Identifying lynch syndrome in patients with ovarian carcinoma: The significance of tumor subtype

Advances in Anatomic Pathology

Volumn 20, Issue 6, 2013, Pages 378-386

  Chui, Michael Herman ^a   Gilks, C Blake ^c   Cooper, Kumaresan ^d   Clarke, Blaise A ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b TORONTO GENERAL HOSPITAL   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

immunohistochemistry; Lynch syndrome; mismatch repair; ovarian cancer; reflex testing

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; MISMATCH REPAIR PROTEIN; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6;

AGE; CANCER STAGING; CLEAR CELL CARCINOMA; CLINICAL FEATURE; DISEASE ASSOCIATION; ENDOMETRIOID CARCINOMA; ENDOMETRIOSIS; ENDOMETRIUM CARCINOMA; GENE MUTATION; GENOTYPE; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; MICROSATELLITE INSTABILITY; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SAMPLE SIZE;

ADULT; AGED; COLORECTAL NEOPLASMS, HEREDITARY NONPOLYPOSIS; DNA MISMATCH REPAIR; FEMALE; HUMANS; MICROSATELLITE INSTABILITY; MIDDLE AGED; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS;

EID: 84886469620     PISSN: 10724109     EISSN: 15334031     Source Type: Journal    
DOI: 10.1097/PAP.0b013e3182a92cf8     Document Type: Review

References (60)

1. Beamer LC, Grant ML, Espenschied CR, et al. Reflex immunohistochemistry and microsatellite instability testing of colorectal tumors for Lynch syndrome among US cancer programs and follow-up of abnormal results. J Clin Oncol. 2012;30:1058-1063.
2. Boland CR, Shike M. Report from the Jerusalem workshop on Lynch syndrome-hereditary nonpolyposis colorectal cancer. Gastroenterology. 2010;138:2197.e1-2197.e7.
3. Clarke BA, Cooper K. Identifying Lynch syndrome in patients with endometrial carcinoma: shortcomings of morphologic and clinical schemas. Adv Anat Pathol. 2012;19:231-238.
4. Pal T, Permuth-Wey J, Sellers TA. A review of the clinical relevance of mismatch-repair deficiency in ovarian cancer. Cancer. 2008;113:733-742.
5. Lu KH, Dinh M, Kohlmann W, et al. Gynecologic cancer as a "sentinel cancer" for women with hereditary nonpolyposis colorectal cancer syndrome. Obstet Gynecol. 2005;105:569-574. (Pubitemid 40271224)
6. Schmeler KM, Lu KH. Gynecologic cancers associated with Lynch syndrome/HNPCC. Clin Transl Oncol. 2008;10: 313-317.
7. Ryan P, Mulligan AM, Aronson M, et al. Comparison of clinical schemas and morphologic features in predicting Lynch syndrome in mutation-positive patients with endometrial cancer encountered in the context of familial gastrointestinal cancer registries. Cancer. 2012;118:681-688.
8. de Leeuw WJ, Dierssen J, Vasen HF, et al. Prediction of a mismatch repair gene defect by microsatellite instability and immunohistochemical analysis in endometrial tumours from HNPCC patients. J Pathol. 2000;192:328-335.
9. Broaddus RR, Lynch HT, Chen LM, et al. Pathologic features of endometrial carcinoma associated with HNPCC: a comparison with sporadic endometrial carcinoma. Cancer. 2006;106:87-94. (Pubitemid 43032552)
10. Carcangiu ML, Radice P, Casalini P, et al. Lynch syndrome-related endometrial carcinomas show a high frequency of nonendometrioid types and of high FIGO grade endometrioid types. Int J Surg Pathol. 2010;18:21-26.
11. Lund B, Thomsen HK, Olsen J. Reproducibility of histopathological evaluation in epithelial ovarian carcinoma. Clinical implications. APMIS. 1991;99:353-358.
12. Cramer SF, Roth LM, Ulbright TM, et al. Evaluation of the reproducibility of the World Health Organization classification of common ovarian cancers. With emphasis on methodology. Arch Pathol Lab Med. 1987;111:819-829. (Pubitemid 17121987)
13. Kobel M, Kalloger SE, Baker PM, et al. Diagnosis of ovarian carcinoma cell type is highly reproducible: a transcanadian study. Am J Surg Pathol. 2010;34:984-993.
14. Press JZ, De Luca A, Boyd N, et al. Ovarian carcinomas with genetic and epigenetic BRCA1 loss have distinct molecular abnormalities. BMC Cancer. 2008;8:1471-2407.
15. Schrader KA, Hurlburt J, Kalloger SE, et al. Germline BRCA1 and BRCA2 mutations in ovarian cancer: utility of a histologybased referral strategy. Obstet Gynecol. 2012;120:235-240.
16. Pal T, Permuth-Wey J, Kumar A, et al. Systematic review and meta-analysis of ovarian cancers: estimation of microsatellitehigh frequency and characterization of mismatch repair deficient tumor histology. Clin Cancer Res. 2008;14:6847-6854.
17. Ketabi Z, Bartuma K, Bernstein I, et al. Ovarian cancer linked to Lynch syndrome typically presents as early-onset, nonserous epithelial tumors. Gynecol Oncol. 2011;121:462-465.
18. Plumb JA, Strathdee G, Sludden J, et al. Reversal of drug resistance in human tumor xenografts by 20-deoxy-5-azacytidine-induced demethylation of the hMLH1 gene promoter. Cancer Res. 2000;60:6039-6044.
19. Marcelis CL, van der Putten HW, Tops C, et al. Chemotherapy resistant ovarian cancer in carriers of an hMSH2 mutation? Fam Cancer. 2001;1:107-109. (Pubitemid 35221524)
20. Hampel H, Frankel WL, Martin E, et al. Screening for the Lynch syndrome (hereditary nonpolyposis colorectal cancer). N Engl J Med. 2005;352:1851-1860.
21. Lancaster JM, Powell CB, Kauff ND, et al. Society of Gynecologic Oncologists Education Committee statement on risk assessment for inherited gynecologic cancer predispositions. Gynecol Oncol. 2007;107:159-162. (Pubitemid 47575743)
22. Ryan P, Pollett A, Mulligan AM, et al. Ovarian tumors in lynch syndrome: genotype-phenotype correlation (abstract 1124). Mod Pathol. 2011;24:265A.
23. Kwon JS, Scott JL, Gilks CB, et al. Testing women with endometrial cancer to detect Lynch syndrome. J Clin Oncol. 2011;29:2247-2252.
24. Ladabaum U, Wang G, Terdiman J, et al. Strategies to identify the Lynch syndrome among patients with colorectal cancer: a cost-effectiveness analysis. Ann Intern Med. 2011;155:69-79.
25. Bewtra C, Watson P, Conway T, et al. Hereditary ovarian cancer: a clinicopathological study. Int J Gynecol Pathol. 1992;11:180-187.
26. Rubin SC, Blackwood MA, Bandera C, et al. BRCA1, BRCA2, and hereditary nonpolyposis colorectal cancer gene mutations in an unselected ovarian cancer population: relationship to family history and implications for genetic testing. Am J Obstet Gynecol. 1998;178:670-677. (Pubitemid 28196872)
27. Aarnio M, Sankila R, Pukkala E, et al. Cancer risk in mutation carriers of DNA-mismatch-repair genes. Int J Cancer. 1999;81: 214-218. (Pubitemid 29144749)
28. Ichikawa Y, Lemon SJ, Wang S, et al. Microsatellite instability and expression of MLH1 and MSH2 in normal and malignant endometrial and ovarian epithelium in hereditary nonpolyposis colorectal cancer family members. Cancer Genet Cytogenet. 1999;112:2-8. (Pubitemid 29425862)
29. Wu Y, Berends MJ, Mensink RG, et al. Association of hereditary nonpolyposis colorectal cancer-related tumors displaying low microsatellite instability with MSH6 germline mutations. Am J Hum Genet. 1999;65:1291-1298. (Pubitemid 30460379)
30. Brown GJ St, John DJ, Macrae FA, et al. Cancer risk in young women at risk of hereditary nonpolyposis colorectal cancer: implications for gynecologic surveillance. Gynecol Oncol. 2001; 80:346-349. (Pubitemid 32207533)
31. Watson P, Butzow R, Lynch HT, et al. The clinical features of ovarian cancer in hereditary nonpolyposis colorectal cancer. Gynecol Oncol. 2001;82:223-228. (Pubitemid 32730595)
32. Crijnen TE, Janssen-Heijnen ML, Gelderblom H, et al. Survival of patients with ovarian cancer due to a mismatch repair defect. Fam Cancer. 2005;4:301-305. (Pubitemid 41795805)
33. Vasen HF, Stormorken A, Menko FH, et al. MSH2 mutation carriers are at higher risk of cancer than MLH1 mutation carriers: a study of hereditary nonpolyposis colorectal cancer families. J Clin Oncol. 2001;19:4074-4080. (Pubitemid 32976695)
34. Suchy J, Kurzawski G, Jakubowska A, et al. Ovarian cancer of endometrioid type as part of the MSH6gene mutation phenotype. J Hum Genet. 2002;47:529-531. (Pubitemid 35238968)
35. Wagner A, Hendriks Y, Meijers-Heijboer EJ, et al. Atypical HNPCC owing to MSH6 germline mutations: analysis of a large Dutch pedigree. J Med Genet. 2001;38:318-322. (Pubitemid 32433985)
36. Malander S, Rambech E, Kristoffersson U, et al. The contribution of the hereditary nonpolyposis colorectal cancer syndrome to the development of ovarian cancer. Gynecol Oncol. 2006;101:238-243.
37. Cederquist K, Emanuelsson M,Wiklund F, et al. Two Swedish founder MSH6 mutations, one nonsense and one missense, conferring high cumulative risk of Lynch syndrome. Clin Genet. 2005;68:533-541. (Pubitemid 41748853)
38. Ramsoekh D, Wagner A, van Leerdam ME, et al. Cancer risk in MLH1, MSH2 and MSH6 mutation carriers; different risk profiles may influence clinical management. Hered Cancer Clin Pract. 2009;7:1897-4287.
39. Bonadona V, Bonaiti B, Olschwang S, et al. Cancer risks associated with germline mutations in MLH1, MSH2, and MSH6 genes in Lynch syndrome. JAMA. 2011;305:2304-2310.
40. Pal T, Akbari MR, Sun P, et al. Frequency of mutations in mismatch repair genes in a population-based study of women with ovarian cancer. Br J Cancer. 2012;107:1783-1790.
41. Engel C, Loeffler M, Steinke V, et al. Risks of less common cancers in proven mutation carriers with lynch syndrome. J Clin Oncol. 2012;30:4409-4415.
42. Stratton JF, Thompson D, Bobrow L, et al. The genetic epidemiology of early-onset epithelial ovarian cancer: a population-based study. Am J Hum Genet. 1999;65:1725-1732. (Pubitemid 30468686)
43. Kobel M, Kalloger SE, Huntsman DG, et al. Differences in tumor type in low-stage versus high-stage ovarian carcinomas. Int J Gynecol Pathol. 2010;29:203-211.
44. Howlader NNA, Krapcho M, Garshell J, et al. SEER Cancer Statistics Review, 1975-2010. Web site. Available at: http://seer.cancer.gov/csr/1975-2010/ . Accessed July 23, 2013.
45. Liu J, Albarracin CT, Chang KH, et al. Microsatellite instability and expression of hMLH1 and hMSH2 proteins in ovarian endometrioid cancer. Mod Pathol. 2004;17:75-80. (Pubitemid 41656455)
46. Cai KQ, Albarracin C, Rosen D, et al. Microsatellite instability and alteration of the expression of hMLH1 and hMSH2 in ovarian clear cell carcinoma. Hum Pathol. 2004;35: 552-559. (Pubitemid 38656938)
47. Rosen DG, Cai KQ, Luthra R, et al. Immunohistochemical staining of hMLH1 and hMSH2 reflects microsatellite instability status in ovarian carcinoma. Mod Pathol. 2006;19: 1414-1420. (Pubitemid 44624159)
48. Domanska K, Malander S, Masback A, et al. Ovarian cancer at young age: the contribution of mismatch-repair defects in a population-based series of epithelial ovarian cancer before age 40. Int J Gynecol Cancer. 2007;17:789-793. (Pubitemid 47063326)
49. Zhai QJ, Rosen DG, Lu K, et al. Loss of DNA mismatch repair protein hMSH6 in ovarian cancer is histotype-specific. Int J Clin Exp Pathol. 2008;1:502-509.
50. Jensen KC, Mariappan MR, Putcha GV, et al. Microsatellite instability and mismatch repair protein defects in ovarian epithelial neoplasms in patients 50 years of age and younger. Am J Surg Pathol. 2008;32:1029-1037.
51. Lu FI, Gilks CB, Mulligan AM, et al. Prevalence of loss of expression of DNA mismatch repair proteins in primary epithelial ovarian tumors. Int J Gynecol Pathol. 2012;31: 524-531.
52. Gras E, Catasus L, Arguelles R, et al. Microsatellite instability, MLH-1 promoter hypermethylation, and frameshift mutations at coding mononucleotide repeat microsatellites in ovarian tumors. Cancer. 2001;92:2829-2836. (Pubitemid 33091919)
53. Sood AK, Holmes R, Hendrix MJ, et al. Application of the National Cancer Institute international criteria for determination of microsatellite instability in ovarian cancer. Cancer Res. 2001;61:4371-4374. (Pubitemid 32685761)
54. Dellas A, Puhl A, Schraml P, et al. Molecular and clinicopathological analysis of ovarian carcinomas with and without microsatellite instability. Anticancer Res. 2004;24: 361-369. (Pubitemid 38279733)
55. Geisler JP, Goodheart MJ, Sood AK, et al. Mismatch repair gene expression defects contribute to microsatellite instability in ovarian carcinoma. Cancer. 2003;98:2199-2206. (Pubitemid 37392424)
56. Singer G, Kallinowski T, Hartmann A, et al. Different types of microsatellite instability in ovarian carcinoma. Int J Cancer. 2004;112:643-646. (Pubitemid 39425944)
57. Ueda H, Watanabe Y, Nakai H, et al. Microsatellite status and immunohistochemical features of ovarian clear-cell carcinoma. Anticancer Res. 2005;25:2785-2788. (Pubitemid 41044662)
58. Soliman PT, Broaddus RR, Schmeler KM, et al. Women with synchronous primary cancers of the endometrium and ovary: do they have Lynch syndrome? J Clin Oncol. 2005;23: 9344-9350.
59. Aysal A, Karnezis A, Medhi I, et al. Ovarian endometrioid adenocarcinoma: incidence and clinical significance of the morphologic and immunohistochemical markers of mismatch repair protein defects and tumor microsatellite instability. Am J Surg Pathol. 2012;36:163-172.
60. Turner JW, Baehner FL, Bloom KJ, et al. Prognostic uses of MSI testing 2011 [CAP Web site]. Available at. http://www.cap.org/apps/docs/committees/ technology/microsatellite-testing.pdf. Accessed July 23, 2013.