Diagnostic Histopathology
Volume 14, Issue 2 , Pages 78-93 , February 2008

The serrated polyp pathway to colorectal carcinoma

References 

  1. Goldman H, Ming S, Hickock DF. Nature and significance of hyperplastic polyps of the human colon. Arch Pathol. 1970;89:349–354
  2. Jass JR. Relation between metaplastic polyp and carcinoma of the colorectum. Lancet. 1983;1:28–30
  3. Morson BC. Precancerous lesions of the colon and rectum: classification and controversial issues. JAMA. 1962;179:316–321
  4. Jass JR, Whitehall VL, Young J, Leggett BA. Emerging concepts in colorectal neoplasia. Gastroenterology. 2002;123:862–876
  5. Torlakovic E, Snover DC. Serrated adenomatous polyposis in humans. Gastroenterology. 1996;110:748–755
  6. Leggett BA, Devereaux B, Biden K, Searle J, Young J, Jass J. Hyperplastic polyposis: association with colorectal cancer. Am J Surg Pathol. 2001;25:177–184
  7. Jass JR. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology. 2007;50:113–130
  8. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics. CA Cancer J Clin. 2007;57:43–66
  9. Rosenberg DW, Yang S, Pleau DC, et al. Mutations in BRAF and KRAS differentially distinguish serrated versus non-serrated hyperplastic aberrant crypt foci in humans. Cancer Res. 2007;67:3551–3554
  10. O’Brien MJ, Yang S, Mack C, 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;30:1491–1501
  11. Powell SM, Zilz N, Beazer-Barclay Y, et al. APC mutations occur early during colorectal tumorigenesis. Nature. 1992;359:235–237
  12. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med. 2004;10:789–799
  13. Longacre TA, Fenoglio-Preiser CM. Mixed hyperplastic adenomatous polyps/serrated adenomas. A distinct form of colorectal neoplasia. Am J Surg Pathol. 1990;14:524–537
  14. Torlakovic E, Skovlund E, Snover DC, Torlakovic G, Nesland JM. Morphologic reappraisal of serrated colorectal polyps. Am J Surg Pathol. 2003;27:65–81
  15. Lee EJ, Choi C, Park CK, et al. Tracing origin of serrated adenomas with BRAF and KRAS mutations. Virchows Arch. 2005;447:597–602
  16. Dong SM, Lee EJ, Jeon ES, Park CK, Kim KM. Progressive methylation during the serrated neoplasia pathway of the colorectum. Mod Pathol. 2005;18:170–178
  17. 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;28:1452–1459
  18. O’Brien MJ, Yang S, Clebanoff JL, 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;28:423–434
  19. Jass JR, Baker K, Zlobec I, et al. Advanced colorectal polyps with the molecular and morphological features of serrated polyps and adenomas: concept of a ‘fusion’ pathway to colorectal cancer. Histopathology. 2006;49:121–131
  20. Kambara T, Simms LA, Whitehall VL, et al. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut. 2004;53:1137–1144
  21. Samowitz WS, Albertsen H, Sweeney C, et al. Association of smoking, CpG island methylator phenotype, and V600E BRAF mutations in colon cancer. J Natl Cancer Inst. 2006;98:1731–1738
  22. Young J, Jass JR. The case for a genetic predisposition to serrated neoplasia in the colorectum: hypothesis and review of the literature. Cancer Epidemiol Biomarkers Prev. 2006;15:1778–1784
  23. Kolch W. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. Biochem J. 2000;351:289–305
  24. Barradas M, Gonos ES, Zebedee Z, et al. Identification of a candidate tumor-suppressor gene specifically activated during Ras-induced senescence. Exp Cell Res. 2002;273:127–137
  25. Minoo P, Jass JR. Senescence and serration: a new twist to an old tale. J Pathol. 2006;210:137–140
  26. Mooi WJ, Peeper DS. Oncogene-induced cell senescence—halting on the road to cancer. N Engl J Med. 2006;355:1037–1046
  27. Michaloglou C, Vredeveld LC, Soengas MS, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature. 2005;436:720–724
  28. Kaye GI, Fenoglio CM, Pascal RR, Lane N. Comparative electron microscopic features of normal, hyperplastic, and adenomatous human colonic epithelium. Variations in cellular structure relative to the process of epithelial differentiation. Gastroenterology. 1973;64:926–945
  29. Hayashi T, Yatani R, Apostol J, Stemmermann GN. Pathogenesis of hyperplastic polyps of the colon: a hypothesis based on ultrastructure and in vitro cell kinetics. Gastroenterology. 1974;66:347–356
  30. Minoo P, Baker K, Goswami R, et al. Extensive DNA methylation in normal colorectal mucosa in hyperplastic polyposis. Gut. 2006;55:1467–1474
  31. Jones PA. Overview of cancer epigenetics. Semin Hematol. 2005;42:S3–S8
  32. Weisenberger DJ, Siegmund KD, Campan M, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet. 2006;38:787–793
  33. Issa JP. CpG island methylator phenotype in cancer. Nat Rev Cancer. 2004;4:988–993
  34. Park SJ, Rashid A, Lee JH, Kim SG, Hamilton SR, Wu TT. Frequent CpG island methylation in serrated adenomas of the colorectum. Am J Pathol. 2003;162:815–822
  35. Samowitz WS, Albertsen H, Herrick J, et al. Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer. Gastroenterology. 2005;129:837–845
  36. Chirieac LR, Shen L, Catalano PJ, Issa JP, Hamilton SR. Phenotype of microsatellite-stable colorectal carcinomas with CpG island methylation. Am J Surg Pathol. 2005;29:429–436
  37. Vogelstein B, Fearon ER, Hamilton SR, et al. Genetic alterations during colorectal-tumor development. N Engl J Med. 1988;319:525–532
  38. Fodde R, Kuipers J, Rosenberg C, et al. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol. 2001;3:433–438
  39. Rajagopalan H, Nowak MA, Vogelstein B, Lengauer C. The significance of unstable chromosomes in colorectal cancer. Nat Rev Cancer. 2003;3:695–701
  40. Abal M, Obrador-Hevia A, Janssen KP, et al. APC Inactivation associates with abnormal mitosis completion and concomitant BUB1B/MAD2L1 up-regulation. Gastroenterology. 2007;132:2448–2458
  41. Chan AO, Issa JP, Morris JS, Hamilton SR, Rashid A. Concordant CpG island methylation in hyperplastic polyposis. Am J Pathol. 2002;160:529–536
  42. Spring KJ, Zhao ZZ, Karamatic R, et al. High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy. Gastroenterology. 2006;131:1400–1407
  43. Anderson JC, Pollack BJ. Predicting of hyperplastic histology by endoscopic features. Gastrointest Endosc. 2000;52:149–150
  44. Rex DK, Rahmani EY. New endoscopic finding associated with hyperplastic polyps. Gastrointest Endosc. 1999;50:704–706
  45. Rothstein RD, Kochman M. Large hyperplastic polyps of the right colon. Gastrointest Endosc. 1998;47(2):211–212
  46. Langdon DE. Large hyperplastic polyps of the right colon. Gastrointest Endosc. 1998;48:659
  47. Higuchi T, Sugihara K, Jass JR. Demographic and pathological characteristics of serrated polyps of colorectum. Histopathology. 2005;47:32–40
  48. Goldstein NS. Morphologic features of high-grade serrated dysplasia in sessile serrated adenomas without co-existent invasive adenocarcinoma. Lab Invest. 3-3-2007;87(suppl 1):A115
  49. Baker K, Zhang Y, Jin C, Jass JR. Proximal versus distal hyperplastic polyps of the colorectum: different lesions or a biological spectrum?. J Clin Pathol. 2004;57:1089–1093
  50. 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;124:380–391
  51. Iwabuchi M, Sasano H, Hiwatashi N, et al. Serrated adenoma: a clinicopathological, DNA ploidy, and immunohistochemical study. Anticancer Res. 2000;20:1141–1147
  52. Huang CS, O’Brien MJ, Yang S, Farraye FA. Hyperplastic polyps, serrated adenomas, and the serrated polyp neoplasia pathway. Am J Gastroenterol. 2004;99:2242–2255
  53. Matsumoto T, Mizuno M, Shimizu M, Manabe T, Iida M. Clinicopathological features of serrated adenoma of the colorectum: comparison with traditional adenoma. J Clin Pathol. 1999;52:513–516
  54. Jaramillo E, Watanabe M, Slezak P, Rubio C. Flat neoplastic lesions of the colon and rectum detected by high-resolution video endoscopy and chromoscopy. Gastrointest Endosc. 1995;42:114–122
  55. 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;31:1238–1245
  56. Oka S, Tanaka S, Hiyama T, et al. Clinicopathologic and endoscopic features of colorectal serrated adenoma: differences between polypoid and superficial types. Gastrointest Endosc. 2004;59:213–219
  57. Robbins J, Yang S, Xu H, et al. Distinct spectrum of pathology is associated with KRAS mutation in the serrated polyp neoplasia pathway. Lab Invest. 2007;87:128A;[abstract #576]
  58. 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;125:132–145
  59. Chan TL, Zhao W, Leung SY, Yuen ST. BRAF and KRAS mutations in colorectal hyperplastic polyps and serrated adenomas. Cancer Res. 2003;63:4878–4881
  60. Sawyer EJ, Cerar A, Hanby AM, et al. Molecular characteristics of serrated adenomas of the colorectum. Gut. 2002;51:200–206
  61. Maltzman T, Knoll K, Martinez ME, et al. Ki-ras proto-oncogene mutations in sporadic colorectal adenomas: relationship to histologic and clinical characteristics. Gastroenterology. 2001;121:302–309
  62. Jass JR, Smith M. Sialic acid and epithelial differentiation in colorectal polyps and cancer—a morphological, mucin and lectin histochemical study. Pathology. 1992;24:233–242
  63. Tuppurainen K, Makinen JM, Junttila O, et al. Morphology and microsatellite instability in sporadic serrated and non-serrated colorectal cancer. J Pathol. 2005;207:285–294
  64. 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;193:286–294
  65. Young J, Simms LA, Biden KG, et al. Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis. Am J Pathol. 2001;159:2107–2116
  66. Makinen MJ. Colorectal serrated adenocarcinoma. Histopathology. 2007;50:131–150
  67. Hinoi T, Tani M, Lucas PC, et al. Loss of CDX2 expression and microsatellite instability are prominent features of large cell minimally differentiated carcinomas of the colon. Am J Pathol. 2001;159:2239–2248
  68. Samowitz WS, Sweeney C, Herrick J, et al. Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers. Cancer Res. 2005;65:6063–6069
  69. Jass JR, Barker M, Fraser L, et al. APC mutation and tumour budding in colorectal cancer. J Clin Pathol. 2003;56:69–73
  70. Samowitz WS. The CpG island methylator phenotype in colorectal cancer. J Mol Diagn. 2007;9:281–283
  71. Koinuma K, Shitoh K, Miyakura Y, et al. Mutations of BRAF are associated with extensive hMLH1 promoter methylation in sporadic colorectal carcinomas. Int J Cancer. 2004;108:237–242
  72. Samowitz WS, Curtin K, Schaffer D, Robertson M, Leppert M, Slattery ML. Relationship of Ki-ras mutations in colon cancers to tumor location, stage, and survival: a population-based study. Cancer Epidemiol Biomarkers Prev. 2000;9:1193–1197
  73. Winawer SJ, Zauber AG, Fletcher RH, et al. Guidelines for colonoscopy surveillance after polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer and the American Cancer Society. CA Cancer J Clin. 2006;56:143–159
  74. Anderson J, Pollack B. Predicting of hyperplastic histology by endoscopic features. Gastrointest Endosc. 2007;52:149–150
  75. Rex DK, Ulbright TM. Step section histology of proximal colon polyps that appear hyperplastic by endoscopy. Am J Gastroenterol. 2002;97:1530–1534
  76. Young JP, Jenkins MA, Parry S, et al. Serrated pathway colorectal cancer in the population: an alternative to the adenoma-carcinoma sequence. Gut. 2007;[epub]
  77. Bosler D, Goldstein NS. Histologic features that distinguish sessile serrated adenomas and hyperplastic polyps are related to polyp size: smaller polyps merge into a single histological entity. Lab Investig. 2007;87:109A

PII: S1756-2317(07)00128-4

doi: 10.1016/j.mpdhp.2007.12.003

Diagnostic Histopathology
Volume 14, Issue 2 , Pages 78-93 , February 2008