Serrated pathway: Alternative route to colorectal cancer

World Journal of Gastroenterology

Volumn 19, Issue 5, 2013, Pages 607-615

  Patai, Árpád V ^a   Molnár, Béla ^b   Tulassay, Zsolt ^b   Sipos, Ferenc ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Colorectal cancer; DNA methylation; Endoscopic surveillance; Hyperplastic polyps; Serrated adenomas; Serrated pathway

Indexed keywords

EPHRIN RECEPTOR B2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE; NONSTEROID ANTIINFLAMMATORY AGENT; SOMATOMEDIN BINDING PROTEIN;

ABERRANT CRYPT FOCUS; ADENOCARCINOMA; CALCIUM INTAKE; CHROMOENDOSCOPY; COLONOSCOPY; COLORECTAL CANCER; COLORECTAL POLYP; DNA METHYLATION; DYSPLASIA; EDITORIAL; GENE EXPRESSION; GENE MUTATION; HORMONE SUBSTITUTION; HUMAN; MICROADENOMA; PREVALENCE; RISK FACTOR; SIGNAL TRANSDUCTION;

EID: 84873691159     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v19.i5.607     Document Type: Editorial

References (66)

1. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM, Bos JL. Genetic alterations during colorectal-tumor development. N Engl J Med 1988; 319: 525-532. [PMID: 2841597 DOI: 10.1056/ NEJM198809013190901]
2. Goldman H, Ming S, Hickock DF. Nature and significance of hyperplastic polyps of the human colon. Arch Pathol 1970; 89: 349-354. [PMID: 5435674]
3. Jass JR. Relation between metaplastic polyp and carcinoma of the colorectum. Lancet 1983; 1: 28-30. [PMID: 6129371 DOI: 10.1016/S0140-6736(83)91564-7]
4. Young J, Jenkins M, Parry S, Young B, Nancarrow D, English D, Giles G, Jass J. Serrated pathway colorectal cancer in the population: genetic consideration. Gut 2007; 56: 1453-1459. [PMID: 17566021 DOI: 10.1136/gut.2007.126870]
5. Snover DC. Update on the serrated pathway to colorectal carcinoma. Hum Pathol 2011; 42: 1-10. [PMID: 20869746 DOI: 10.1016/j.humpath.2010.06.002]
6. Tateyama H, Li W, Takahashi E, Miura Y, Sugiura H, Eimoto T. Apoptosis index and apoptosis-related antigen expression in serrated adenoma of the colorectum: the saw-toothed structure may be related to inhibition of apoptosis. Am J Surg Pathol 2002; 26: 249-256. [PMID: 11812948 DOI: 10.1097/00000 478-200202000-00013]
7. Higuchi T, Jass JR. My approach to serrated polyps of the colorectum. J Clin Pathol 2004; 57: 682-686. [PMID: 15220357 DOI: 10.1136/jcp.2003.015230]
8. Carragher LA, Snell KR, Giblett SM, Aldridge VS, Patel B, Cook SJ, Winton DJ, Marais R, Pritchard CA. V600EBraf induces gastrointestinal crypt senescence and promotes tumour progression through enhanced CpG methylation of p16INK4a. EMBO Mol Med 2010; 2: 458-471. [PMID: 20941790 DOI: 10.1002/emmm.201000099]
9. O'Brien MJ. Hyperplastic and serrated polyps of the colorectum. Gastroenterol Clin North Am 2007; 36: 947-968, viii. [PMID: 17996799 DOI: 10.1016/j.gtc.2007.08.007]
10. Chan AO, Broaddus RR, Houlihan PS, Issa JP, Hamilton SR, Rashid A. CpG island methylation in aberrant crypt foci of the colorectum. Am J Pathol 2002; 160: 1823-1830. [PMID: 12000733 DOI: 10.1016/S0002-9440(10)61128-5]
11. Suehiro Y, Hinoda Y. Genetic and epigenetic changes in aberrant crypt foci and serrated polyps. Cancer Sci 2008; 99: 1071-1076. [PMID: 18384435]
12. Nucci MR, Robinson CR, Longo P, Campbell P, Hamilton SR. Phenotypic and genotypic characteristics of aberrant crypt foci in human colorectal mucosa. Hum Pathol 1997; 28: 1396-1407. [PMID: 9416697 DOI: 10.1016/S0046-8177(97)90230-6]
13. Takayama T, Ohi M, Hayashi T, Miyanishi K, Nobuoka A, Nakajima T, Satoh T, Takimoto R, Kato J, Sakamaki S, Niitsu Y. Analysis of K-ras, APC, and beta-catenin in aberrant crypt foci in sporadic adenoma, cancer, and familial adenomatous polyposis. Gastroenterology 2001; 121: 599-611. [PMID: 11522744 DOI: 10.1053/gast.2001.27203]
14. Stevens RG, Swede H, Rosenberg DW. Epidemiology of colonic aberrant crypt foci: review and analysis of existing studies. Cancer Lett 2007; 252: 171-183. [PMID: 17182176 DOI: 10.1016/j.canlet.2006.11.009]
15. Rosenberg DW, Yang S, Pleau DC, Greenspan EJ, Stevens RG, Rajan TV, Heinen CD, Levine J, Zhou Y, O'Brien MJ. Mutations in BRAF and KRAS differentially distinguish serrated versus non-serrated hyperplastic aberrant crypt foci in humans. Cancer Res 2007; 67: 3551-3554. [PMID: 17440063 DOI: 10.1158/0008-5472.CAN-07-0343]
16. Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, Majoor DM, Shay JW, Mooi WJ, Peeper DS. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005; 436: 720-724. [PMID: 16079850 DOI: 10.1038/nature03890]
17. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR. Role for IGFBP7 in senescence induction by BRAF. Cell 2010; 141: 746-747. [PMID: 20510919 DOI: 10.1016/j.cell.2010.05.014]
18. Aust DE, Baretton GB. Serrated polyps of the colon and rectum (hyperplastic polyps, sessile serrated adenomas, traditional serrated adenomas, and mixed polyps)-proposal for diagnostic criteria. Virchows Arch 2010; 457: 291-297. [PMID: 20617338 DOI: 10.1007/s00428-010-0945-1]
19. Torlakovic E, Skovlund E, Snover DC, Torlakovic G, Nesland JM. Morphologic reappraisal of serrated colorectal polyps. Am J Surg Pathol 2003; 27: 65-81. [PMID: 12502929 DOI: 10.109 7/00000478-200301000-00008]
20. 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 Biomarkers Prev 2002; 11: 1012-1018. [PMID: 12376501]
21. Kearney J, Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Bleday R, Willett WC. Diet, alcohol, and smoking and the occurrence of hyperplastic polyps of the colon and rectum (United States). Cancer Causes Control 1995; 6: 45-56. [PMID: 7718735 DOI: 10.1007/BF00051680]
22. Samowitz WS, Albertsen H, Sweeney C, Herrick J, Caan BJ, Anderson KE, Wolff RK, Slattery ML. Association of smoking, CpG island methylator phenotype, and V600E BRAF mutations in colon cancer. J Natl Cancer Inst 2006; 98: 1731-1738. [PMID: 17148775 DOI: 10.1093/jnci/djj468]
23. Limsui D, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Cigarette smoking and colorectal cancer risk by molecularly defined subtypes. J Natl Cancer Inst 2010; 102: 1012-1022. [PMID: 20587792 DOI: 10.1093/jnci/djq201]
24. O'Brien MJ, Yang S, Mack C, Xu H, Huang CS, Mulcahy E, Amorosino M, Farraye FA. 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. [PMID: 17122504 DOI: 10.1097/01.pas.0000213313.36306.85]
25. O'Brien MJ, Yang S, Clebanoff JL, Mulcahy E, Farraye FA, Amorosino M, Swan N. 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. [PMID: 15087661]
26. 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. [PMID: 15489648 DOI: 10.1097/01. pas.0000141404.56839.6a]
27. Spring KJ, Zhao ZZ, Karamatic R, Walsh MD, Whitehall VL, Pike T, Simms LA, Young J, James M, Montgomery GW, Appleyard M, Hewett D, Togashi K, Jass JR, Leggett BA. High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy. Gastroenterology 2006; 131: 1400-1407. [PMID: 17101316 DOI: 10.1053/j.gastro.2006.08.038]
28. Huang CS, Farraye FA, Yang S, O'Brien MJ. The clinical significance of serrated polyps. Am J Gastroenterol 2011; 106: 229-240; quiz 241. [PMID: 21045813 DOI: 10.1038/ ajg.2010.429]
29. Arnold CA, Montgomery E, Iacobuzio-Donahue M. The serrated pathway of neoplasia: new insights into an evolving concept. Diagn Histopathol 2011; 17: 367-375. [DOI: 10.1016/ j.mpdhp.2011.06.006]
30. 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. [PMID: 2186644 DOI: 10.1097/00000478-199006000-00003]
31. Goldstein NS, Bhanot P, Odish E, Hunter S. Hyperplasticlike colon polyps that preceded microsatellite-unstable ad. Am J Clin Pathol 2003; 119: 778-796. [PMID: 12817424 DOI: 10.1309/DRFQ0WFUF1G13CTK]
32. Higuchi T, Sugihara K, Jass JR. Demographic and pathological characteristics of serrated polyps of colorectum. Histopathology 2005; 47: 32-40. [PMID: 15982321 DOI: 10.1111/ j.1365-2559.2005.02180.x]
33. Tannapfel A, Neid M, Aust D, Baretton G. The origins of colorectal carcinoma: specific nomenclature for different pathways and precursor lesions. Dtsch Arztebl Int 2010; 107: 760-766. [PMID: 21085545]
34. 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: 25-46. [PMID: 18313538 DOI: 10.1016/j.gtc.2007.12.014]
35. Snover D, Ahnen D, Burt R, Odze RD. Serrated Polyps of the Colon and Rectum and Serrated Polyposis. WHO Classification of Tumours of the Digestive System. 4th ed. Lyon: IARC, 2010
36. Fidalgo CA, Santos L, Rosa I, Fonseca R, Lage P, Claro I, Chaves P, Dias Pereira A. Hyperplastic polyp? The impact of the new classification for serrated polyps. Gut 2011; 60 Suppl 3: A306
37. Torlakovic E, Snover DC. Serrated adenomatous polyposis in humans. Gastroenterology 1996; 110: 748-755. [PMID: 8608884 DOI: 10.1053/gast.1996.v110.pm8608884]
38. Mäkinen MJ. Colorectal serrated adenocarcinoma. Histopathology 2007; 50: 131-150. [PMID: 17204027 DOI: 10.1111/ j.1365-2559.2006.02548.x]
39. Kimura T, Yamamoto E, Yamano HO, Suzuki H, Kamimae S, Nojima M, Sawada T, Ashida M, Yoshikawa K, Takagi R, Kato R, Harada T, Suzuki R, Maruyama R, Kai M, Imai K, Shinomura Y, Sugai T, Toyota M. A novel pit pattern identifies the precursor of colorectal cancer derived from sessile serrated adenoma. Am J Gastroenterol 2012; 107: 460-469. [PMID: 22233696 DOI: 10.1038/ajg.2011.457]
40. Sheridan TB, Fenton H, Lewin MR, Burkart AL, Iacobuzio-Donahue CA, Frankel WL, Montgomery E. Sessile serrated adenomas with lowand high-grade dysplasia and early carcinomas: an immunohistochemical study of serrated lesions "caught in the act". Am J Clin Pathol 2006; 126: 564-571. [PMID: 16938659 DOI: 10.1309/C7JE8BVL8420V5VT]
41. Oono Y, Fu K, Nakamura H, Iriguchi Y, Yamamura A, Tomino Y, Oda J, Mizutani M, Takayanagi S, Kishi D, Shinohara T, Yamada K, Matumoto J, Imamura K. Progression of a sessile serrated adenoma to an early invasive cancer within 8 months. Dig Dis Sci 2009; 54: 906-909. [PMID: 18688718 DOI: 10.1007/s10620-008-0407-7]
42. Torlakovic EE, Gomez JD, Driman DK, Parfitt JR, Wang C, Benerjee T, Snover DC. Sessile serrated adenoma (SSA) vs. traditional serrated adenoma (TSA). Am J Surg Pathol 2008; 32: 21-29. [PMID: 18162766 DOI: 10.1097/ PAS.0b013e318157f002]
43. 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. [PMID: 17667549 DOI: 10.1097/PAS.0b013e31802d74c0]
44. Ha SY, Lee SM, Lee EJ, Kang SY, Jang KT, Park CK, Kim JY, Kim YH, Chang DK, Kim KM. Filiform serrated adenoma is an unusual, less aggressive variant of traditional serrated adenoma. Pathology 2012; 44: 18-23. [PMID: 22157687 DOI: 10.1097/PAT.0b013e32834d7bbf]
45. Jass JR, Whitehall VL, Young J, Leggett BA. Emerging concepts in colorectal neoplasia. Gastroenterology 2002; 123: 862-876. [PMID: 12198712 DOI: 10.1053/gast.2002.35392]
46. 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. [PMID: 1289763 DOI: 10.3109/00313029209068874]
47. Mäkinen MJ, George SM, Jernvall P, Mäkelä J, Vihko P, Karttunen TJ. Colorectal carcinoma associated with serrated adenoma--prevalence, histological features, and prognosis. J Pathol 2001; 193: 286-294. [PMID: 11241406 DOI: 10.1002/1096-9896(2000)9999:]
48. Tuppurainen K, Mäkinen JM, Junttila O, Liakka A, Kyllönen AP, Tuominen H, Karttunen TJ, Mäkinen MJ. Morphology and microsatellite instability in sporadic serrated and nonserrated colorectal cancer. J Pathol 2005; 207: 285-294. [PMID: 16177963 DOI: 10.1002/path.1850]
49. Laiho P, Kokko A, Vanharanta S, Salovaara R, Sammalkorpi H, Järvinen H, Mecklin JP, Karttunen TJ, Tuppurainen K, Davalos V, Schwartz S, Arango D, Mäkinen MJ, Aaltonen LA. Serrated carcinomas form a subclass of colorectal cancer with distinct molecular basis. Oncogene 2007; 26: 312-320. [PMID: 16819509 DOI: 10.1038/sj.onc.1209778]
50. García-Solano J, Pérez-Guillermo M, Conesa-Zamora P, Acosta-Ortega J, Trujillo-Santos J, Cerezuela-Fuentes P, Mäkinen MJ. Clinicopathologic study of 85 colorectal serrated adenocarcinomas: further insights into the full recognition of a new subset of colorectal carcinoma. Hum Pathol 2010; 41: 1359-1368. [PMID: 20594582 DOI: 10.1016/j.humpath.2010.04.002]
51. Leonard DF, Dozois EJ, Smyrk TC, Suwanthanma W, Baron TH, Cima RR, Larson DW. Endoscopic and surgical management of serrated colonic polyps. Br J Surg 2011; 98: 1685-1694. [PMID: 22034178 DOI: 10.1002/bjs.7654]
52. Patai AV, Molnár B, Kalmár A, Schöller A, Tóth K, Tulassay Z. Role of DNA methylation in colorectal carcinogenesis. Dig Dis 2012; 30: 310-315. [PMID: 22722557 DOI: 10.1159/000337004.]
53. Patai AV, Galamb O, Kalmár A, Wichmann B, Valcz G, Patai A, Leiszter K, Tóth K, Tulassay Z, Molnár B. Non-sequential DNA methylation alterations in the adenoma-dysplasia-carcinoma sequence in the distal colon. Gut 2011; 60 Suppl 3: A76.
54. Samowitz WS, Sweeney C, Herrick J, Albertsen H, Levin TR, Murtaugh MA, Wolff RK, Slattery ML. Poor survival associated with the BRAF V600E mutation in microsatellitestable colon cancers. Cancer Res 2005; 65: 6063-6069. [PMID: 16024606 DOI: 10.1158/0008-5472.CAN-05-0404]
55. Pai RK, Jayachandran P, Koong AC, Chang DT, Kwok S, Ma L, Arber DA, Balise RR, Tubbs RR, Shadrach B, Pai RK. BRAF-mutated, microsatellite-stable adenocarcinoma of the proximal colon: an aggressive adenocarcinoma with poor survival, mucinous differentiation, and adverse morphologic features. Am J Surg Pathol 2012; 36: 744-752. [PMID: 22314188 DOI: 10.1097/PAS.0b013e31824430d7]
56. Samowitz WS, Curtin K, Ma KN, Schaffer D, Coleman LW, Leppert M, Slattery ML. Microsatellite instability in sporadic colon cancer is associated with an improved prognosis at the population level. Cancer Epidemiol Biomarkers Prev 2001; 10: 917-923. [PMID: 11535541]
57. Lockett MJ, Atkin WS. Hyperplastic polyposis: prevalence and cancer risk. Gut 2001; 48 Suppl 1: A4
58. Roberts A, Nancarrow D, Clendenning M, Buchanan DD, Jenkins MA, Duggan D, Taverna D, McKeone D, Walters R, Walsh MD, Young BW, Jass JR, Rosty C, Gattas M, Pelzer E, Hopper JL, Goldblatt J, George J, Suthers GK, Phillips K, Parry S, Woodall S, Arnold J, Tucker K, Muir A, Drini M, Macrae F, Newcomb P, Potter JD, Pavluk E, Lindblom A, Young JP. Linkage to chromosome 2q32.2-q33.3 in familial serrated neoplasia (Jass syndrome). Fam Cancer 2011; 10: 245-254. [PMID: 21165777]
59. Kalady MF, Jarrar A, Leach B, LaGuardia L, O'Malley M, Eng C, Church JM. Defining phenotypes and cancer risk in hyperplastic polyposis syndrome. Dis Colon Rectum 2011; 54: 164-170. [PMID: 21228663 DOI: 10.1007/DCR.0b013e3181fd4c15]
60. Jarrar AM, Church JM, Fay S, Kalady MF. Is the phenotype mixed or mistaken? Hereditary nonpolyposis colorectal cancer and hyperplastic polyposis syndrome. Dis Colon Rectum 2009; 52: 1949-1955. [PMID: 19934914 DOI: 10.1007/ DCR.0b013e3181b5450c]
61. Teriaky A, Driman DK, Chande N. Outcomes of a 5-year follow-up of patients with sessile serrated adenomas. Scand J Gastroenterol 2012; 47: 178-183. [PMID: 22229626 DOI: 10.3109 /00365521.2011.645499]
62. Rondagh EJ, Masclee AA, Bouwens MW, Winkens B, Riedl RG, de Bruïne AP, de Ridder R, Kaltenbach T, Soetikno RM, Sanduleanu S. Endoscopic red flags for the detection of highrisk serrated polyps: an observational study. Endoscopy 2011; 43: 1052-1058. [PMID: 21971921 DOI: 10.1055/s-0030-1256770]
63. Kashida H, Ikehara N, Hamatani S, Kudo SE, Kudo M. Endoscopic characteristics of colorectal serrated lesions. Hepatogastroenterology 2011; 58: 1163-1167. [PMID: 21937375 DOI: 10.5754/hge10093]
64. Terdiman JP, McQuaid KR. Surveillance guidelines should be updated to recognize the importance of serrated polyps. Gastroenterology 2010; 139: 1444-1447. [PMID: 20875785 DOI: 10.1053/j.gastro.2010.09.024]
65. Gurudu SR, Heigh RI, De Petris G, Heigh EG, Leighton JA, Pasha SF, Malagon IB, Das A. Sessile serrated adenomas: demographic, endoscopic and pathological characteristics. World J Gastroenterol 2010; 16: 3402-3405. [PMID: 20632442 DOI: 10.3748/wjg.v16.i27.3402]
66. Brooker JC, Saunders BP, Shah SG, Thapar CJ, Suzuki N, Williams CB. Treatment with argon plasma coagulation reduces recurrence after piecemeal resection of large sessile colonic polyps: a randomized trial and recommendations. Gastrointest Endosc 2002; 55: 371-375. [PMID: 11868011 DOI: 10.1067/mge.2002.121597]