Combination of microsatellite instability and BRAF mutation status for subtyping colorectal cancer

British Journal of Cancer

Volumn 112, Issue 12, 2015, Pages 1966-1975

  Seppala T T ^a   Bohm J P ^a   Friman, M ^a   Lahtinen, L ^a   Vayrynen V M J ^a   Liipo, T K E ^a   Ristimaki A P ^b,c   Kairaluoma, M V J ^a   Kellokumpu, I H ^a   Kuopio, T H I ^a   Mecklin, J P ^a  

^a JYVÄSKYLÄ CENTRAL HOSPITAL   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

BRAF; colon cancer; colorectal cancer; microsatellite instability; rectal cancer

Indexed keywords

B RAF KINASE; BRAF PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; COLORECTAL CANCER; DISEASE FREE SURVIVAL; DISEASE SPECIFIC SURVIVAL; FEMALE; GENE MUTATION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; PRIORITY JOURNAL; VERY ELDERLY; COLORECTAL TUMOR; ENZYMOLOGY; GENETICS; MUTATION; PATHOLOGY; PROGNOSIS;

AGED; AGED, 80 AND OVER; COLORECTAL NEOPLASMS; FEMALE; HUMANS; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; MUTATION; PROGNOSIS; PROTO-ONCOGENE PROTEINS B-RAF;

EID: 84930864927     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2015.160     Document Type: Article

References (50)

1. Aparicio T, Schischmanoff O, Poupardin C, Soufir N, Angelakov C, Barrat C, Levy V, Choudat L, Cucherousset J, Boubaya M, Lagorce C, Guetz Des G, Wind P, Benamouzig R (2012) Deficient mismatch repair phenotype is a prognostic factor for colorectal cancer in elderly patients. Dig Liver Dis 45: 245-250.
2. Barnetson RA, Tenesa A, Farrington SM, Nicholl ID, Cetnarskyj R, Porteous ME, Campbell H, Dunlop MG (2006) Identification and survival of carriers of mutations in DNA mismatch-repair genes in colon cancer. N Engl J Med 354: 2751-2763.
3. Belt EJT, Velde te EA, Krijgsman O, Brosens RPM, Tijssen M, van Essen HF, HBAC Stockmann, Bril H, Carvalho B, Ylstra B, Bonjer HJ, Meijer GA (2012) High lymph node yield is related to microsatellite instability in colon cancer. Ann Surg Oncol 19: 1222-1230.
4. Benatti P (2005) Microsatellite instability and colorectal cancer prognosis. Clin Cancer Res 11: 8332-8340.
5. Berg M, Guriby M (2013) Influence of microsatellite instability and KRAS and BRAF mutations on lymph node harvest in stage I-III colon cancers. Mol Med 19: 1.
6. Boissière-Michot F, Lazennec G, Frugier H, Jarlier M, Roca L, Duffour J, Paty Du E, Laune D, Blanchard F, Le Pessot F, Sabourin J-C, Bibeau F (2014) Characterization of an adaptive immune response in microsatellite-instable colorectal cancer. Oncoimmunology 3: e29256.
7. Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshleman JR, Burt RW, Meltzer SJ, Rodriguez-Bigas MA, Fodde R, Ranzani GN, Srivastava S (1998) A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res 58: 5248-5257.
8. Corso G, Pascale V, Flauti G, Ferrara F, Marrelli D, Roviello F (2013) Oncogenic mutations and microsatellite instability phenotype predict specific anatomical subsite in colorectal cancer patients. Eur J Hum Genet 21: 1383-1388.
9. Erichsen R, Baron JA, Stoffel EM, Laurberg S, Sandler RS, Sørensen HT (2013) Characteristics and survival of interval and sporadic colorectal cancer patients: a nationwide population-based cohort study. Am J Gastroenterol 108: 1332-1340.
10. Funkhouser WK, Lubin IM, Monzon FA, Zehnbauer BA, Evans JP, Ogino S, Nowak JA (2012) Relevance, pathogenesis, and testing algorithm for mismatch repair-defective colorectal carcinomas: a report of the association for molecular pathology. J Mol Diagn 14: 91-103.
11. Galon J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C, Lugli A, Zlobec I, Hartmann A, Bifulco C, Nagtegaal ID, Palmqvist R, Masucci GV, Botti G, Tatangelo F, Delrio P, Maio M, Laghi L, Grizzi F, Asslaber M, D'Arrigo C, Vidal-Vanaclocha F, Zavadova E, Chouchane L, Ohashi PS, Hafezi-Bakhtiari S, Wouters BG, Roehrl M, Nguyen L, Kawakami Y, Hazama S, Okuno K, Ogino S, Gibbs P, Waring P, Sato N, Torigoe T, Itoh K, Patel PS, Shukla SN, Wang Y, Kopetz S, Sinicrope FA, Scripcariu V, Ascierto PA, Marincola FM, Fox BA, Pagès F (2014) Towards the introduction of the 'Immunoscore' in the classification of malignant tumours. J Pathol 232: 199-209.
12. Gryfe R, Kim H, Hsieh ET, Aronson MD, Holowaty EJ, Bull SB, Redston M, Gallinger S (2000) Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N Engl J Med 342: 69-77.
13. Guidoboni M, Gafà R, Viel A, Doglioni C, Russo A, Santini A, Del Tin L, Macrì E, Lanza G, Boiocchi M, Dolcetti R (2001) Microsatellite instability and high content of activated cytotoxic lymphocytes identify colon cancer patients with a favorable prognosis. Am J Pathol 159: 297-304.
14. Hamilton SR (2013) BRAF mutation and microsatellite instability status in colonic and rectal carcinoma: context really does matter. J Natl Cancer Inst 105: 1075-1077.
15. Hutchins G, Southward K, Handley K, Magill L, Beaumont C, Stahlschmidt J, Richman S, Chambers P, Seymour M, Kerr D, Gray R, Quirke P (2011) Value of mismatch repair, KRAS, and BRAF mutations in predicting recurrence and benefits from chemotherapy in colorectal cancer. J Clin Oncol 29: 1261-1270.
16. Ionov Y, Peinado MA, Malkhosyan S, Shibata D, Perucho M (1993) Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 363: 558-561.
17. Kim H, Jen J, Vogelstein B, Hamilton SR (1994) Clinical and pathological characteristics of sporadic colorectal carcinomas with DNA replication errors in microsatellite sequences. Am J Pathol 145: 148-156.
18. Laghi L, Bianchi P, Malesci A (2003) Gender difference for promoter methylation pattern of hMLH1 and p16 in sporadic MSI colorectal cancer. Gastroenterology 124: 1165-1166.
19. Lochhead P, Kuchiba A, Imamura Y, Liao X, Yamauchi M, Nishihara R, Qian ZR, Morikawa T, Shen J, Meyerhardt JA, Fuchs CS, Ogino S (2013) Microsatellite instability and BRAF mutation testing in colorectal cancer prognostication. J Natl Cancer Inst 105: 1151-1156.
20. Lothe RA, Peltomäki P, Meling GI, Aaltonen LA, Nyström-Lahti M, Pylkkänen L, Heimdal K, Andersen TI, Moller P, Rognum TO (1993) Genomic instability in colorectal cancer: relationship to clinicopathological variables and family history. Cancer Res 53: 5849-5852.
21. Malesci A, Laghi L, Bianchi P, Delconte G, Randolph A, Torri V, Carnaghi C, Doci R, Rosati R, Montorsi M, Roncalli M, Gennari L, Santoro A (2007) Reduced likelihood of metastases in patients with microsatellite-unstable colorectal cancer. Clin Cancer Res 13: 3831-3839.
22. Malkhosyan SR, Yamamoto H, Piao Z, Perucho M (2000) Late onset and high incidence of colon cancer of the mutator phenotype with hypermethylated hMLH1 gene in women. Gastroenterology 119: 598.
23. Mäkinen MJ (2007) Colorectal serrated adenocarcinoma. Histopathology 50: 131-150.
24. Merok MA, Ahlquist T, Royrvik EC, Tufteland KF, Hektoen M, Sjo OH, Mala T, Svindland A, Lothe RA, Nesbakken A (2013) Microsatellite instability has a positive prognostic impact on stage II colorectal cancer after complete resection: results from a large, consecutive Norwegian series. Ann Oncol 24: 1274-1282.
25. Miyakura Y, Sugano K, Konishi F, Ichikawa A, Maekawa M, Shitoh K, Igarashi S, Kotake K, Koyama Y, Nagai H (2001) Extensive methylation of hMLH1 promoter region predominates in proximal colon cancer with microsatellite instability. Gastroenterology 121: 1300-1309.
26. Moreira L, Balaguer F, Lindor N, la Chapelle de A, Hampel H, Aaltonen LA, Hopper JL, Le Marchand L, Gallinger S, Newcomb PA, Haile R, Thibodeau SN, Gunawardena S, Jenkins MA, Buchanan DD, Potter JD, Baron JA, Ahnen DJ, Moreno V, Andreu M, Ponz de Leon M, Rustgi AK, Castells A. EPICOLON Consortium (2012) Identification of Lynch syndrome among patients with colorectal cancer. JAMA 308: 1555-1565.
27. Nishihara R, Wu K, Lochhead P, Morikawa T, Liao X, Qian ZR, Inamura K, Kim SA, Kuchiba A, Yamauchi M, Imamura Y, Willett WC, Rosner BA, Fuchs CS, Giovannucci E, Ogino S, Chan AT (2013) Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med 369: 1095-1105.
28. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Meyerhardt JA, Loda M, Giovannucci EL, Fuchs CS (2009) CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut 58: 90-96.
29. Ogino S, Shima K, Meyerhardt JA, McCleary NJ, Ng K, Hollis D, Saltz LB, Mayer RJ, Schaefer P, Whittom R, Hantel A, Benson AB, Spiegelman D, Goldberg RM, Bertagnolli MM, Fuchs CS (2012) Predictive and prognostic roles of BRAF mutation in stage III colon cancer: results from intergroup trial CALGB 89803. Clin Cancer Res 18: 890-900.
30. Palomaki GE, McClain MR, Melillo S, Hampel HL, Thibodeau SN (2009) EGAPP supplementary evidence review: DNA testing strategies aimed at reducing morbidity and mortality from Lynch syndrome. Genet Med 11: 42-65.
31. Phipps AI, Buchanan DD, Makar KW, Burnett-Hartman AN, Coghill AE, Passarelli MN, Baron JA, Ahnen DJ, Win AK, Potter JD, Newcomb PA (2012) BRAF mutation status and survival after colorectal cancer diagnosis according to patient and tumor characteristics. Cancer Epidemiol Biomarkers Prev 21: 1792-1798.
32. Phipps AI, Limburg PJ, Baron JA, Burnett-Hartman AN, Weisenberger DJ, Laird PW, Sinicrope FA, Rosty C, Buchanan DD, Potter JD, Newcomb PA (2015) Association between molecular subtypes of colorectal cancer and patient survival. Gastroenterology 148: 77-87e2.
33. Popat S (2004) Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol 23: 609-618.
34. Richards CH, Roxburgh CSD, Powell AG, Foulis AK, Horgan PG, McMillan DC (2014) The clinical utility of the local inflammatory response in colorectal cancer. Eur J Cancer 50: 309-319.
35. Roth AD, Tejpar S, Delorenzi M, Yan P, Fiocca R, Klingbiel D, Dietrich D, Biesmans B, Bodoky G, Barone C, Aranda E, Nordlinger B, Cisar L, Labianca R, Cunningham D, Van Cutsem E, Bosman F (2010) Prognostic role of KRAS and BRAF in stage II and III resected colon cancer: results of the translational study on the PETACC-3, EORTC 40993, SAKK 60-00 trial. J Clin Oncol 28: 466-474.
36. Samadder NJ, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ (2013) Associations between colorectal cancer molecular markers and pathways with clinicopathologic features in older women. Gastroenterology 145: 348-356e1-2.
37. Samowitz WS, Sweeney C, Herrick J, Albertsen H, Levin TR, Murtaugh MA, Wolff RK, Slattery ML (2005) Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers. Cancer Res 65: 6063-6069.
38. Sargent DJ, Marsoni S, Monges G, Thibodeau SN, Labianca R, Hamilton SR, French AJ, Kabat B, Foster NR, Torri V, Ribic C, Grothey A, Moore M, Zaniboni A, Seitz J-F, Sinicrope F, Gallinger S (2010) Defective mismatch repair as a predictive marker for lack of efficacy of fluorouracil-based adjuvant therapy in colon cancer. J Clin Oncol 28: 3219-3226.
39. Shia J (2008) Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome. Part I. The utility of immunohistochemistry. J Mol Diagn 10: 293-300.
40. Sloothaak DAM, Grewal S, Doornewaard H, van Duijvendijk P, Tanis PJ, Bemelman WA, van der Zaag ES, Buskens CJ (2014) Lymph node size as a predictor of lymphatic staging in colonic cancer. Br J Surg 101: 701-706.
41. Snover DC, Jass JR, Fenoglio-Preiser C, Batts KP (2005) Serrated polyps of the large intestine: a morphologic and molecular review of an evolving concept. Am J Clin Pathol 124: 380-391.
42. Thibodeau SN, Bren G, Schaid D (1993) Microsatellite instability in cancer of the proximal colon. Science 260: 816-819.
43. Thiel A, Heinonen M, Kantonen J, Gylling A, Lahtinen L, Korhonen M, Kytölä S, Mecklin J-P, Orpana A, Peltomäki P, Ristimäki A (2013) BRAF mutation in sporadic colorectal cancer and Lynch syndrome. Virchows Arch 463: 613-621.
44. Thiel A, Ristimäki A (2013) Toward a molecular classification of colorectal cancer: the role of BRAF. Front Oncol 3: 281.
45. Toon CW, Chou A, Desilva K, Chan J, Patterson J, Clarkson A, Sioson L, Jankova L, Gill AJ (2013) BRAFV600E immunohistochemistry in conjunction with mismatch repair status predicts survival in patients with colorectal cancer. Mod Pathol 27(5): 644-650.
46. Tuppurainen K, Mäkinen JM, Junttila O, Liakka A, Kyllönen AP, Tuominen H, Karttunen TJ, Mäkinen MJ (2005) Morphology and microsatellite instability in sporadic serrated and non-serrated colorectal cancer. J Pathol 207: 285-294.
47. Vasen HFA, Blanco I, Aktán-Collán K, Gopie JP, Alonso A, Aretz S, Bernstein I, Bertario L, Burn J, Capella G, Colas C, Engel C, Frayling IM, Genuardi M, Heinimann K, Hes FJ, Hodgson SV, Karagiannis JA, Lalloo F, Lindblom A, Mecklin J-P, Møller P, Myrhøj T, Nagengast FM, Parc Y, Ponz de Leon M, Renkonen-Sinisalo L, Sampson JR, Stormorken A, Sijmons RH, Tejpar S, Thomas HJW, Rahner N, Wijnen JT, Järvinen HJ, Möslein G. Mallorca group (2013) Revised guidelines for the clinical management of Lynch syndrome (HNPCC): recommendations by a group of European experts. Gut 62: 812-823.
48. Weissman SM, Burt R, Church J, Erdman S, Hampel H, Holter S, Jasperson K, Kalady MF, Haidle JL, Lynch HT, Palaniappan S, Wise PE, Senter L (2012) Identification of individuals at risk for Lynch syndrome using targeted evaluations and genetic testing: National Society of Genetic Counselors and the Collaborative Group of the Americas on Inherited Colorectal Cancer joint practice guideline. J Genet Couns 21: 484-493.
49. Yang Z, Oki E, Ando K, Morita M, Kakeji Y, Maehara Y (2010) The impact of a high-frequency microsatellite instability phenotype on the tumor location-related genetic differences in colorectal cancer. Cancer Genet Cytogenet 196: 133-139.
50. Young J, Simms LA, Biden KG, Wynter C, Whitehall V, Karamatic R, George J, Goldblatt J, Walpole I, Robin SA, Borten MM, Stitz R, Searle J, McKeone D, Fraser L, Purdie DR, Podger K, Price R, Buttenshaw R, Walsh MD, Barker M, Leggett BA, Jass JR (2001) Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis. Am J Pathol 159: 2107-2116.