Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: A kin-cohort study in Ontario, Canada

Journal of the National Cancer Institute

Volumn 98, Issue 23, 2006, Pages 1694-1706

  Risch, Harvey A ^a   McLaughlin, John R ^b,c   Cole, David E C ^c   Rosen, Barry ^c   Bradley, Linda ^c   Fan, Isabel ^d   Tang, James ^d   Li, Song ^d   Zhang, Shiyu ^d   Shaw, Patricia A ^e   Narod, Steven A ^c,d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN;

ADULT; AGED; ARTICLE; BREAST CANCER; CANADA; CANCER GENETICS; CANCER INCIDENCE; COHORT ANALYSIS; CONFIDENCE INTERVAL; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; DENATURING HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ETHNIC DIFFERENCE; EXON; FEMALE; GENE FREQUENCY; GENE MUTATION; GENETIC SCREENING; GENETIC VARIABILITY; GERM LINE; HETEROZYGOTE; HISTOPATHOLOGY; HUMAN; MAJOR CLINICAL STUDY; MALE; MALIGNANT NEOPLASTIC DISEASE; MUTATIONAL ANALYSIS; OUTCOMES RESEARCH; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROPORTIONAL HAZARDS MODEL; TESTIS CANCER;

BREAST NEOPLASMS; BREAST NEOPLASMS, MALE; COHORT STUDIES; FEMALE; GENE FREQUENCY; GENES, BRCA1; GENES, BRCA2; HUMANS; MALE; MUTATION; NEOPLASMS; ONTARIO; OVARIAN NEOPLASMS;

EID: 33845654907     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djj465     Document Type: Article

References (87)

1. Narod S, Ford D, Devilee P, Barkardottir RB, Eyfjord J, Lenoir G, et al. Genetic heterogeneity of breast-ovarian cancer revisited. Breast Cancer Linkage Consortium. Am J Hum Genet 1995;57:957-8.
2. Frank TS, Manley SA, Olopade OI, Cummings S, Garber JE, Bernhardt B, et al. Sequence analysis of BRCA1 and BRCA2: Correlation of mutations with family history and ovarian cancer risk. J Clin Oncol 1998; 16:1-10.
3. Takahashi H, Behbakht K, McGovern PE, Chiu H-C, Couch FJ, Weber BL, et al. Mutation analysis of the BRCA1 gene in ovarian cancers. Cancer Res 1995;55:2998-3002.
4. Stratton JF, Gayther SA, Russel PL, Dearden J, Gore M, Blake P, et al. Contribution of BRCA1 mutations to ovarian cancer. N Engl J Med 1997; 336:1125-30.
5. Rubin SC, Blackwood MA, Bandera C, Behbakht K, Benjamin I, Rebbeck TR, 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;178:670-7.
6. Tonin PN, Mes-Masson A-M, Narod SA, Ghadirian P, Provencher D. Founder BRCA1 and BRCA2 mutations in French Canadian ovarian cancer cases unselected for family history. Clin Genet 1999:55:318-24.
7. Anton-Culver H, Cohen PF, Gildea ME, Ziogas A. Characteristics of BRCA1 mutations in a population-based case series of breast and ovarian cancer. Eur J Cancer 2000;36:1200-8.
8. Van der Looij M, Szabo C, Besznyak I, Liszka G, Csokay B, Pulay T, et al. Prevalence of founder BRCA1 and BRCA2 mutations among breast and ovarian cancer patients in Hungary. Int J Cancer 2000;86: 737-40.
9. Risch HA, McLaughlin JR, Cole DEC, Rose n B, Bradley L, Kwan E, et al. Prevalence and penetrance of germline BRCA1 and BRCA2 mutations in a population series of 649 women with ovarian cancer. Am J Hum Genet 2001;68:700-10.
10. Smith SA, Richards WE, Caito K, Hanjani P, Markman M, DeGeest K, et al. BRCA1 germline mutations and polymorphisms in a clinic-based series of ovarian cancer cases: A Gynecologic Oncology Group study. Gynecol Oncol 2001;83:586-92.
11. Sarantaus L, Vahteristo P, Bloom E, Tamminen A, Unkila-Kallio L, Butzow R, et al. BRCA1 and BRCA2 mutations among 233 unselected Finnish ovarian carcinoma patients. Eur J Hum Genet 2001;9:424-30.
12. Heimdal K, Mæhlea L, Apold J, Pedersen JC, Møller P. The Norwegian founder mutations in BRCA1: High penetrance confirmed in an incident cancer series and differences observed in the risk of ovarian cancer. Eur J Cancer 2003;39:2205-13.
13. Bjørge T, Lie AK, Hovig E, Gislefoss RE, Hansen S, Jellum E, et al. BRCA1 mutations in ovarian cancer and borderline tumours in Norway: A nested case-control study. Br J Cancer 2004;91:1829-34.
14. Gorski B, Menkiszak J, Gronwald J, Lubinski J, Narod SA. A protein truncating BRCA1 allele with a low penetrance of breast cancer. J Med Genet 2004;41:e130.
15. Malander S, Ridderheim M, Måsbäck A, Loman N, Kristoffersson U, Olsson H, et al. One in 10 ovarian cancer patients carry germ line BRCA1 or BRCA2 mutations: Results of a prospective study in southern Sweden. Eur J Cancer 2004;40:422-8.
16. Rafnar T, Benediktsdottir KR, Eldon BJ, Gestsson T, Saemundsson H, Olafsson K, et al. BRCA2, but not BRCA1, mutations account for familial ovarian cancer in Iceland: A population-based study. Eur J Cancer 2004;40:2788-93.
17. Pal T, Permuth-Wey J, Betts JA, Krischer JP, Fiorica J, Arango H, et al. BRCA1 and BRCA2 mutations account for a large proportion of ovarian carcinoma cases. Cancer 2005;104:2807-16.
18. Foster KA, Harrington P, Kerr J, Russell P, DiCioccio RA, Scott IV, et al. Somatic and germline mutations of the BRCA2 gene in sporadic ovarian cancer. Cancer Res 1996;56:3622-5.
19. Takahashi H, Chiu H-C, Bandera CA, Behbakht K, Liu PC, Couch FJ, et al. Mutations of the BRCA2 gene in ovarian carcinomas. Cancer Res 1996;56:2738-41.
20. Ford D, Easton DF, Peto J. Estimates of the gene frequency of BRCA1 and its contribution to breast and ovarian cancer incidence. Am J Hum Genet 1995;57:1457-62.
21. Whittemore AS, Gong G, Itnyre J. Prevalence and contribution of BRCA1 mutations in breast cancer and ovarian cancer: Results from three U.S. population-based case-control studies of ovarian cancer. Am J Hum Genet 1997;60:496-504.
22. Antoniou AC, Pharoah PDP, McMullan G, Day NE, Stratton MR, Peto J, et al. A comprehensive model for familial breast cancer incorporating BRCA1, BRCA2 and other genes. Br J Cancer 2002;86:76-83.
23. Whittemore AS, Gong G, John EM, McGuire V, Li FP, Ostrow KL, et al. Prevalence of BRCA1 mutation carriers among U.S. non-Hispanic whites. Cancer Epidemiol Biomarkers Prev 2004;13:2078-83.
24. Tonin PN, Mes-Masson A-M, Futreal PA, Morgan K, Mahon M, Foulkes WD, et al. Founder BRCA1 and BRCA2 mutations in French Canadian breast and ovarian cancer families. Am J Hum Genet 1998;63: 1341-51.
25. Kuperstein G, Foulkes WD, Ghadirian P, Hakimi J, Narod SA. A rapid fluorescent multiplexed-PCR analysis FMPA for founder mutations in the BRCA1 and BRCA2 genes. Clin Genet 2000;57:213-20.
26. Puget N, Sinilnikova OM, Stoppa-Lyonnet D, Audoynaud C, Pagès S, Lynch HT, et al. An Alu-mediated 6-kb duplication in the BRCA1 gene: A new founder mutation? Am J Hum Genet 1999;64:300-2.
27. Breast Cancer Information Core (BIC). Available at: http://research.nhgri.nih.gov/bic/. [Last accessed: November 2, 2006.]
28. Kuperstein G, Jack E, Narod SA. A fluorescent multiplexed-denaturing gradient gel electrophoresis screening test for mutations in the BRCA1 gene. Genet Test 2006;10:1-7.
29. Gross E, Arnold N, Pfeifer K, Bandick K, Kiechle M. Identification of specific BRCA1 and BRCA2 variants by DHPLC. Hum Mutat 2000;16: 345-53.
30. Peelen T, van Vliet M, Bosch A, Bignell G, Vasen HFA, Klijn JGM, et al. Screening for BRCA2 mutations in 81 Dutch breast-ovarian cancer families. Br J Cancer 2000;82:151-6.
31. Francis B, Green M, Payne C. The GLIM system: Generalised linear interactive modelling. Release 4 manual. Oxford U.K.): Clarendon Press; 1993.
32. Saunders CL, Begg CB. Kin-cohort evaluation of relative risks of genetic variants. Genet Epidemiol 2003;24:220-9.
33. Oehlert, GW. A note on the delta method. Am Stat 1992;46:27-9.
34. Cancer Care Ontario. Cancer incidence, mortality, survival and prevalence in Ontario. Release 4, April 2004, 1964-2002 [CD]. Toronto, Ontario ON): Cancer Care Ontario, Division of Preventive Oncology, Surveillance Unit.
35. Ontario Cancer Registry, Cancer Care Ontario. Ontario incidence rates, 1979-2002. Available at: http://canques.seer.cancer.gov/ontario/. [Last accessed: February 26, 2006.]
36. Ontario Cancer Registry, Cancer Care Ontario. Ontario mortality rates, 1979-2002. Available at: http://canques.seer.cancer.gov/ontario/. [Last accessed: February 26, 2006.]
37. Statistics Canada, Health Statistics Division. Major chronic diseases surveillance on-line. Major chronic diseases mortality by age group. Available at: http://dsol-smed.phac-aspc.gc.ca/dsol-smed/mcd-smcm/ d_age_e.html. [Last accessed: February 26, 2006.]
38. Statistical Research and Applications Branch, National Cancer Institute. DevCan: Probability of developing or dying of cancer software. Version 6.1 Beta, 2005. Available at: http://srab.cancer.gov/devcan. [Last accessed: January 23, 2006.]
39. Fay MP, Pfeiffer R, Cronin KA, Le C, Feuer EJ. Age-conditional probabilities of developing cancer. Stat Med 2003;22:1837-48.
40. Fay MP. Estimating age conditional probability of developing disease from surveHllance data. Popul Health Metr 2004;2:6. Available at: http://www.pophealthmetrics.com/content/2/1/6. [Last accessed: September 20, 2005.]
41. Thompson D, Easton D; Breast Cancer Linkage Consortium. Variation in cancer risks, by mutation position, in BRCA2 mutation carriers. Am J Hum Genet 2001;68:410-9.
42. Lubinski J, Phelan CM, Ghadirian P, Lynch HT, Garber J, Weber B, et al. Cancer variation associated with the position of the mutation in the BRCA2 gene. Fam Cancer 2004;3:1-10.
43. Oddoux C, Struewing JP, Clayton CM, Neuhausen S, Brody LC, Kaback M, et al. The carrier frequency of the BRCA2 6174delT mutation among Ashkenazi Jewish individuals is approximately 1%. Nat Genet 1996;14:188-90.
44. Roa BB, Boyd AA, Volcik K, Richards CS. Ashkenazi Jewish population frequencies for common mutations in BRCA1 and BRCA2. Nat Genet 1996;14:185-7.
45. Struewing JP, Hartge P, Wacholder S, Baker SM, Berlin M, McAdams M, et al. The risk of cancer associated with specific mutations of BRCA1 and BRCA2 among Ashkenazi Jews. N Engl J Med 1997;336:1401-8.
46. Bahar AY, Taylor PJ, Andrews L, Proos A, Burnett L, Tucker K, et al. The frequency of founder mutations in the BRCA1, BRCA2, and APC genes in Australian Ashkenazi Jews: Implications for the generality of U.S. population data. Cancer 2001;92:440-5.
47. Modan B, Gak E, Sade-Bruchim RB, Hirsh-Yechezkel G, Theodor L, Lubin F, et al. High frequency of BRCA1 185delAG mutation in ovarian cancer in Israel. National Israel Study of Ovarian Cancer. JAMA 1996;276:1823-5.
48. Abeliovich D, Kaduri L, Lerer I, Weinberg N, Amir G, Sagi M, et al. The founder mutations 185delAG and 5382insC in BRCA1 and 6174delT in BRCA2 appear in 60% of ovarian cancer and 30% of early-onset breast cancer patients among Ashkenazi women. Am J Hum Genet 1997;60: 505-14.
49. Levy-Lahad E, Catane R, Eisenberg S, Kaufman B, Hornreich G, Lishinsky E, et al. Founder BRCA1 and BRCA2 mutations in Ashkenazi Jews in Israel: frequency and differential penetrance in ovarian cancer and in breast-ovarian cancer families. Am J Hum Genet 1997;60:1059-67.
50. Lu KH, Cramer DW, Muto MG, Li EY, Niloff J, Mok SC. A population-based study of BRCA1 and BRCA2 mutations in Jewish women with epithelial ovarian cancer. Obstet Gynecol 1999;93:34-7.
51. Boyd J, Sonoda Y, Federici MG, Bogomolniy F, Rhei E, Maresco DL, et al. Clinicopathologic features of BRCA-linked and sporadic ovarian cancer. J Am Med Assoc 2000;283:2260-5.
52. Moslehi R, Chu W, Karlan B, Fishman D, Risch H, Fields A, et al. BRCA1 and BRCA2 mutation analysis of 208 Ashkenazi Jewish women with ovarian cancer. Am J Hum Genet 2000;66:1259-72.
53. Tobias DH, Eng C, McCurdy LD, Kalir T, Mandelli J, Dottino PR, et al. Founder BRCA 1 and 2 mutations among a consecutive series of Ashkenazi Jewish ovarian cancer patients. Gynecol Oncol 2000;78:148-51.
54. Modan B, Hartge P, Hirsh-Yechezkel G, Chetrit A, Lubin F, Beller U, et al. Parity, oral contraceptives, and the risk of ovarian cancer among carriers and noncarriers of a BRCA1 or BRCA2 mutation. N Engl J Med 2001; 345:235-40.
55. Surveillance, Epidemiology, and End Results SEER Program SEER*Stat Database: Incidence - SEER 9 Regs Public-Use, Nov 2004 Sub 1973-2003), based on the November 2005 submission, released April 2006. Bethesda MD): National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch. Available at: http://seer.cancer.gov/ publicdata/. [Last accessed: November 2, 2005.]
56. Rubin SC, Benjamin I, Behbakht K, Takahashi H, Morgan MA, LiVolsi VA, et al. Clinical and pathological features of ovarian cancer in women with germ-line mutations of BRCA1. N Engl J Med 1996;335:1413-6.
57. Brunet J-S, Narod SA, Tonin P, Foulkes WD. BRCA1 mutations and survival in women with ovarian cancer. N Engl J Med 1997;336:1256.
58. Johannsson OT, Ranstarn J, Borg A, Olsson H. Survival of BRCA1 breast and ovarian cancer patients: A population-based study from southern Sweden. J Clin Oncol 1998;16:397-404.
59. Ramus SJ, Fishman A, Pharoah PD, Yarkoni S, Altaras M, Ponder BA. Ovarian cancer survival in Ashkenazi Jewish patients with BRCA1 and BRCA2 mutations. Eur J Surg Oncol 2001;27:278-81.
60. Ben David Y, Chetrit A, Hirsh-Yechezkel G, Friedman E, Beck BD, Beller U, et al.; National Israeli Study of Ovarian Cancer. Effect of BRCA mutations on the length of survival in epithelial ovarian tumors. J Clin Oncol 2002;20:463-6.
61. Buller RE, Shahin MS, Geisler JP, Zogg M, De Young BR, Davis CS. Failure of BRCA1 dysfunction to alter ovarian cancer survival. Clin Cancer Res 2002;8:1196-202.
62. Cass I, Baldwin RL, Varkey T, Moslehi R, Narod SA, Karlan BY. Improved survival in women with BRCA-associated ovarian carcinoma. Cancer 2003;97:2187-95.
63. Ziogas A, Anton-Culver H. Validation of family history data in cancer family registries. Am J Prev Med 2003;24:190-8.
64. Chang ET, Ekström Smedby K, Hjalgrim H, Glimelius B, Adami H-O. Reliability of self-reported family history of cancer in a large case-control study of lymphoma. J Natl Cancer Inst 2006;98:61-8.
65. Begg CB. On the use of familial aggregation in population-based case probands for calculating penetrance. J Natl Cancer Inst 2002;94: 1221-6.
66. Risch HA, Narod SA. Re: On the use of familial aggregation in population-based case probands for calculating penetrance. J Natl Cancer Inst 2003;95:73-4.
67. Chatterjee N, Shib J, Hartge P, Brody L, Tucker M, Wacholder S. Association and aggregation analysis using kin-cohort designs with applications to genotype and family history data from the Washington Ashkenazi Study. Genet Epidemiol 2001;21:123-38.
68. Unger MA, Nathanson KL, Calzone K, Antin-Ozerkis D, Shih HA, Martin A-M, et al. Screening for genomic rearrangements in families with breast and ovarian cancer identifies BRCA1 mutations previously missed by conformation-sensitive gel electrophoresis or sequencing. Am J Hum Genet 2000;67:841-50.
69. Kremeyer B, Soller M, Lagerstedt K, Maguire P, Mazoyer S, Nordling M, et al. The BRCA1 exon 13 duplication in the Swedish population. Fam Cancer 2005;4:191-4.
70. The BRCA1 Exon 13 Duplication Screening Group. The exon 13 duplication in the BRCA1 gene is a founder mutation present in geographically diverse populations. Am J Hum Genet 2000;67:207-12.
71. Ford D, Easton DF, Bishop DT, Narod SA, Goldgar DE; Breast Cancer Linkage Consortium. Risks of cancer in BRCA 1-mutation carriers. Lancet 1994;343:692-5.
72. Anglian Breast Cancer Study Group. Prevalence and penetrance of BRCA1 and BRCA2 mutations in a population-based series of breast cancer cases. Br J Cancer 2000;83:1301-8.
73. Antoniou AC, Gayther SA, Stratton JF, Ponder BAJ, Easton DF. Risk models for familial ovarian and breast cancer. Genet Epidemiol 2000;18:173-90.
74. Satagopan JM, Offit K, Foulkes W, Robson ME, Wacholder S, Eng CM, et al. The lifetime risks of breast cancer in Ashkenazi Jewish carriers of BRCA1 and BRCA2 mutations. Cancer Epidemiol Biomarkers Prev 2001;10:467-73.
75. Antoniou A, Pharoah PDP, Narod S, Risch HA, Eyfjord JE, Hopper JL, et al. Average risks of breast and ovarian cancer associated with BRCA1 or BRCA2 mutations detected in case series unselected for family history: A combined analysis of 22 studies. Am J Hum Genet 2003;72: 1117-30.
76. King M-C, Marks JH, Mandell JB; New York Breast Cancer Study Group. Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science 2003;302:643-6.
77. Marroni F, Aretini P, D'Andrea E, Caligo MA, Cortesi L, Viel A, et al. Penetrances of breast and ovarian cancer in a large series of families tested for BRCA1/2 mutations. Eur J Hum Genet 2004; 12:899-906.
78. Satagopan JM, Boyd J, Kauff ND, Robson M, Scheuer L, Narod S, et al. Ovarian cancer risk in Ashkenazi Jewish carvers of BRCA1 and BRCA2 mutations. Clin Cancer Res 2002;8:3776-81.
79. Thorlacius S, Struewing JP, Hartge P, Olafsdottir GH, Sigvaldason H, Tryggvadottir L, et al. Population-based study of risk of breast cancer in carriers of BRCA2 mutation. Lancet 1998;352:1337-9.
80. Breast Cancer Linkage Consortium. Cancer risks in BRCA2 mutation carriers. J Natl Cancer Inst 1999;91:1310-6.
81. Thompson D, Easton D; Breast Cancer Linkage Consortium. Variation in BRCA1 cancer risks by mutation position. Cancer Epidemiol Biomarkers Prev 2002;11:329-36.
82. Liede A, Malik IA, Aziz Z, de los Rios P, Kwan E, Narod SA. Contribution of BRCA1 and BRCA2 mutations to breast and ovarian cancer in Pakistan. Am J Hum Genet 2002;71:595-606.
83. Syrjäkoski K, Kuukasjärvi T, Waltering K, Haraldsson K, Auvinen A, Borg Å, et al. BRCA2 mutations in 154 Finnish male breast cancer patients. Neoplasia 2004;6:541-5.
84. Lehrer S, Fodor F, Stock RG, Stone NN, Eng C, Song HK, et al. Absence of 185delAG mutation of the BRCA1 gene and 6174delT mutation of the BRCA2 gene in Ashkenazi Jewish men with prostate cancer. Br J Cancer 1998;78:771-3.
85. Sinclair CS, Berry R, Schaid D, Thibodeau SN, Couch FJ. BRCA1 and BRCA2 have a limited role in familial prostate cancer. Cancer Res 2000;60:1371-5.
86. Tulinius H, Olafsdottir GH, Sigvaldason H, Arason A, Barkardottir RB, Egilsson V, et al. The effect of a single BRCA2 mutation on cancer in Iceland. J Med Genet 2002;39:457-62.
87. Wacholder S. Binomial regression in GLIM: Estimating risk ratios and risk differences. Am J Epidemiol 1986;123:174-84.