, Koornstra JJ, Nagengast FM, van Leerdam M, van Noesel CJ, et al. Increased colorectal cancer risk during follow-up in patients with hyperplastic polyposis syndrome: a multicentre cohort study. Gut. 2010;59(8):1094-100.
31. Edelstein DL, Axilbund JE, Hylind LM, Romans K, Griffin CA, Cruz-Correa M, et al. Serrated polyposis: rapid and relentless development of colorectal neoplasia. Gut. 2013;62(3):404-8.
32. Bengoechea O, Martinez-Penuela JM, Larrinaga B, Valerdi J, Borda F. Hyperplastic polyposis of the colorectum and adenocarcinoma in a 24-year-old man. Am J Surg Pathol. 1987;11(4):323-7.
33. Guarinos C, Sanchez-Fortun C, Rodriguez-Soler M, Alenda C, Paya A, Jover R. Serrated polyposis syndrome: molecular, pathological and clinical aspects. World J Gastroenterol. 2012;18(20):2452-61.
34. Spring KJ, Zhao ZZ, Karamatic R, Walsh MD, Whitehall VL, Pike T, et al. High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy. Gastroenterology. 2006;131(5):1400-7.
35. Williams AR, Balasooriya BA, Day DW. Polyps and cancer of the large bowel: a necropsy study in Liverpool. Gut. 1982;23(10):835-42.
36. Min YW, Lee JH, Lee SH, Park DI, Han DS, Rhee PL, et al. Prevalence of proximal colon serrated polyps in a population at average risk undergoing screening colonoscopy: a multicenter study. Clin Res Hepatol Gastroenterol. 2012;36(6):604-8.
37. Hetzel JT, Huang CS, Coukos JA, Omstead K, Cerda SR, Yang S, et al. Variation in the detection of serrated polyps in an average risk colorectal cancer screening cohort. Am J Gastroenterol. 2010;105(12):2656-64. This paper describes the wide variation in both endoscopic detection and pathologic interpretation of serrated polyps.
38. Buda A, De Bona M, Dotti I, Piselli P, Zabeo E, Barbazza R, et al. Prevalence of different subtypes of serrated polyps and risk of synchronous advanced colorectal neoplasia in average-risk population undergoing first-time colonoscopy. Clin Transl Gastroenterol. 2012;3:e6.
39. Kumbhari V, Behary J, Hui JM. Prevalence of adenomas and sessile serrated adenomas in Chinese compared with Caucasians. J Gastroenterol Hepatol. 2013;28(4):608-12.
40. Martinez ME, McPherson RS, Levin B, Glober GA. A case-control study of dietary intake and other lifestyle risk factors for hyperplastic polyps. Gastroenterology. 1997;113(2):423-9.
41. Erhardt JG, Kreichgauer HP, Meisner C, Bode JC, Bode C. Alcohol, cigarette smoking, dietary factors and the risk of colorectal adenomas and hyperplastic polyps-a case control study. Eur J Nutr. 2002;41(1):35-43.
42. Ji B-T, Weissfeld JL, Chow W-H, Huang W-Y, Schoen RE, Hayes RB. Tobacco smoking and colorectal hyperplastic and adenomatous polyps. Cancer Epidemiol Biomark Prev: Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol. 2006;15(5):897-901.
43. Kearney J, Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, et al. Diet, alcohol, and smoking and the occurrence of hyperplastic polyps of the colon and rectum (United States). Cancer Causes Control. 1995;6(1):45-56.
44. Morimoto LM, Newcomb PA, Ulrich CM, Bostick RM, Lais CJ, Potter JD. Risk factors for hyperplastic and adenomatous polyps: evidence for malignant potential? Cancer Epidemiol Biomark Prev: Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol. 2002;11(10 Pt 1):1012-8.
45. Omata F, Brown WR, Tokuda Y, Takahashi O, Fukui T, Ueno F, et al. Modifiable risk factors for colorectal neoplasms and hyperplastic polyps. Intern Med. 2009;48(3):123-8.
46. Shrubsole MJ, Wu H, Ness RM, Shyr Y, Smalley WE, Zheng W. Alcohol drinking, cigarette smoking, and risk of colorectal adenomatous and hyperplastic polyps. Am J Epidemiol. 2008;167(9):1050-8.
47. Anderson JC, Rangasamy P, Rustagi T, Myers M, Sanders M, Vaziri H, et al. Risk factors for sessile serrated adenomas. J Clin Gastroenterol. 2011;45(8):694-9.
48. Burnett-Hartman AN, Passarelli MN, Adams SV, Upton MP, Zhu LC, Potter JD, et al. Differences in epidemiologic risk factors for colorectal adenomas and serrated polyps by lesion severity and anatomical site. Am J Epidemiol. 2013;177(7):625-37.
49. Yang S, Farraye FA, Mack C, Posnik O, O'Brien MJ. BRAF and KRAS Mutations in hyperplastic polyps and serrated adenomas of the colorectum: relationship to histology and CpG island methylation status. Am J Surg Pathol. 2004;28(11):1452-9.
50. O'Brien MJ, Yang S, Mack C, Xu H, Huang CS, Mulcahy E, et al. Comparison of microsatellite instability, CpG island methylation phenotype, BRAF and KRAS status in serrated polyps and traditional adenomas indicates separate pathways to distinct colorectal carcinoma end points. Am J Surg Pathol. 2006;30(12):1491-501.
51. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet. 2006;38(7):787-93.
52. Kambara T, Simms LA, Whitehall VL, Spring KJ, Wynter CV, Walsh MD, et al. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut. 2004;53(8):1137-44.
53. Gupta AK, Pretlow TP, Schoen RE. Aberrant crypt foci: what we know and what we need to know. Clin Gastroenterol Hepatol. 2007;5(5):526-33.
54. Rosenberg DW, Yang S, Pleau DC, Greenspan EJ, Stevens RG, Rajan TV, et al. Mutations in BRAF and KRAS differentially distinguish serrated versus non-serrated hyperplastic aberrant crypt foci in humans. Cancer Res. 2007;67(8):3551-4.
55. Fu B, Yachida S, Morgan R, Zhong Y, Montgomery EA, Iacobuzio-Donahue CA. Clinicopathologic and genetic characterization of traditional serrated adenomas of the colon. Am J Clin Pathol. 2012;138(3):356-66.
56. Kim KM, Lee EJ, Kim YH, Chang DK, Odze RD. KRAS mutations in traditional serrated adenomas from Korea herald an aggressive phenotype. Am J Surg Pathol. 2010;34(5):667-75.
57. Patil DT, Shadrach BL, Rybicki LA, Leach BH, Pai RK. Proximal colon cancers and the serrated pathway: a systematic analysis of precursor histology and BRAF mutation status. Mod Pathol. 2012;25(10):1423-31.
58. Makinen MJ, George SM, Jernvall P, Makela J, Vihko P, Karttunen TJ. Colorectal carcinoma associated with serrated adenoma-prevalence, histological features, and prognosis. J Pathol. 2001;193(3):286-94.
59. Goldstein NS. Small colonic microsatellite unstable adenocarcinomas and high-grade epithelial dysplasias in sessile serrated adenoma polypectomy specimens: a study of eight cases. Am J Clin Pathol. 2006;125(1):132-45.
60. Garcia-Solano J, Perez-Guillermo M, Conesa-Zamora P, Acosta-Ortega J, Trujillo-Santos J, Cerezuela-Fuentes P, et al. Clinicopathologic study of 85 colorectal serrated adenocarcinomas: further insights into the full recognition of a new subset of colorectal carcinoma. Hum Pathol. 2010;41(10):1359-68.
61. Tonooka T, Sano Y, Fujii T, Kato S, Yoshino T, Fu KI, et al. Adenocarcinoma in solitary large hyperplastic polyp diagnosed by magnifying colonoscope: report of a case. Dis Colon Rectum. 2002;45(10):1407-11.
62. Cooper HS, Patchefsky AS, Marks G. Adenomatous and carcinomatous changes within hyperplastic colonic epithelium. Dis Colon Rectum. 1979;22(3):152-6.
63. Sheridan TB, Fenton H, Lewin MR, Burkart AL, Iacobuzio-Donahue CA, Frankel WL, et al. Sessile serrated adenomas with low- and high-grade dysplasia and early carcinomas: an immunohistochemical study of serrated lesions "caught in the act". Am J Clin Pathol. 2006;126(4):564-71.
64. O'Brien MJ, Yang S, Clebanoff JL, Mulcahy E, Farraye FA, Amorosino M, et al. Hyperplastic (serrated) polyps of the colorectum: relationship of CpG island methylator phenotype and K-ras mutation to location and histologic subtype. Am J Surg Pathol. 2004;28(4):423-34.
65. Lynch HT, Smyrk T, Jass JR. Hereditary nonpolyposis colorectal cancer and colonic adenomas: aggressive adenomas? Semin Surg Oncol. 1995;11(6):406-10.
66. Oono Y, Fu K, Nakamura H, Iriguchi Y, Yamamura A, Tomino Y, et al. Progression of a sessile serrated adenoma to an early invasive cancer within 8 months. Dig Dis Sci. 2009;54(4):906-9.
67. Yamauchi T, Watanabe M, Hasegawa H, Yamamoto S, Endo T, Kabeshima Y, et al. Serrated adenoma developing into advanced colon cancer in 2 years. J Gastroenterol. 2002;37(6):467-70.
68. Hiraoka S, Kato J, Fujiki S, Kaji E, Morikawa T, Murakami T, et al. The presence of large serrated polyps increases risk for colorectal cancer. Gastroenterology. 2010;139(5):1503-10. 10 e1-3.
69. Alvarez C, Andreu M, Castells A, Quintero E, Bujanda L, Cubiella J, et al. Relationship of colonoscopy-detected serrated polyps with synchronous advanced neoplasia in average-risk individuals. Gastrointest Endosc. 2013;78(2):333-41 e1.
70. Li D, Jin C, McCulloch C, Kakar S, Berger BM, Imperiale TF, et al. Association of large serrated polyps with synchronous advanced colorectal neoplasia. Am J Gastroenterol. 2009;104(3):695-702.
71. Schreiner MA, Weiss DG, Lieberman DA. Proximal and large hyperplastic and nondysplastic serrated polyps detected by colonoscopy are associated with neoplasia. Gastroenterology. 2010;139(5):1497-502. This paper describes the elevated risk of synchronous and metachronous neoplasia associated with proximal and large serrated polyps.
72. Vu HT, Lopez R, Bennett A, Burke CA. Individuals with sessile serrated polyps express an aggressive colorectal phenotype. Dis Colon Rectum. 2011;54(10):1216-23.
73. Snover DC. Sessile serrated adenoma/polyp of the large intestine: a potentially aggressive lesion in need of a new screening strategy. Dis Colon Rectum. 2011;54(10):1205-6.
74. Pai RK, Hart J, Noffsinger AE. Sessile serrated adenomas strongly predispose to synchronous serrated polyps in non-syndromic patients. Histopathology. 2010;56(5):581-8.
75. Goldstein NS, Bhanot P, Odish E, Hunter S. Hyperplastic-like colon polyps that preceded microsatellite-unstable adenocarcinomas. Am J Clin Pathol. 2003;119(6):778-96.
76. Teriaky A, Driman DK, Chande N. Outcomes of a 5-year follow-up of patients with sessile serrated adenomas. Scand J Gastroenterol. 2012;47(2):178-83.
77. Lu FI, van Niekerk DW, Owen D, Tha SPL, Turbin DA, Webber DL. Longitudinal outcome study of sessile serrated adenomas of the colorectum: an increased risk for subsequent right-sided colorectal carcinoma. Am J Surg Pathol. 2010;34(7):927-34.
78. Lazarus R, Junttila OE, Karttunen TJ, Makinen MJ. The risk of metachronous neoplasia in patients with serrated adenoma. Am J Clin Pathol. 2005;123(3):349-59.
79. Limketkai BN, Lam-Himlin D, Arnold CA, Arnold MA. The cutting edge of serrated polyps: a practical guide to approaching and managing serrated colon polyps. Gastrointest Endosc. 2013;77(3):360-75.
80. Tadepalli US, Feihel D, Miller KM, Itzkowitz SH, Freedman JS, Kornacki S, et al. A morphologic analysis of sessile serrated polyps observed during routine colonoscopy (with video). Gastrointest Endosc. 2011;74(6):1360-8.
81. Lambert R, Kudo SE, Vieth M, Allen JI, Fujii H, Fujii T, et al. Pragmatic classification of superficial neoplastic colorectal lesions. Gastrointest Endosc. 2009;70(6):1182-99.
82. Ishigooka S, Nomoto M, Obinata N, Oishi Y, Sato Y, Nakatsu S, et al. Evaluation of magnifying colonoscopy in the diagnosis of serrated polyps. World J Gastroenterol. 2012;18(32):4308-16.
83. Kahi CJ, Hewett DG, Norton DL, Eckert GJ, Rex DK. Prevalence and variable detection of proximal colon serrated polyps during screening colonoscopy. Clin Gastroenterol Hepatol. 2011;9(1):42-6.
84. de Wijkerslooth TR, Stoop EM, Bossuyt PM, Tytgat KM, Dees J, Mathus-Vliegen EM, et al. Differences in proximal serrated polyp detection among endoscopists are associated with variability in withdrawal time. Gastrointest Endosc. 2013;77(4):617-23.
85. Crockett SD, Snover DC, Ahnen DJ, Baron JA. Sessile Serrated Adenomas: An evidence-based guide to management. Clin Gastroenterol Hepatol. 2013.
86. East JE, Saunders BP, Jass JR. Sporadic and syndromic hyperplastic polyps and serrated adenomas of the colon: classification, molecular genetics, natural history, and clinical management. Gastroenterol Clin North Am. 2008;37(1):25-46. v.
87. Pohl H, Srivastava A, Bensen SP, Anderson P, Rothstein RI, Gordon SR, et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology. 2013;144(1):74-80 e1.
88. Glatz K, Pritt B, Glatz D, Hartmann A, O'Brien MJ, Blaszyk H. A multinational, internet-based assessment of observer variability in the diagnosis of serrated colorectal polyps. Am J Clin Pathol. 2007;127(6):938-45.
89. Farris AB, Misdraji J, Srivastava A, Muzikansky A, Deshpande V, Lauwers GY, et al. Sessile serrated adenoma: challenging discrimination from other serrated colonic polyps. Am J Surg Pathol. 2008;32(1):30-5.
90. Singh H, Bay D, Ip S, Bernstein CN, Nugent Z, Gheorghe R, et al. Pathological reassessment of hyperplastic colon polyps in a city-wide pathology practice: implications for polyp surveillance recommendations. Gastrointest Endosc. 2012;76(5):1003-8.
91. Lieberman DA, Rex DK, Winawer SJ, Giardiello FM, Johnson DA, Levin TR. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology. 2012;143(3):844-57.
92. Hoff G, Bretthauer M, Garborg K, Eide TJ. New polyps, old tricks: controversy about removing benign bowel lesions. Bmj. 2013;347:f5843.
93. Heldwein W, Dollhopf M, Rosch T, Meining A, Schmidtsdorff G, Hasford J, et al. The Munich Polypectomy Study (MUPS): prospective analysis of complications and risk factors in 4000 colonic snare polypectomies. Endoscopy. 2005;37(11):1116-22.
94. Nakao Y, Saito S, Ohya T, Aihara H, Arihiro S, Kato T, et al. Endoscopic features of colorectal serrated lesions using image-enhanced endoscopy with pathological analysis. Eur J Gastroenterol Hepatol. 2013;25(8):981-8.
95. Kutsukawa M, Kudo SE, Ikehara N, Ogawa Y, Wakamura K, Mori Y et al. Efficiency of endocytoscopy in differentiating types of serrated polyps. Gastrointest Endosc. 2013.
96. Lidgard GP, Domanico MJ, Bruinsma JJ, Light J, Gagrat ZD, Oldham-Haltom RL, et al. Clinical performance of an automated stool DNA assay for detection of colorectal neoplasia. Clin Gastroenterol Hepatol. 2013;11(10):1313-8.