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[Cancer Research 58, 5248-5257, November 15, 1998]
© 1998 American Association for Cancer Research
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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

C. Richard Boland1, Stephen N. Thibodeau, Stanley R. Hamilton, David Sidransky, James R. Eshleman, Randall W. Burt, Stephen J. Meltzer, Miguel A. Rodriguez-Bigas, Riccardo Fodde, G. Nadia Ranzani and Sudhir Srivastava2

University of California, San Diego, La Jolla, California 92093-0688 [C. R. B.]; Molecular Genetics Laboratory, Mayo Clinic, Rochester, Minnesota 55905 [S. N. T.]; School of Medicine [S. R. H., J. R. E.] and Head & Neck Cancer Research [D. S.], Johns Hopkins University, Baltimore, Maryland 21205-2196; University of Utah Health Sciences Center, Salt Lake City, Utah 84132 [R. W. B.]; University of Maryland Hospital, Baltimore, Maryland 21201 [S. J. M.]; Department of Surgery, Roswell Park Cancer Institute, Buffalo, New York 14263 [M. A. R-B.]; Department of Human Genetics, Leiden University, Leiden AL 2333, the Netherlands [R. F.]; Department of Genetics and Microbiology, University of Pavia, 27100 Pavia, Italy [G. N. R.]; and Division of Cancer Prevention, National Cancer Institute, Bethesda, Maryland 20892-7346 [S. S.]

In December 1997, the National Cancer Institute sponsored "The International Workshop on Microsatellite Instability and RER Phenotypes in Cancer Detection and Familial Predisposition," to review and unify the field. The following recommendations were endorsed at the workshop. (a) The form of genomic instability associated with defective DNA mismatch repair in tumors is to be called microsatellite instability (MSI). (b) A panel of five microsatellites has been validated and is recommended as a reference panel for future research in the field. Tumors may be characterized on the basis of: high-frequency MSI (MSI-H), if two or more of the five markers show instability (i.e., have insertion/deletion mutations), and low-frequency MSI (MSI-L), if only one of the five markers shows instability. The distinction between microsatellite stable (MSS) and low frequency MSI (MSI-L) can only be accomplished if a greater number of markers is utilized. (c) A unique clinical and pathological phenotype is identified for the MSI-H tumors, which comprise ~15% of colorectal cancers, whereas MSI-L and MSS tumors appear to be phenotypically similar. MSI-H colorectal tumors are found predominantly in the proximal colon, have unique histopathological features, and are associated with a less aggressive clinical course than are stage-matched MSI-L or MSS tumors. Preclinical models suggest the possibility that these tumors may be resistant to the cytotoxicity induced by certain chemotherapeutic agents. The implications for MSI-L are not yet clear. (d) MSI can be measured in fresh or fixed tumor specimens equally well; microdissection of pathological specimens is recommended to enrich for neoplastic tissue; and normal tissue is required to document the presence of MSI. (e) The "Bethesda guidelines," which were developed in 1996 to assist in the selection of tumors for microsatellite analysis, are endorsed. (f) The spectrum of microsatellite alterations in noncolonic tumors was reviewed, and it was concluded that the above recommendations apply only to colorectal neoplasms. (g) A research agenda was recommended.

1 To whom correspondence should be addressed, at University of California, San Diego, 4028 BSB, 9500 Gilman Drive, La Jolla, CA 92093-0688. E-mail: crboland@ucsd.edu.

2 To whom requests for reprints should be addressed, at EPN-330F, 6130 Executive Blvd., NCl, NIH, Bethesda, MD 20892.

Received 2/26/98. Accepted 9/ 9/98.




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 CarcinogenesisHome page
M. Mrkonjic, S. Raptis, R. C. Green, N. Monga, D. Daftary, E. Dicks, H.B. Younghusband, P. S. Parfrey, S. S. Gallinger, J. R. McLaughlin, et al.
MSH2 118T>C and MSH6 159C>T promoter polymorphisms and the risk of colorectal cancer
Carcinogenesis, December 1, 2007; 28(12): 2575 - 2580.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. A. McIlhatton, J. Tyler, S. Burkholder, J. Ruschoff, B. Rigas, L. Kopelovich, and R. Fishel
Nitric Oxide Donating Aspirin Derivatives Suppress Microsatellite Instability in Mismatch Repair Deficient and Hereditary Nonpolyposis Colorectal Cancer Cells
Cancer Res., November 15, 2007; 67(22): 10966 - 10975.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
A. Broniscer, S. Gururangan, T. J. MacDonald, S. Goldman, R. J. Packer, C. F. Stewart, D. Wallace, M. K. Danks, H. S. Friedman, T. Y. Poussaint, et al.
Phase I Trial of Single-Dose Temozolomide and Continuous Administration of O6-Benzylguanine in Children with Brain Tumors: a Pediatric Brain Tumor Consortium Report
Clin. Cancer Res., November 15, 2007; 13(22): 6712 - 6718.
[Abstract] [Full Text] [PDF]

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 JCOHome page
T. M. Horton, P. A. Thompson, S. L. Berg, P. C. Adamson, A. M. Ingle, M. E. Dolan, S. M. Delaney, M. Hedge, H. L. Weiss, M.-F. Wu, et al.
Phase I Pharmacokinetic and Pharmacodynamic Study of Temozolomide in Pediatric Patients With Refractory or Recurrent Leukemia: A Children's Oncology Group Study
J. Clin. Oncol., November 1, 2007; 25(31): 4922 - 4928.
[Abstract] [Full Text] [PDF]

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 Cancer Epidemiol. Biomarkers Prev.Home page
L. A. Boardman, A. P. Lanier, A. J. French, K. V. Schowalter, L. J. Burgart, K. R. Koller, S. K. McDonnell, D. J. Schaid, and S. N. Thibodeau
Frequency of Defective DNA Mismatch Repair in Colorectal Cancer among the Alaska Native People
Cancer Epidemiol. Biomarkers Prev., November 1, 2007; 16(11): 2344 - 2350.
[Abstract] [Full Text] [PDF]

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 Cancer Epidemiol. Biomarkers Prev.Home page
P. A. Newcomb, J. Baron, M. Cotterchio, S. Gallinger, J. Grove, R. Haile, D. Hall, J. L. Hopper, J. Jass, L. Le Marchand, et al.
Colon Cancer Family Registry: An International Resource for Studies of the Genetic Epidemiology of Colon Cancer
Cancer Epidemiol. Biomarkers Prev., November 1, 2007; 16(11): 2331 - 2343.
[Abstract] [Full Text] [PDF]

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 GutHome page
S. Ogino, T. Kawasaki, G. J Kirkner, Y. Suemoto, J. A Meyerhardt, and C. S Fuchs
Molecular correlates with MGMT promoter methylation and silencing support CpG island methylator phenotype-low (CIMP-low) in colorectal cancer
Gut, November 1, 2007; 56(11): 1564 - 1571.
[Abstract] [Full Text] [PDF]

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 Genes Dev.Home page
A. K. Rustgi
The genetics of hereditary colon cancer
Genes & Dev., October 15, 2007; 21(20): 2525 - 2538.
[Abstract] [Full Text] [PDF]

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 JCOHome page
M. Svrcek, J. El-Bchiri, A. Chalastanis, E. Capel, S. Dumont, O. Buhard, C. Oliveira, R. Seruca, C. Bossard, J.-F. Mosnier, et al.
Specific Clinical and Biological Features Characterize Inflammatory Bowel Disease Associated Colorectal Cancers Showing Microsatellite Instability
J. Clin. Oncol., September 20, 2007; 25(27): 4231 - 4238.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
S. Ogino, A. Hazra, G. J. Tranah, G. J. Kirkner, T. Kawasaki, K. Nosho, M. Ohnishi, Y. Suemoto, J. A. Meyerhardt, D. J. Hunter, et al.
MGMT germline polymorphism is associated with somatic MGMT promoter methylation and gene silencing in colorectal cancer
Carcinogenesis, September 1, 2007; 28(9): 1985 - 1990.
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H. T. Lynch, C. R. Boland, M. A. Rodriguez-Bigas, C. Amos, J. F. Lynch, and P. M. Lynch
Who Should Be Sent for Genetic Testing in Hereditary Colorectal Cancer Syndromes?
J. Clin. Oncol., August 10, 2007; 25(23): 3534 - 3542.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
P. A. Newcomb, Y. Zheng, V. M. Chia, L. M. Morimoto, V. P. Doria-Rose, A. Templeton, S. N. Thibodeau, and J. D. Potter
Estrogen Plus Progestin Use, Microsatellite Instability, and the Risk of Colorectal Cancer in Women
Cancer Res., August 1, 2007; 67(15): 7534 - 7539.
[Abstract] [Full Text] [PDF]

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 INT J SURG PATHOLHome page
N. Khilko, P. Bourne, Qi Yang, and Ping Tang
Mismatch Repair Genes hMLH1 and hMSH2 May Not Play an Essential Role in Breast Carcinogenesis
International Journal of Surgical Pathology, July 1, 2007; 15(3): 233 - 241.
[Abstract] [PDF]

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 J. Clin. Pathol.Home page
E R Nijhuis, H W Nijman, K A Oien, A Bell, K A ten Hoor, N Reesink-Peters, H M Boezen, H Hollema, and A G J van der Zee
Loss of MSH2 protein expression is a risk factor in early stage cervical cancer
J. Clin. Pathol., July 1, 2007; 60(7): 824 - 830.
[Abstract] [Full Text] [PDF]

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 GutHome page
A Gylling, W M Abdel-Rahman, M Juhola, K Nuorva, E Hautala, H J Jarvinen, J-P Mecklin, M Aarnio, and P Peltomaki
Is gastric cancer part of the tumour spectrum of hereditary non-polyposis colorectal cancer? A molecular genetic study
Gut, July 1, 2007; 56(7): 926 - 933.
[Abstract] [Full Text] [PDF]

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 J. Mol. Diagn.Home page
S. Ogino, T. Kawasaki, G. J. Kirkner, P. Kraft, M. Loda, and C. S. Fuchs
Evaluation of Markers for CpG Island Methylator Phenotype (CIMP) in Colorectal Cancer by a Large Population-Based Sample
J. Mol. Diagn., July 1, 2007; 9(3): 305 - 314.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
A. Malesci, L. Laghi, P. Bianchi, G. Delconte, A. Randolph, V. Torri, C. Carnaghi, R. Doci, R. Rosati, M. Montorsi, et al.
Reduced Likelihood of Metastases in Patients with Microsatellite-Unstable Colorectal Cancer
Clin. Cancer Res., July 1, 2007; 13(13): 3831 - 3839.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Sammalkorpi, P. Alhopuro, R. Lehtonen, J. Tuimala, J.-P. Mecklin, H. J. Jarvinen, J. Jiricny, A. Karhu, and L. A. Aaltonen
Background Mutation Frequency in Microsatellite-Unstable Colorectal Cancer
Cancer Res., June 15, 2007; 67(12): 5691 - 5698.
[Abstract] [Full Text] [PDF]

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P. J. O'Dwyer, S. G. Eckhardt, D. G. Haller, J. Tepper, D. Ahnen, S. Hamilton, A. B. Benson III, M. Rothenberg, N. Petrelli, H.-J. Lenz, et al.
Priorities in Colorectal Cancer Research: Recommendations From the Gastrointestinal Scientific Leadership Council of the Coalition of Cancer Cooperative Groups
J. Clin. Oncol., June 1, 2007; 25(16): 2313 - 2321.
[Abstract] [Full Text] [PDF]

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 J. Clin. Pathol.Home page
Y. Kazama, T. Watanabe, T. Kanazawa, J. Tanaka, T. Tanaka, and H. Nagawa
Microsatellite instability in poorly differentiated adenocarcinomas of the colon and rectum: relationship to clinicopathological features
J. Clin. Pathol., June 1, 2007; 60(6): 701 - 704.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
K. Nosho, H. Yamamoto, T. Takahashi, M. Mikami, H. Taniguchi, N. Miyamoto, Y. Adachi, Y. Arimura, F. Itoh, K. Imai, et al.
Genetic and epigenetic profiling in early colorectal tumors and prediction of invasive potential in pT1 (early invasive) colorectal cancers
Carcinogenesis, June 1, 2007; 28(6): 1364 - 1370.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. Bettstetter, S. Dechant, P. Ruemmele, M. Grabowski, G. Keller, E. Holinski-Feder, A. Hartmann, F. Hofstaedter, and W. Dietmaier
Distinction of Hereditary Nonpolyposis Colorectal Cancer and Sporadic Microsatellite-Unstable Colorectal Cancer through Quantification of MLH1 Methylation by Real-time PCR
Clin. Cancer Res., June 1, 2007; 13(11): 3221 - 3228.
[Abstract] [Full Text] [PDF]

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 J. Med. Genet.Home page
H F A Vasen, G Moslein, A Alonso, I Bernstein, L Bertario, I Blanco, J Burn, G Capella, C Engel, I Frayling, et al.
Guidelines for the clinical management of Lynch syndrome (hereditary non-polyposis cancer)
J. Med. Genet., June 1, 2007; 44(6): 353 - 362.
[Abstract] [Full Text] [PDF]

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 JCOHome page
I. Zighelboim, P. J. Goodfellow, F. Gao, R. K. Gibb, M. A. Powell, J. S. Rader, and D. G. Mutch
Microsatellite Instability and Epigenetic Inactivation of MLH1 and Outcome of Patients With Endometrial Carcinomas of the Endometrioid Type
J. Clin. Oncol., May 20, 2007; 25(15): 2042 - 2048.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
L. J. Mead, M. A. Jenkins, J. Young, S. G. Royce, L. Smith, D. J. B. St. John, F. Macrae, G. G. Giles, J. L. Hopper, and M. C. Southey
Microsatellite Instability Markers for Identifying Early-Onset Colorectal Cancers Caused by Germ-Line Mutations in DNA Mismatch Repair Genes
Clin. Cancer Res., May 15, 2007; 13(10): 2865 - 2869.
[Abstract] [Full Text] [PDF]

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D. W. Rosenberg, S. Yang, D. C. Pleau, E. J. Greenspan, R. G. Stevens, T. V. Rajan, C. D. Heinen, J. Levine, Y. Zhou, and M. J. O'Brien
Mutations in BRAF and KRAS Differentially Distinguish Serrated versus Non-Serrated Hyperplastic Aberrant Crypt Foci in Humans
Cancer Res., April 15, 2007; 67(8): 3551 - 3554.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
E. J. Greenspan, J. L. Cyr, D. C. Pleau, J. Levine, T. V. Rajan, D. W. Rosenberg, and C. D. Heinen
Microsatellite instability in aberrant crypt foci from patients without concurrent colon cancer
Carcinogenesis, April 1, 2007; 28(4): 769 - 776.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
S. Raptis, M. Mrkonjic, R. C. Green, V. V. Pethe, N. Monga, Y. M. Chan, D. Daftary, E. Dicks, B. H. Younghusband, P. S. Parfrey, et al.
MLH1 -93G>A Promoter Polymorphism and the Risk of Microsatellite-Unstable Colorectal Cancer
J Natl Cancer Inst, March 21, 2007; 99(6): 463 - 474.
[Abstract] [Full Text] [PDF]

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 JCOHome page
S. L. Cossio, P. Ashton-Prolla, M.-C. Bortolini, R. S. Coura, R. Giugliani, and J. C. Prolla
Microsatellite Instability Testing in Genetically Heterogeneous Populations
J. Clin. Oncol., March 1, 2007; 25(7): 913 - 914.
[Full Text] [PDF]

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G. P. Kim, L. H. Colangelo, H. S. Wieand, S. Paik, I. R. Kirsch, N. Wolmark, and C. J. Allegra
Prognostic and Predictive Roles of High-Degree Microsatellite Instability in Colon Cancer: A National Cancer Institute-National Surgical Adjuvant Breast and Bowel Project Collaborative Study
J. Clin. Oncol., March 1, 2007; 25(7): 767 - 772.
[Abstract] [Full Text] [PDF]

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L. Valle, J. Perea, P. Carbonell, V. Fernandez, A. M. Dotor, J. Benitez, and M. Urioste
Clinicopathologic and Pedigree Differences in Amsterdam I-Positive Hereditary Nonpolyposis Colorectal Cancer Families According to Tumor Microsatellite Instability Status
J. Clin. Oncol., March 1, 2007; 25(7): 781 - 786.
[Abstract] [Full Text] [PDF]

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 JCOHome page
C. R. Boland
Clinical Uses of Microsatellite Instability Testing in Colorectal Cancer: An Ongoing Challenge
J. Clin. Oncol., March 1, 2007; 25(7): 754 - 756.
[Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
R. M. Xicola, X. Llor, E. Pons, A. Castells, C. Alenda, V. Pinol, M. Andreu, S. Castellvi-Bel, A. Paya, R. Jover, et al.
Performance of Different Microsatellite Marker Panels for Detection of Mismatch Repair-Deficient Colorectal Tumors
J Natl Cancer Inst, February 7, 2007; 99(3): 244 - 252.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
L. Aaltonen, L. Johns, H. Jarvinen, J.-P. Mecklin, and R. Houlston
Explaining the Familial Colorectal Cancer Risk Associated with Mismatch Repair (MMR)-Deficient and MMR-Stable Tumors
Clin. Cancer Res., January 1, 2007; 13(1): 356 - 361.
[Abstract] [Full Text] [PDF]

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 J. Med. Genet.Home page
H. Alazzouzi, G. Suriano, A. Guerra, A. Plaja, E. Espin, M. Armengol, P. Alhopuro, S. Velho, Y. Shinomura, J. J. Gonzalez-Aguilera, et al.
Tumour selection advantage of non-dominant negative P53 mutations in homozygotic MDM2-SNP309 colorectal cancer cells
J. Med. Genet., January 1, 2007; 44(1): 75 - 80.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
B. Brandt, S. Meyer-Staeckling, H. Schmidt, K. Agelopoulos, and H. Buerger
Mechanisms of egfr Gene Transcription Modulation: Relationship to Cancer Risk and Therapy Response
Clin. Cancer Res., December 15, 2006; 12(24): 7252 - 7260.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
W. S. Samowitz, H. Albertsen, C. Sweeney, J. Herrick, B. J. Caan, K. E. Anderson, R. K. Wolff, and M. L. Slattery
Association of Smoking, CpG Island Methylator Phenotype, and V600E BRAF Mutations in Colon Cancer
J Natl Cancer Inst, December 6, 2006; 98(23): 1731 - 1738.
[Abstract] [Full Text] [PDF]

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 GutHome page
R C Niessen, M J W Berends, Y Wu, R H Sijmons, H Hollema, M J L Ligtenberg, H E K de Walle, E G E de Vries, A Karrenbeld, C H C M Buys, et al.
Identification of mismatch repair gene mutations in young patients with colorectal cancer and in patients with multiple tumours associated with hereditary non-polyposis colorectal cancer
Gut, December 1, 2006; 55(12): 1781 - 1788.
[Abstract] [Full Text] [PDF]

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 JCOHome page
G. Y. Locker, S. Hamilton, J. Harris, J. M. Jessup, N. Kemeny, J. S. Macdonald, M. R. Somerfield, D. F. Hayes, and R. C. Bast Jr
ASCO 2006 Update of Recommendations for the Use of Tumor Markers in Gastrointestinal Cancer
J. Clin. Oncol., November 20, 2006; 24(33): 5313 - 5327.
[Abstract] [Full Text] [PDF]

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 Cancer Epidemiol. Biomarkers Prev.Home page
J. Vandrovcova, K. Lagerstedt-Robinsson, L. Pahlman, and A. Lindblom
Somatic BRAF-V600E Mutations in Familial Colorectal Cancer.
Cancer Epidemiol. Biomarkers Prev., November 1, 2006; 15(11): 2270 - 2273.
[Abstract] [Full Text] [PDF]

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 J. Mol. Diagn.Home page
S. Ogino, T. Kawasaki, G. J. Kirkner, M. Loda, and C. S. Fuchs
CpG Island Methylator Phenotype-Low (CIMP-Low) in Colorectal Cancer: Possible Associations with Male Sex and KRAS Mutations
J. Mol. Diagn., November 1, 2006; 8(5): 582 - 588.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
T. Watanabe, T. Kobunai, E. Toda, Y. Yamamoto, T. Kanazawa, Y. Kazama, J. Tanaka, T. Tanaka, T. Konishi, Y. Okayama, et al.
Distal Colorectal Cancers with Microsatellite Instability (MSI) Display Distinct Gene Expression Profiles that Are Different from Proximal MSI Cancers
Cancer Res., October 15, 2006; 66(20): 9804 - 9808.
[Abstract] [Full Text] [PDF]

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 J. Clin. Pathol.Home page
M Ebinger, K Sotlar, A Weber, C T Bock, B D Bultmann, and R Kandolf
Simplified detection of microsatellite instability in colorectal cancer without the need for corresponding germline DNA analysis.
J. Clin. Pathol., October 1, 2006; 59(10): 1114 - 1115.
[Abstract] [Full Text] [PDF]


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