Relevance, Pathogenesis, and testing algorithm for mismatch repair-defective colorectal carcinomas: A report of the association for molecular pathology

Journal of Molecular Diagnostics

Volumn 14, Issue 2, 2012, Pages 91-103

  Funkhouser, William K ^a   Lubin, Ira M ^a,b   Monzon, Federico A ^a,c   Zehnbauer, Barbara A ^b   Evans, James P ^a   Ogino, Shuji ^d   Nowak, Jan A ^e  

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

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c HOUSTON METHODIST HOSPITAL   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; EPITHELIAL CELL ADHESION MOLECULE; FLUOROURACIL; MISMATCH REPAIR PROTEIN PMS2; PROTEIN MLH1; PROTEIN MSH2;

ARTICLE; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER SURVIVAL; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CLASSIFICATION ALGORITHM; COLORECTAL ADENOMA; COLORECTAL CARCINOMA; DNA METHYLATION; DRUG TREATMENT FAILURE; GENE DELETION; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETIC SCREENING; GERM LINE; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HETEROZYGOTE; HUMAN; LOSS OF FUNCTION MUTATION; METASTASIS; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; MUTATIONAL ANALYSIS; ONCOGENE K RAS; PENETRANCE; PROMOTER REGION; SCREENING TEST;

EID: 84857242852     PISSN: 15251578     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmoldx.2011.11.001     Document Type: Article

References (129)

1. M.R. Griffin, E.J. Bergstralh, R.J. Coffey, R.W. Beart Jr., L.J. Melton 3rd Predictors of survival after curative resection of carcinoma of the colon and rectum Cancer 60 1987 2318 2324 (Pubitemid 17153502)
2. R. Gryfe, H. Kim, E.T. Hsieh, M.D. Aronson, E.J. Holowaty, S.B. Bull, M. Redston, S. Gallinger Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer N Engl J Med 342 2000 69 77 (Pubitemid 30036597)
3. C. Compton, C.M. Fenoglio-Preiser, N. Pettigrew, L.P. Fielding American Joint Committee on Cancer Prognostic Factors Consensus Conference: Colorectal Working Group Cancer 88 2000 1739 1757 (Pubitemid 30183160)
4. M. Aarnio, H. Mustonen, J.P. Mecklin, H.J. Jarvinen Prognosis of colorectal cancer varies in different high-risk conditions Ann Med 30 1998 75 80 (Pubitemid 28154500)
5. R. Sankila, L.A. Aaltonen, H.J. Jarvinen, J.P. Mecklin Better survival rates in patients with MLH1-associated hereditary colorectal cancer Gastroenterology 110 1996 682 687 (Pubitemid 26071836)
6. K.C. Halling, A.J. French, S.K. McDonnell, L.J. Burgart, D.J. Schaid, B.J. Peterson, L. Moon-Tasson, M.R. Mahoney, D.J. Sargent, M.J. O'Connell, T.E. Witzig, G.H. Farr Jr., R.M. Goldberg, S.N. Thibodeau Microsatellite instability and 8p allelic imbalance in stage B2 and C colorectal cancers J Natl Cancer Inst 91 1999 1295 1303 (Pubitemid 29387571)
7. P. Karran Microsatellite instability and DNA mismatch repair in human cancer Cancer Biol 7 1996 15 24 (Pubitemid 26132192)
8. N. Arnheim, D. Shibata DNA mismatch repair in mammals: role in disease and meiosis Curr Opin Genet Dev 7 1997 364 370 (Pubitemid 27292288)
9. L.A. Aaltonen, P. Peltomaki, F.S. Leach, P. Sistonen, L. Pylkkanen, J.P. Mecklin, H. Jarvinen, S.M. Powell, J. Jen, S.R. Hamilton, G.M. Petersen, K.W. Kinzler, B. Vogelstein, A. de la Chapelle Clues to the pathogenesis of familial colorectal cancer [see comments] Science 260 1993 812 816 (Pubitemid 23167611)
10. S.N. Thibodeau, G. Bren, D. Schaid Microsatellite instability in cancer of the proximal colon Science 260 1993 816 819 (Pubitemid 23167612)
11. W. Dietmaier, S. Wallinger, T. Bocker, F. Kullmann, R. Fishel, J. Ruschoff Diagnostic microsatellite instability: definition and correlation with mismatch repair protein expression Cancer Res 57 1997 4749 4756 (Pubitemid 27468981)
12. M.G. Hanford, B.C. Rushton, L.C. Gowen, R.A. Farber Microsatellite mutation rates in cancer cell lines deficient or proficient in mismatch repair Oncogene 16 1998 2389 2393 (Pubitemid 28226886)
13. S.N. Thibodeau, A.J. French, J.M. Cunningham, D. Tester, L.J. Burgart, P.C. Roche, S.K. McDonnell, D.J. Schaid, C.W. Vockley, V.V. Michels, G.H. Farr Jr., M.J. O'Connell Microsatellite instability in colorectal cancer: different mutator phenotypes and the principal involvement of hMLH1 Cancer Res 58 1998 1713 1718 (Pubitemid 28215098)
14. L.M. Baudhuin, L.J. Burgart, O. Leontovich, S.N. Thibodeau Use of microsatellite instability and immunohistochemistry testing for the identification of individuals at risk for Lynch syndrome Fam Cancer 4 2005 255 265 (Pubitemid 41242196)
15. T. Myrhoj, M.L. Bisgaard, I. Bernstein, L.B. Svendsen, J.O. Sondergaard, S. Bulow Hereditary non-polyposis colorectal cancer: clinical features and survival Results from the Danish HNPCC register Scand J Gastroenterol 32 1997 572 576 (Pubitemid 27314268)
16. W.S. Samowitz, K. Curtin, K.N. Ma, D. Schaffer, L.W. Coleman, M. Leppert, M.L. Slattery Microsatellite instability in sporadic colon cancer is associated with an improved prognosis at the population level Cancer Epidemiol Biomarkers Prev 10 2001 917 923 (Pubitemid 32844897)
17. J.R. Jass Classification of colorectal cancer based on correlation of clinical, morphological and molecular features Histopathology 50 2007 113 130 (Pubitemid 44953403)
18. K. Nosho, N. Irahara, K. Shima, S. Kure, G.J. Kirkner, E.S. Schernhammer, A. Hazra, D.J. Hunter, J. Quackenbush, D. Spiegelman, E.L. Giovannucci, C.S. Fuchs, S. Ogino Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample PLoS One 3 2008 e3698
19. H. Kim, J. Jen, B. Vogelstein, S.R. Hamilton Clinical and pathological characteristics of sporadic colorectal carcinomas with DNA replication errors in microsatellite sequences Am J Pathol 145 1994 148 156 (Pubitemid 24217493)
20. A. de la Chapelle Genetic predisposition to colorectal cancer Nat Rev Cancer 4 2004 769 780 (Pubitemid 39331149)
21. H.F. Vasen, J.P. Mecklin, P.M. Khan, H.T. Lynch The International Collaborative Group on Hereditary Non-Polyposis Colorectal Cancer (ICG-HNPCC) Dis Colon Rectum 34 1991 424 425
22. H.T. Lynch, T.C. Smyrk, P. Watson, S. Lanspa, J.F. Lynch, P.M. Lynch, R.J. Cavalieri, C.R. Boland Genetics, natural history, tumor spectrum, and pathology of hereditary nonpolyposis colorectal cancer: an update review Gastroenterology 104 1993 1535 1549 (Pubitemid 23235432)
23. S.C. Rossi, S. Srivastava National Cancer Institute workshop on genetic screening for colorectal cancer J Natl Cancer Inst 88 1996 331 339
24. L.A. Aaltonen, R. Salovaara, P. Kristo, F. Canzian, A. Hemminki, P. Peltomaki, R.B. Chadwick, H. Kaariainen, M. Eskelinen, H. Jarvinen, J.P. Mecklin, A. de LA Chapelle Incidence of hereditary nonpolyposis colorectal cancer and the feasibility of molecular screening for the disease [see comments] N Engl J Med 338 1998 1481 1487 (Pubitemid 28226275)
25. J.M. Cunningham, C.Y. Kim, E.R. Christensen, D.J. Tester, Y. Parc, L.J. Burgart, K.C. Halling, S.K. McDonnell, D.J. Schaid, C. Walsh Vockley, V. Kubly, H. Nelson, V.V. Michels, S.N. Thibodeau The frequency of hereditary defective mismatch repair in a prospective series of unselected colorectal carcinomas Am J Hum Genet 69 2001 780 790 (Pubitemid 32868523)
26. M.C. Southey, M.A. Young, J. Whitty, S. Mifsud, M. Keilar, L. Mead, L. Trute, K. Aittomaki, S.A. McLachlan, H. Debinski, D.J. Venter, J.E. Armes Molecular pathologic analysis enhances the diagnosis and management of Muir-Torre syndrome and gives insight into its underlying molecular pathogenesis Am J Surg Pathol 25 2001 936 941 (Pubitemid 32594988)
27. P. Watson, K.M. Lin, M.A. Rodriguez-Bigas, T. Smyrk, S. Lemon, M. Shashidharan, B. Franklin, B. Karr, A. Thorson, H.T. Lynch Colorectal carcinoma survival among hereditary nonpolyposis colorectal carcinoma family members Cancer 83 1998 259 266 (Pubitemid 28317805)
28. S. Popat, R. Hubner, R.S. Houlston Systematic review of microsatellite instability and colorectal cancer prognosis J Clin Oncol 23 2005 609 618 (Pubitemid 46224239)
29. P. Benatti, R. Gafa, D. Barana, M. Marino, A. Scarselli, M. Pedroni, I. Maestri, L. Guerzoni, L. Roncucci, M. Menigatti, B. Roncari, S. Maffei, G. Rossi, G. Ponti, A. Santini, L. Losi, C. Di Gregorio, C. Oliani, M. Ponz de Leon, G. Lanza Microsatellite instability and colorectal cancer prognosis Clin Cancer Res 11 2005 8332 8340 (Pubitemid 41746945)
30. G. Lanza, R. Gafa, A. Santini, I. Maestri, L. Guerzoni, L. Cavazzini Immunohistochemical test for MLH1 and MSH2 expression predicts clinical outcome in stage II and III colorectal cancer patients J Clin Oncol 24 2006 2359 2367 (Pubitemid 46630668)
31. C.M. Wright, O.F. Dent, M. Barker, R.C. Newland, P.H. Chapuis, E.L. Bokey, J.P. Young, B.A. Leggett, J.R. Jass, G.A. Macdonald Prognostic significance of extensive microsatellite instability in sporadic clinicopathological stage C colorectal cancer Br J Surg 87 2000 1197 1202
32. C.M. Ribic, D.J. Sargent, M.J. Moore, S.N. Thibodeau, A.J. French, R.M. Goldberg, S.R. Hamilton, P. Laurent-Puig, R. Gryfe, L.E. Shepherd, D. Tu, M. Redston, S. Gallinger Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer N Engl J Med 349 2003 247 257 (Pubitemid 36859476)
33. J.M. Carethers, E.J. Smith, C.A. Behling, L. Nguyen, A. Tajima, R.T. Doctolero, B.L. Cabrera, A. Goel, C.A. Arnold, K. Miyai, C.R. Boland Use of 5-fluorouracil and survival in patients with microsatellite-unstable colorectal cancer Gastroenterology 126 2004 394 401 (Pubitemid 38182296)
34. W. de Vos, H. Meulenbeld, J. Keibeuker, F. Nagengast, F. Menko, G. Griffioen, A. Cats, H. Morreau, H. Gelderblom, H. Vasen Survival after adjuvant 5-FU treatment for stage III colon cancer in HNPCC CRC Int J Cancer 109 2004 468
35. R. Jover, P. Zapater, A. Castells, X. Llor, M. Andreu, J. Cubiella, V. Pinol, R.M. Xicola, L. Bujanda, J.M. Rene, J. Clofent, X. Bessa, J.D. Morillas, D. Nicolas-Perez, A. Paya, C. Alenda Mismatch repair status in the prediction of benefit from adjuvant fluorouracil chemotherapy in colorectal cancer Gut 55 2006 848 855 (Pubitemid 43764557)
36. D.J. Sargent, S. Marsoni, G. Monges, S.N. Thibodeau, R. Labianca, S.R. Hamilton, A.J. French, B. Kabat, N.R. Foster, V. Torri, C. Ribic, A. Grothey, M. Moore, A. Zaniboni, J.F. Seitz, F. Sinicrope, S. Gallinger Defective mismatch repair as a predictive marker for lack of efficacy of fluorouracil-based adjuvant therapy in colon cancer J Clin Oncol 28 2010 3219 3226
37. F.A. Sinicrope DNA mismatch repair and adjuvant chemotherapy in sporadic colon cancer Nat Rev Clin Oncol 7 2010 174 177
38. R. Siegel, E. Ward, O. Brawley, A. Jemal Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths CA Cancer J Clin 61 2011 212 236
39. Berg: Recommendations from the EGAPP Working Group: genetic testing strategies in newly diagnosed individuals with colorectal cancer aimed at reducing morbidity and mortality from Lynch syndrome in relatives Genet Med 11 2009 35 41
40. W.S. Samowitz, H. Albertsen, J. Herrick, T.R. Levin, C. Sweeney, M.A. Murtaugh, R.K. Wolff, M.L. Slattery Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer Gastroenterology 129 2005 837 845 (Pubitemid 41242676)
41. S. de Vogel, M.P. Weijenberg, J.G. Herman, K.A. Wouters, A.F. de Goeij, P.A. van den Brandt, A.P. de Bruine, M. van Engeland MGMT and MLH1 promoter methylation versus APC KRAS and BRAF gene mutations in colorectal cancer: indications for distinct pathways and sequence of events Ann Oncol 20 2009 1216 1222
42. L. Barault, C. Charon-Barra, V. Jooste, M.F. de la Vega, L. Martin, P. Roignot, P. Rat, A.M. Bouvier, P. Laurent-Puig, J. Faivre, C. Chapusot, F. Piard Hypermethylator phenotype in sporadic colon cancer: study on a population-based series of 582 cases Cancer Res 68 2008 8541 8546
43. D.R. English, J.P. Young, J.A. Simpson, M.A. Jenkins, M.C. Southey, M.D. Walsh, D.D. Buchanan, M.A. Barker, A.M. Haydon, S.G. Royce, A. Roberts, S. Parry, J.L. Hopper, J.J. Jass, G.G. Giles Ethnicity and risk for colorectal cancers showing somatic BRAF V600E mutation or CpG island methylator phenotype Cancer Epidemiol Biomarkers Prev 17 2008 1774 1780
44. Campbell PT, Jacobs ET, Ulrich CM, Figueiredo JC, Poynter JN, McLaughlin JR, Haile RW, Jacobs EJ, Newcomb PA, Potter JD, Le Marchand L, Green RC, Parfrey P, Younghusband HB, Cotterchio M, Gallinger S, Jenkins MA, Hopper JL, Baron JA, Thibodeau SN, Lindor NM, Limburg PJ, Martinez ME: Case-control study of overweight, obesity, and colorectal cancer risk, overall and by tumor microsatellite instability status. J Natl Cancer Inst 102:391400
45. D.C. Snover Update on the serrated pathway to colorectal carcinoma Hum Pathol 42 2011 1 10
46. M.F. Kane, M. Loda, G.M. Gaida, J. Lipman, R. Mishra, H. Goldman, J.M. Jessup, R. Kolodner Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines Cancer Res 57 1997 808 811 (Pubitemid 27097998)
47. J.G. Herman, A. Umar, K. Polyak, J.R. Graff, N. Ahuja, J.P. Issa, S. Markowitz, J.K. Willson, S.R. Hamilton, K.W. Kinzler, M.F. Kane, R.D. Kolodner, B. Vogelstein, T.A. Kunkel, S.B. Baylin Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma Proc Natl Acad Sci U S A 95 1998 6870 6875 (Pubitemid 28278073)
48. J.M. Cunningham, E.R. Christensen, D.J. Tester, C.Y. Kim, P.C. Roche, L.J. Burgart, S.N. Thibodeau Hypermethylation of the hMLH1 promoter in colon cancer with microsatellite instability Cancer Res 58 1998 3455 3460 (Pubitemid 28371090)
49. S.A. Kuismanen, M.T. Holmberg, R. Salovaara, A. de la Chapelle, P. Peltomaki Genetic and epigenetic modification of MLH1 accounts for a major share of microsatellite-unstable colorectal cancers Am J Pathol 156 2000 1773 1779 (Pubitemid 30646714)
50. W.S. Samowitz The CpG island methylator phenotype in colorectal cancer J Mol Diagn 2007
51. S. Ogino, T. Kawasaki, G.J. Kirkner, P. Kraft, M. Loda, C.S. Fuchs Evaluation of markers for CpG island methylator phenotype (CIMP) in colorectal cancer by a large population-based sample J Mol Diagn 9 2007 305 314 (Pubitemid 47305066)
52. C. Oliveira, J.L. Westra, D. Arango, M. Ollikainen, E. Domingo, A. Ferreira, S. Velho, R. Niessen, K. Lagerstedt, P. Alhopuro, P. Laiho, I. Veiga, M.R. Teixeira, M. Ligtenberg, J.H. Kleibeuker, R.H. Sijmons, J.T. Plukker, K. Imai, P. Lage, R. Hamelin, C. Albuquerque, S. Schwartz Jr., A. Lindblom, P. Peltomaki, H. Yamamoto, L.A. Aaltonen, R. Seruca, R.M. Hofstra Distinct patterns of KRAS mutations in colorectal carcinomas according to germline mismatch repair defects and hMLH1 methylation status Hum Mol Genet 13 2004 2303 2311 (Pubitemid 39359927)
53. M. Menigatti, C. Di Gregorio, F. Borghi, E. Sala, A. Scarselli, M. Pedroni, M. Foroni, P. Benatti, L. Roncucci, M. Ponz de Leon, A. Percesepe Methylation pattern of different regions of the MLH1 promoter and silencing of gene expression in hereditary and sporadic colorectal cancer Genes Chromosomes Cancer 31 2001 357 361 (Pubitemid 32622712)
54. A. McGivern, C.V. Wynter, V.L. Whitehall, T. Kambara, K.J. Spring, M.D. Walsh, M.A. Barker, S. Arnold, L.A. Simms, B.A. Leggett, J. Young, J.R. Jass Promoter hypermethylation frequency and BRAF mutations distinguish hereditary non-polyposis colon cancer from sporadic MSI-H colon cancer Fam Cancer 3 2004 101 107 (Pubitemid 40645891)
55. J. Young, L.A. Simms, K.G. Biden, C. Wynter, V. Whitehall, R. Karamatic, J. George, J. Goldblatt, I. Walpole, S.A. Robin, M.M. Borten, R. Stitz, J. Searle, D. McKeone, L. Fraser, D.R. Purdie, K. Podger, R. Price, R. Buttenshaw, M.D. Walsh, M. Barker, B.A. Leggett, J.R. Jass Features of colorectal cancers with high-level microsatellite instability occurring in familial and sporadic settings: parallel pathways of tumorigenesis Am J Pathol 159 2001 2107 2116 (Pubitemid 33104265)
56. N. Rahner, N. Friedrichs, V. Steinke, S. Aretz, W. Friedl, R. Buettner, E. Mangold, P. Propping, C. Walldorf Coexisting somatic promoter hypermethylation and pathogenic MLH1 germline mutation in Lynch syndrome J Pathol 214 2008 10 16
57. M. Morak, H.K. Schackert, N. Rahner, B. Betz, M. Ebert, C. Walldorf, B. Royer-Pokora, K. Schulmann, M. von Knebel-Doeberitz, W. Dietmaier, G. Keller, B. Kerker, G. Leitner, E. Holinski-Feder Further evidence for heritability of an epimutation in one of 12 cases with MLH1 promoter methylation in blood cells clinically displaying HNPCC Eur J Hum Genet 16 2008 804 811 (Pubitemid 351865678)
58. R.C. Niessen, R.M. Hofstra, H. Westers, M.J. Ligtenberg, K. Kooi, P.O. Jager, M.L. de Groote, T. Dijkhuizen, M.J. Olderode-Berends, H. Hollema, J.H. Kleibeuker, R.H. Sijmons Germline hypermethylation of MLH1 and EPCAM deletions are a frequent cause of Lynch syndrome Genes Chromosomes Cancer 48 2009 737 744
59. M. Toyota, C. Ho, N. Ahuja, K.W. Jair, Q. Li, M. Ohe-Toyota, S.B. Baylin, J.P. Issa Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification Cancer Res 59 1999 2307 2312 (Pubitemid 29242273)
60. M. Toyota, N. Ahuja, M. Ohe-Toyota, J.G. Herman, S.B. Baylin, J.P. Issa CpG island methylator phenotype in colorectal cancer Proc Natl Acad Sci U S A 96 1999 8681 8686 (Pubitemid 29354851)
61. A.R. Sepulveda, D. Jones, S. Ogino, W. Samowitz, M.L. Gulley, R. Edwards, V. Levenson, V.M. Pratt, B. Yang, K. Nafa, L. Yan, P. Vitazka CpG methylation analysiscurrent status of clinical assays and potential applications in molecular diagnostics: a report of the Association for Molecular Pathology J Mol Diagn 11 2009 266 278
62. J.M. Teodoridis, C. Hardie, R. Brown CpG island methylator phenotype (CIMP) in cancer: causes and implications Cancer Lett 268 2008 177 186
63. S. Ogino, A. Goel Molecular classification and correlates in colorectal cancer J Mol Diagn 10 2008 13 27 (Pubitemid 351184831)
64. H.G. Linhart, H. Lin, Y. Yamada, E. Moran, E.J. Steine, S. Gokhale, G. Lo, E. Cantu, M. Ehrich, T. He, A. Meissner, R. Jaenisch Dnmt3b promotes tumorigenesis in vivo by gene-specific de novo methylation and transcriptional silencing Genes Dev 21 2007 3110 3122 (Pubitemid 350223528)
65. K. Nosho, K. Shima, N. Irahara, S. Kure, Y. Baba, G.J. Kirkner, L. Chen, S. Gokhale, A. Hazra, D. Spiegelman, E.L. Giovannucci, R. Jaenisch, C.S. Fuchs, S. Ogino DNMT3B expression might contribute to CpG island methylator phenotype in colorectal cancer Clin Cancer Res 15 2009 3663 3671
66. T. Kambara, L.A. Simms, V.L. Whitehall, K.J. Spring, C.V. Wynter, M.D. Walsh, M.A. Barker, S. Arnold, A. McGivern, N. Matsubara, N. Tanaka, T. Higuchi, J. Young, J.R. Jass, B.A. Leggett BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum Gut 53 2004 1137 1144 (Pubitemid 38961968)
67. J.R. Jass Serrated adenoma of the colorectum and the DNA-methylator phenotype Nat Clin Pract Oncol 2 2005 398 405 (Pubitemid 43115008)
68. S. Ogino, K. Nosho, G.J. Kirkner, T. Kawasaki, J.A. Meyerhardt, M. Loda, E.L. Giovannucci, C.S. Fuchs CpG island methylator phenotype, microsatellite instability: BRAF mutation and clinical outcome in colon cancer Gut 58 2009 90 96
69. E. Domingo, P. Laiho, M. Ollikainen, M. Pinto, L. Wang, A.J. French, J. Westra, T. Frebourg, E. Espin, M. Armengol, R. Hamelin, H. Yamamoto, R.M. Hofstra, R. Seruca, A. Lindblom, P. Peltomaki, S.N. Thibodeau, L.A. Aaltonen, S. Schwartz Jr. BRAF screening as a low-cost effective strategy for simplifying HNPCC genetic testing J Med Genet 41 2004 664 668 (Pubitemid 39208606)
70. K. Koinuma, K. Shitoh, Y. Miyakura, T. Furukawa, Y. Yamashita, J. Ota, R. Ohki, Y.L. Choi, T. Wada, F. Konishi, H. Nagai, H. Mano Mutations of BRAF are associated with extensive hMLH1 promoter methylation in sporadic colorectal carcinomas Int J Cancer 108 2004 237 242 (Pubitemid 37541777)
71. B. Halvarsson, H. Anderson, K. Domanska, G. Lindmark, M. Nilbert Clinicopathologic factors identify sporadic mismatch repair-defective colon cancers Am J Clin Pathol 129 2008 238 244 (Pubitemid 352029314)
72. H. Rajagopalan, A. Bardelli, C. Lengauer, K.W. Kinzler, B. Vogelstein, V.E. Velculescu Tumorigenesis: rAF/RAS oncogenes and mismatch-repair status Nature 418 2002 934 (Pubitemid 34976022)
73. G. Deng, I. Bell, S. Crawley, J. Gum, J.P. Terdiman, B.A. Allen, B. Truta, M.H. Sleisenger, Y.S. Kim BRAF mutation is frequently present in sporadic colorectal cancer with methylated hMLH1, but not in hereditary nonpolyposis colorectal cancer Clin Cancer Res 10 2004 191 195 (Pubitemid 38114179)
74. E. Domingo, R.C. Niessen, C. Oliveira, P. Alhopuro, C. Moutinho, E. Espin, M. Armengol, R.H. Sijmons, J.H. Kleibeuker, R. Seruca, L.A. Aaltonen, K. Imai, H. Yamamoto, S. Schwartz Jr., R.M. Hofstra BRAF-V600E is not involved in the colorectal tumorigenesis of HNPCC in patients with functional MLH1 and MSH2 genes Oncogene 24 2005 3995 3998 (Pubitemid 40896411)
75. X. Bessa, B. Balleste, M. Andreu, A. Castells, B. Bellosillo, F. Balaguer, S. Castellvi-Bel, A. Paya, R. Jover, C. Alenda, L. Tito, M. Martinez-Villacampa, A. Vilella, R.M. Xicola, E. Pons, X. Llor A prospective, multicenter, population-based study of BRAF mutational analysis for Lynch syndrome screening Clin Gastroenterol Hepatol 6 2008 206 214
76. H. Nakagawa, T. Nagasaka, H.M. Cullings, K. Notohara, N. Hoshijima, J. Young, H.T. Lynch, N. Tanaka, N. Matsubara Efficient molecular screening of Lynch syndrome by specific 3′ promoter methylation of the MLH1 or BRAF mutation in colorectal cancer with high-frequency microsatellite instability Oncol Rep 21 2009 1577 1583
77. M.J. O'Brien, S. Yang, C. Mack, H. Xu, C.S. Huang, E. Mulcahy, M. Amorosino, F.A. Farraye 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 30 2006 1491 1501 (Pubitemid 44808785)
78. P. Minoo, K. Baker, R. Goswami, G. Chong, W.D. Foulkes, A.R. Ruszkiewicz, M. Barker, D. Buchanan, J. Young, J.R. Jass Extensive DNA methylation in normal colorectal mucosa in hyperplastic polyposis Gut 55 2006 1467 1474 (Pubitemid 44476793)
79. N. Tanaka, C. Huttenhower, K. Nosho, Y. Baba, K. Shima, J. Quackenbush, K.M. Haigis, E. Giovannucci, C.S. Fuchs, S. Ogino Novel application of structural equation modeling to correlation structure analysis of CpG island methylation in colorectal cancer Am J Pathol 177 2010 2731 2740
80. T. Hinoue, D.J. Weisenberger, F. Pan, M. Campan, M. Kim, J. Young, V.L. Whitehall, B.A. Leggett, P.W. Laird Analysis of the association between CIMP and BRAF in colorectal cancer by DNA methylation profiling PLoS One 4 2009 e8357
81. D.J. Weisenberger, K.D. Siegmund, M. Campan, J. Young, T.I. Long, M.A. Faasse, G.H. Kang, M. Widschwendter, D. Weener, D. Buchanan, H. Koh, L. Simms, M. Barker, B. Leggett, J. Levine, M. Kim, A.J. French, S.N. Thibodeau, J. Jass, R. Haile, P.W. Laird CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer Nat Genet 38 2006 787 793 (Pubitemid 43980599)
82. H.T. Lynch, A. de la Chapelle Hereditary colorectal cancer N Engl J Med 348 2003 919 932 (Pubitemid 36298000)
83. R.A. Barnetson, A. Tenesa, S.M. Farrington, I.D. Nicholl, R. Cetnarskyj, M.E. Porteous, H. Campbell, M.G. Dunlop Identification and survival of carriers of mutations in DNA mismatch-repair genes in colon cancer N Engl J Med 354 2006 2751 2763 (Pubitemid 43974193)
84. H.F. Vasen, G. Moslein, A. Alonso, I. Bernstein, L. Bertario, I. Blanco, J. Burn, G. Capella, C. Engel, I. Frayling, W. Friedl, F.J. Hes, S. Hodgson, J.P. Mecklin, P. Moller, F. Nagengast, Y. Parc, L. Renkonen-Sinisalo, J.R. Sampson, A. Stormorken, J. Wijnen Guidelines for the clinical management of Lynch syndrome (hereditary non-polyposis cancer) J Med Genet 44 2007 353 362 (Pubitemid 46953715)
85. G.E. Palomaki, M.R. McClain, S. Melillo, H.L. Hampel, S.N. Thibodeau EGAPP supplementary evidence review: dNA testing strategies aimed at reducing morbidity and mortality from Lynch syndrome Genet Med 11 2009 42 65
86. J. Wijnen, H. van der Klift, H. Vasen, P.M. Khan, F. Menko, C. Tops, H. Meijers Heijboer, D. Lindhout, P. Moller, R. Fodde MSH2 genomic deletions are a frequent cause of HNPCC Nat Genet 20 1998 326 328 (Pubitemid 28541626)
87. C.F. Taylor, R.S. Charlton, J. Burn, E. Sheridan, G.R. Taylor Genomic deletions in MSH2 or MLH1 are a frequent cause of hereditary non-polyposis colorectal cancer: identification of novel and recurrent deletions by MLPA Hum Mutat 22 2003 428 433 (Pubitemid 38009945)
88. F. Kastrinos, E.M. Stoffel, J. Balmana, E.W. Steyerberg, R. Mercado, S. Syngal Phenotype comparison of MLH1 and MSH2 mutation carriers in a cohort of 1,914 individuals undergoing clinical genetic testing in the United States Cancer Epidemiol Biomarkers Prev 17 2008 2044 2051
89. A.E. de Jong, F.M. Nagengast, J.H. Kleibeuker, P.C. van de Meeberg, H.J. van Wijk, A. Cats, G. Griffioen, H.F. Vasen What is the appropriate screening protocol in Lynch syndrome? Fam Cancer 5 2006 373 378 (Pubitemid 44924114)
90. M. Aarnio, J.P. Mecklin, L.A. Aaltonen, M. Nystrom-Lahti, H.J. Jarvinen Life-time risk of different cancers in hereditary non-polyposis colorectal cancer (HNPCC) syndrome Int J Cancer 64 1995 430 433 (Pubitemid 26048907)
91. E. Barrow, W. Alduaij, L. Robinson, A. Shenton, T. Clancy, F. Lalloo, J. Hill, D.G. Evans Colorectal cancer in HNPCC: cumulative lifetime incidence, survival and tumour distribution: A report of 121 families with proven mutations Clin Genet 74 2008 233 242
92. V. Bonadona, B. Bonaiti, S. Olschwang, S. Grandjouan, L. Huiart, M. Longy, R. Guimbaud, B. Buecher, Y.J. Bignon, O. Caron, C. Colas, C. Nogues, S. Lejeune-Dumoulin, L. Olivier-Faivre, F. Polycarpe-Osaer, T.D. Nguyen, F. Desseigne, J.C. Saurin, P. Berthet, D. Leroux, J. Duffour, S. Manouvrier, T. Frebourg, H. Sobol, C. Lasset, C. Bonaiti-Pellie Cancer risks associated with germline mutations in MLH1 MSH2, and MSH6 genes in Lynch syndrome JAMA 305 2011 2304 2310
93. R. Salovaara, A. Loukola, P. Kristo, H. Kaariainen, H. Ahtola, M. Eskelinen, N. Harkonen, R. Julkunen, E. Kangas, S. Ojala, J. Tulikoura, E. Valkamo, H. Jarvinen, J.P. Mecklin, L.A. Aaltonen, A. de LA Chapelle Population-based molecular detection of hereditary nonpolyposis colorectal cancer J Clin Oncol 18 2000 2193 2200 (Pubitemid 30350210)
94. S. Tuupanen, A. Karhu, H. Jarvinen, J.P. Mecklin, V. Launonen, L.A. Aaltonen No evidence for dual role of loss of heterozygosity in hereditary non-polyposis colorectal cancer Oncogene 26 2007 2513 2517 (Pubitemid 46597268)
95. C. Engel, J. Forberg, E. Holinski-Feder, C. Pagenstecher, J. Plaschke, M. Kloor, C. Poremba, C.P. Pox, J. Ruschoff, G. Keller, W. Dietmaier, P. Rummele, N. Friedrichs, E. Mangold, R. Buettner, H.K. Schackert, P. Kienle, S. Stemmler, G. Moeslein, M. Loeffler Novel strategy for optimal sequential application of clinical criteria, immunohistochemistry and microsatellite analysis in the diagnosis of hereditary nonpolyposis colorectal cancer Int J Cancer 118 2006 115 122 (Pubitemid 41681587)
96. S. Ollila, D. Dermadi Bebek, J. Jiricny, M. Nystrom Mechanisms of pathogenicity in human MSH2 missense mutants Hum Mutat 29 2008 1355 1363
97. L.I. Overbeek, M.J. Ligtenberg, R.W. Willems, R.P. Hermens, W.A. Blokx, S.V. Dubois, H. van der Linden, J.W. Meijer, M.L. Mlynek-Kersjes, N. Hoogerbrugge, K.M. Hebeda, J.H. van Krieken Interpretation of immunohistochemistry for mismatch repair proteins is only reliable in a specialized setting Am J Surg Pathol 32 2008 1246 1251
98. J. Shia 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 2008 293 300 (Pubitemid 352019113)
99. H.J. Jarvinen, L. Renkonen-Sinisalo, K. Aktan-Collan, P. Peltomaki, L.A. Aaltonen, J.P. Mecklin Ten years after mutation testing for Lynch syndrome: cancer incidence and outcome in mutation-positive and mutation-negative family members J Clin Oncol 27 2009 4793 4797
100. H.F. Vasen, M. van Ballegooijen, E. Buskens, J.K. Kleibeuker, B.G. Taal, G. Griffioen, F.M. Nagengast, F.H. Menko, P. Meera Khan A cost-effectiveness analysis of colorectal screening of hereditary nonpolyposis colorectal carcinoma gene carriers Cancer 82 1998 1632 1637 (Pubitemid 28208910)
101. H.J. Jarvinen, M. Aarnio, H. Mustonen, K. Aktan-Collan, L.A. Aaltonen, P. Peltomaki, A. De LA Chapelle, J.P. Mecklin Controlled 15-year trial on screening for colorectal cancer in families with hereditary nonpolyposis colorectal cancer Gastroenterology 118 2000 829 834 (Pubitemid 30243745)
102. J. Shia, L.H. Tang, E. Vakiani, J.G. Guillem, Z.K. Stadler, R.A. Soslow, N. Katabi, M.R. Weiser, P.B. Paty, L.K. Temple, G.M. Nash, W.D. Wong, K. Offit, D.S. Klimstra Immunohistochemistry as first-line screening for detecting colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome: a 2-antibody panel may be as predictive as a 4-antibody panel Am J Surg Pathol 33 2009 1639 1645
103. A. Goel, C.N. Arnold, D. Niedzwiecki, D.K. Chang, L. Ricciardiello, J.M. Carethers, J.M. Dowell, L. Wasserman, C. Compton, R.J. Mayer, M.M. Bertagnolli, C.R. Boland Characterization of sporadic colon cancer by patterns of genomic instability Cancer Res 63 2003 1608 1614 (Pubitemid 36373651)
104. S.M. Woerner, A. Benner, C. Sutter, M. Schiller, Y.P. Yuan, G. Keller, P. Bork, M.K. Doeberitz, J.F. Gebert Pathogenesis of DNA repair-deficient cancers: a statistical meta-analysis of putative Real Common Target genes Oncogene 22 2003 2226 2235 (Pubitemid 36566779)
105. H. Iino, J.R. Jass, L.A. Simms, J. Young, B. Leggett, Y. Ajioka, H. Watanabe DNA microsatellite instability in hyperplastic polyps, serrated adenomas, and mixed polyps: a mild mutator pathway for colorectal cancer? J Clin Pathol 52 1999 5 9 (Pubitemid 29023500)
106. H. Iino, L. Simms, J. Young, J. Arnold, I.M. Winship, S.I. Webb, K.L. Furlong, B. Leggett, J.R. Jass DNA microsatellite instability and mismatch repair protein loss in adenomas presenting in hereditary non-polyposis colorectal cancer Gut 47 2000 37 42 (Pubitemid 30430409)
107. A. Gologan, A. Krasinskas, J. Hunt, D.L. Thull, L. Farkas, A.R. Sepulveda Performance of the revised Bethesda guidelines for identification of colorectal carcinomas with a high level of microsatellite instability Arch Pathol Lab Med 129 2005 1390 1397 (Pubitemid 41587011)
108. J.K. Greenson, S.C. Huang, C. Herron, V. Moreno, J.D. Bonner, L.P. Tomsho, O. Ben-Izhak, H.I. Cohen, P. Trougouboff, J. Bejhar, Y. Sova, M. Pinchev, G. Rennert, S.B. Gruber Pathologic predictors of microsatellite instability in colorectal cancer Am J Surg Pathol 33 2009 126 133
109. Y. Schwitalle, M. Kloor, S. Eiermann, M. Linnebacher, P. Kienle, H.P. Knaebel, M. Tariverdian, A. Benner, M. von Knebel Doeberitz Immune response against frameshift-induced neopeptides in HNPCC patients and healthy HNPCC mutation carriers Gastroenterology 134 2008 988 997 (Pubitemid 351459601)
110. F.M. Speetjens, P.J. Kuppen, H. Morreau, S.H. van der Burg Immune response against frameshift-induced neopeptides in HNPCC patients and healthy HNPCC mutation carriers Gastroenterology 135 2008 711 712
111. S. Lee, N.Y. Cho, M. Choi, E.J. Yoo, J.H. Kim, G.H. Kang Clinicopathological features of CpG island methylator phenotype-positive colorectal cancer and its adverse prognosis in relation to KRAS/BRAF mutation Pathol Int 58 2008 104 113
112. J.H. Kim, S.H. Shin, H.J. Kwon, N.Y. Cho, G.H. Kang Prognostic implications of CpG island hypermethylator phenotype in colorectal cancers Virchows Arch 455 2009 485 494
113. W.S. Samowitz, C. Sweeney, J. Herrick, H. Albertsen, T.R. Levin, M.A. Murtaugh, R.K. Wolff, M.L. Slattery Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers Cancer Res 65 2005 6063 6069
114. A.M. Dahlin, R. Palmqvist, M.L. Henriksson, M. Jacobsson, V. Eklof, J. Rutegard, A. Oberg, B.R. Van Guelpen The role of the CpG island methylator phenotype in colorectal cancer prognosis depends on microsatellite instability screening status Clin Cancer Res 16 2010 1845 1855
115. M.A. Jenkins, S. Hayashi, A.M. O'Shea, L.J. Burgart, T.C. Smyrk, D. Shimizu, P.M. Waring, A.R. Ruszkiewicz, A.F. Pollett, M. Redston, M.A. Barker, J.A. Baron, G.R. Casey, J.G. Dowty, G.G. Giles, P. Limburg, P. Newcomb, J.P. Young, M.D. Walsh, S.N. Thibodeau, N.M. Lindor, L. Lemarchand, S. Gallinger, R.W. Haile, J.D. Potter, J.L. Hopper, J.R. Jass Pathology features in Bethesda guidelines predict colorectal cancer microsatellite instability: a population-based study Gastroenterology 133 2007 48 56 (Pubitemid 47039240)
116. H. Hampel, W.L. Frankel, E. Martin, M. Arnold, K. Khanduja, P. Kuebler, H. Nakagawa, K. Sotamaa, T.W. Prior, J. Westman, J. Panescu, D. Fix, J. Lockman, I. Comeras, A. de la Chapelle Screening for the Lynch syndrome (hereditary nonpolyposis colorectal cancer) N Engl J Med 352 2005 1851 1860
117. T. Debniak, G. Kurzawski, B. Gorski, J. Kladny, W. Domagala, J. Lubinski Value of pedigree/clinical data, immunohistochemistry and microsatellite instability analyses in reducing the cost of determining hMLH1 and hMSH2 gene mutations in patients with colorectal cancer Eur J Cancer 36 2000 49 54 (Pubitemid 30035343)
118. V. Pinol, A. Castells, M. Andreu, S. Castellvi-Bel, C. Alenda, X. Llor, R.M. Xicola, F. Rodriguez-Moranta, A. Paya, R. Jover, X. Bessa Accuracy of revised Bethesda guidelines, microsatellite instability, and immunohistochemistry for the identification of patients with hereditary nonpolyposis colorectal cancer JAMA 293 2005 1986 1994 (Pubitemid 40570892)
119. M. Cicek, N. Lindor, S. Gallinger, B. Bapat, J. Hopper, M. Jenkins, J. Young, D. Buchanan, M. Walsh, L. Le Marchand, T. Burnett, P. Newcomb, W. Grady, R. Haile, G. Casey, S. Plummer, L. Krumroy, J. Baron, S. Thibodeau Quality assessment and correlation of MSI and IHC markers among population- and clinic-based colorectal tumors J Mol Diagn 13 2011 271 281
120. H.F. Vasen, P. Watson, J.P. Mecklin, H.T. Lynch New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC Lynch syndrome) proposed by the International Collaborative Group on HNPCC Gastroenterology 116 1999 1453 1456 (Pubitemid 29258894)
121. M.C. Southey, M.A. Jenkins, L. Mead, J. Whitty, M. Trivett, A.A. Tesoriero, L.D. Smith, K. Jennings, G. Grubb, S.G. Royce, M.D. Walsh, M.A. Barker, J.P. Young, J.R. Jass, D.J. St John, F.A. Macrae, G.G. Giles, J.L. Hopper Use of molecular tumor characteristics to prioritize mismatch repair gene testing in early-onset colorectal cancer J Clin Oncol 23 2005 6524 6532 (Pubitemid 46190244)
122. A. Umar, C.R. Boland, J.P. Terdiman, S. Syngal, A. de la Chapelle, J. Ruschoff, R. Fishel, N.M. Lindor, L.J. Burgart, R. Hamelin, S.R. Hamilton, R.A. Hiatt, J. Jass, A. Lindblom, H.T. Lynch, P. Peltomaki, S.D. Ramsey, M.A. Rodriguez-Bigas, H.F. Vasen, E.T. Hawk, J.C. Barrett, A.N. Freedman, S. Srivastava Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability J Natl Cancer Inst 96 2004 261 268 (Pubitemid 38256271)
123. V. Bansal, R. Tewhey, E.M. Leproust, N.J. Schork Efficient and cost effective population resequencing by pooling and in-solution hybridization PLoS One 6 2011 e18353
124. M. Mvundura, S.D. Grosse, H. Hampel, G.E. Palomaki The cost-effectiveness of genetic testing strategies for Lynch syndrome among newly diagnosed patients with colorectal cancer Genet Med 12 2010 93 104
125. National Comprehensive Cancer Network: NCCN Clinical Practice Guidelines in Oncology: Colorectal Cancer Screening Version 2.2011 2010 National Comprehensive Cancer Network Rockledge, PA LS-1 http://www.nccn.org/ professionals/physician-gls/pdf/colorectal-screening.pdf Accessed September 17, 2011
126. D.K. Rex, D.A. Johnson, J.C. Anderson, P.S. Schoenfeld, C.A. Burke, J.M. Inadomi American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected] Am J Gastroenterol 104 2009 739 750
127. N.M. Lindor, G.M. Petersen, D.W. Hadley, A.Y. Kinney, S. Miesfeldt, K.H. Lu, P. Lynch, W. Burke, N. Press Recommendations for the care of individuals with an inherited predisposition to Lynch syndrome: a systematic review JAMA 296 2006 1507 1517 (Pubitemid 44465515)
128. Z. Gatalica, E. Torlakovic Pathology of the hereditary colorectal carcinoma Fam Cancer 7 2008 15 26
129. U. Ladabaum, G. Wang, J. Terdiman, A. Blanco, M. Kuppermann, C.R. Boland, J. Ford, E. Elkin, K.A. Phillips Strategies to identify the Lynch syndrome among patients with colorectal cancer: a cost-effectiveness analysis Ann Intern Med 155 2011 69 79