Cost-effectiveness of population screening for BRCA mutations in Ashkenazi Jewish women compared with family history-based testing

Journal of the National Cancer Institute

Volumn 107, Issue 1, 2015, Pages

  Manchanda, Ranjit ^a,b   Legood, Rosa ^c   Burnell, Matthew ^b   McGuire, Alistair ^d   Raikou, Maria ^d   Loggenberg, Kelly ^b   Wardle, Jane ^b   Sanderson, Saskia ^e   Gessler, Sue ^b   Side, Lucy ^b   Balogun, Nyala ^b   Desai, Rakshit ^b   Kumar, Ajith ^f   Dorkins, Huw ^g   Wallis, Yvonne ^h   Chapman, Cyril ^h   Taylor, Rohan ⁱ   Jacobs, Chris ^j   Tomlinson, Ian ^k   Beller, Uziel ^l   Menon, Usha ^b   Jacobs, Ian ^b,m   more..

^a ST BARTHOLOMEW S HOSPITAL   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d LONDON SCHOOL OF ECONOMICS   (United Kingdom)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^g Kennedy Galton Centre   (United Kingdom)

^h BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

ⁱ ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^j GUY S HOSPITAL   (United Kingdom)

^k UNIVERSITY OF OXFORD   (United Kingdom)

^l HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^m UNIVERSITY OF MANCHESTER   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA1 PROTEIN, HUMAN; BRCA2 PROTEIN; BRCA2 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; CANCER INCIDENCE; CANCER SCREENING; COMPARATIVE STUDY; COST CONTROL; COST EFFECTIVENESS ANALYSIS; FAMILY HISTORY; FEMALE; GENE MUTATION; GENETIC COUNSELING; GENETIC SCREENING; HEALTH CARE COST; HUMAN; INCIDENCE; JEW; LIFE EXPECTANCY; MAMMOGRAPHY; MASS SCREENING; NUCLEAR MAGNETIC RESONANCE IMAGING; OVARY CANCER; PRIORITY JOURNAL; QUALITY ADJUSTED LIFE YEAR; SALPINGOOOPHORECTOMY; SENSITIVITY ANALYSIS; ADULT; AGED; BREAST NEOPLASMS; COST BENEFIT ANALYSIS; EARLY DIAGNOSIS; ECONOMICS; GENETICS; MIDDLE AGED; MUTATION; OVARIAN NEOPLASMS; PROCEDURES; QUALITY OF LIFE; SENSITIVITY AND SPECIFICITY; UNITED KINGDOM;

ADULT; AGED; BRCA1 PROTEIN; BRCA2 PROTEIN; BREAST NEOPLASMS; COST-BENEFIT ANALYSIS; EARLY DETECTION OF CANCER; FEMALE; GENETIC TESTING; GREAT BRITAIN; HUMANS; JEWS; MASS SCREENING; MIDDLE AGED; MUTATION; OVARIAN NEOPLASMS; QUALITY OF LIFE; QUALITY-ADJUSTED LIFE YEARS; SENSITIVITY AND SPECIFICITY;

EID: 84922477275     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/dju380     Document Type: Article

References (112)

1. Levy-Lahad E, Gabai-Kapara E, Kaufman B, et al. Identification of BRCA1/BRCA2 carriers by screening in the healthy population and its implications. In: American Society of Clinical Oncology, Annual meeting. J Clin Oncol. 2011;29(Suppl);abstr 1513.
2. Hartge P, Struewing JP, Wacholder S, et al. The prevalence of common BRCA1 and BRCA2 mutations among Ashkenazi Jews. Am J Hum Genet. 1999;64(4):963-970.
3. Metcalfe KA, Poll A, Royer R, et al. Screening for founder mutations in BRCA1 and BRCA2 in unselected Jewish women. J Clin Oncol. 2010;28(3):387-391.
4. King MC, Marks JH, Mandell JB. Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science. 2003;302(5645):643-646.
5. Hopper JL, Southey MC, Dite GS, et al. Population-based estimate of the average age-specific cumulative risk of breast cancer for a defined set of protein-truncating mutations in BRCA1 and BRCA2. Australian Breast Cancer Family Study. Cancer Epidemiol Biomarkers Prev. 1999;8(9):741-747.
6. Peto J, Collins N, Barfoot R, et al. Prevalence of BRCA1 and BRCA2 gene mutations in patients with early-onset breast cancer. J Natl Cancer Inst. 1999;91(11):943-949.
7. Hirsh-Yechezkel G, Chetrit A, Lubin F, et al. Population attributes affecting the prevalence of BRCA mutation carriers in epithelial ovarian cancer cases in israel. Gynecol Oncol. 2003;89(3):494-498.
8. Moller P, Hagen AI, Apold J, et al. Genetic epidemiology of BRCA mutations-family history detects less than 50% of the mutation carriers. Eur J Cancer. 2007;43(11):1713-1717.
9. de Sanjose S, Leone M, Berez V, et al. Prevalence of BRCA1 and BRCA2 germline mutations in young breast cancer patients: a population-based study. Int J Cancer. 2003;106(4):588-593.
10. Shendure J, Ji H. Next-generation DNA sequencing. Nat Biotechnol. 2008;26(10):1135-1145.
11. Manchanda R, Loggenberg K, Burnell M, et al. Populationbased testing for brca1/2 mutations does not cause short term psychological harm: results from a randomized trial (GCaPPS). Int J Gynecol Cancer. 2012;22(8, Suppl 3):E153. Oral Presentation at IGCS conference, Vancouver, October 2012.
12. Petrou S, Gray A. Economic evaluation using decision analytical modelling: design, conduct, analysis, and reporting. BMJ. 2011;342:d1766.
13. Balmana J, Sanz J, Bonfill X, et al. Genetic counseling program in familial breast cancer: analysis of its effectiveness, cost and cost-effectiveness ratio. Int J Cancer. 2004;112(4):647-652.
14. Anderson K, Jacobson JS, Heitjan DF, et al. Cost-effectiveness of preventive strategies for women with a BRCA1 or a BRCA2 mutation. Ann Intern Med. 2006;144(6):397-406.
15. Yang KY, Caughey AB, Little SE, et al. A cost-effectiveness analysis of prophylactic surgery versus gynecologic surveillance for women from hereditary non-polyposis colorectal cancer (HNPCC) Families. Familial Cancer. 2011;10(3):535-543.
16. Kwon JS, Sun CC, Peterson SK, et al. Cost-effectiveness analysis of prevention strategies for gynecologic cancers in Lynch syndrome. Cancer. 2008;113(2):326-335.
17. Rubinstein WS, Jiang H, Dellefave L, et al. Cost-effectiveness of population-based BRCA1/2 testing and ovarian cancer prevention for Ashkenazi Jews: a call for dialogue. Genet Med. 2009;11(9):629-639.
18. Nelson HD, Fu R, Goddard K, et al. In. Risk Assessment, Genetic Counseling, and Genetic Testing for BRCA-Related Cancer: Systematic Review to Update the U. S. Preventive Services Task Force Recommendation. Rockville, MD; 2013.
19. NICE. Familial breast cancer: Classification and care of people at risk of familial breast cancer and management of breast cancer and related risks in people with a family history of breast cancer. In. NICE clinical guideline CG164 ed. London, UK: National Institute for Health and Care Excellence; 2013.
20. Finch A, Beiner M, Lubinski J, et al. Salpingo-oophorectomy and the risk of ovarian, fallopian tube, and peritoneal cancers in women with a BRCA1 or BRCA2 Mutation. JAMA. 2006;296(2):185-192.
21. Rebbeck TR, Kauff ND, Domchek SM. Meta-analysis of risk reduction estimates associated with risk-reducing salpingooophorectomy in BRCA1 or BRCA2 mutation carriers. J Natl Cancer Inst. 2009;101(2):80-87.
22. Rebbeck TR, Friebel T, Lynch HT, et al. Bilateral prophylactic mastectomy reduces breast cancer risk in BRCA1 and BRCA2 mutation carriers: the PROSE Study Group. J Clin Oncol. 2004;22(6):1055-1062.
23. Cuzick J, Sestak I, Bonanni B, et al. Selective oestrogen receptor modulators in prevention of breast cancer: an updated meta-analysis of individual participant data. Lancet. 2013;381(9880):1827-1834.
24. Jacobs I. Screening for familial ovarian cancer: the need for well-designed prospective studies. J Clin Oncol. 2005;23(24):5443-5445.
25. NICE. Guide to the methods of technology appraisal. In. N1618 ed. London, UK: National Institute for Health and Clinical Excellence (NICE); 2008.
26. Graham D, Schmool M, Waterman S. Jews in Britain: a snapshot from the 2001 Census. In: London, UK: Institute for Jewish Policy Research; 2007.
27. Office of National Statistics. Census 2001: National report for England and Wales, Part1, Section-2. Table S149: Sex and age by religion. In: London, UK: Office of National Statistics; 2003, 182-183.
28. Curtis L. Unit Costs of Health and Social Care 2011. In: Canterbury, Kent: Personal Social Services Research Unit (PSSRU); 2011.
29. Office of National Statistics. Lifetable for females in the UK. Available at: http://www.ons.gov. uk/ons/taxonomy/index.html?nscl=Interim+Life+Tables. Accessed June 2012.
30. Kadouri L, Hubert A, Rotenberg Y, et al. Cancer risks in carriers of the BRCA1/2 Ashkenazi founder mutations. J Med Genet. 2007;44(7):467-471.
31. Boyd J, Sonoda Y, Federici MG, et al. Clinicopathologic features of BRCA-linked and sporadic ovarian cancer. JAMA. 2000;283(17):2260-2265.
32. SEER. Surveillance Epidemiology and End Results. SEER Stat Fact Sheets: Ovary 2005-2009. Available at: http://seer.cancer.gov/statfacts/html/ovary.html. Accessed June 2012.
33. ONS. Cancer Registrations in England. In: London, UK: Office of National Statistics; 2010.
34. Abdel-Rahman M, Stockton D, Rachet B, et al. What if cancer survival in Britain were the same as in Europe: how many deaths are avoidable? Br J Cancer. 2009;101(Suppl 2):S115-S124.
35. Bolton KL, Chenevix-Trench G, Goh C, et al. Association between BRCA1 and BRCA2 mutations and survival in women with invasive epithelial ovarian cancer. JAMA. 2012;307(4):382-390.
36. Walters S, Nur U, Rachet B, et al. (2010) Cancer survival in England: one-year and five-year survival for 21 common cancers, by sex and age. Office for National Statistics, Statistical Bulletin.
37. Bordeleau L, Panchal S, Goodwin P. Prognosis of BRCA-associated breast cancer: a summary of evidence. Breast Cancer Res Treat. 2010;119(1):13-24.
38. Rennert G, Bisland-Naggan S, Barnett-Griness O, et al. Clinical outcomes of breast cancer in carriers of BRCA1 and BRCA2 mutations. N Engl J Med. 2007;357(2):115-123.
39. Madalinska JB, Hollenstein J, Bleiker E, et al. Quality-oflife effects of prophylactic salpingo-oophorectomy versus gynecologic screening among women at increased risk of hereditary ovarian cancer. J Clin Oncol. 2005;23(28):6890-6898.
40. Havrilesky LJ, Broadwater G, Davis DM, et al. Determination of quality of life-related utilities for health states relevant to ovarian cancer diagnosis and treatment. Gynecol Oncol. 2009;113(2):216-220.
41. Drummond M, Sculpher M, Torrance G, et al. Methods for the economic evaluation of health care programs. Third Edition ed. Oxford Oxford University Press; 2005.
42. Armstrong DK. Relapsed ovarian cancer: challenges and management strategies for a chronic disease. Oncologist. 2002;7(Suppl 5):20-28.
43. Yancik R. Ovarian cancer. Age contrasts in incidence, histology, disease stage at diagnosis, and mortality. Cancer. 1993;71(2 Suppl):517-523.
44. Swart A. Long-term follow-up of women enrolled in a randomized trial of adjuvant chemotherapy for early stage ovarian cancer. In: ASCO Annual Meeting Proceedings (Part I). 2007: Abstract 25, p. 18S (June 20 Supplement): 5509. J Clin Oncol.
45. Lyratzopoulos G, Abel GA, Barbiere JM, et al. Variation in advanced stage at diagnosis of lung and female breast cancer in an English region 2006-2009. Br J Cancer. 2012;106(6):1068-1075.
46. CRUK. (2012) Breast Cancer Incidence Statistics UK 2009-2011. Breast Cancer (C50), Average Number of New Cases per Year and Age-Specific Incidence Rates, Females, UK, 2009-2011.
47. NICE. National costing report: Early and locally advanced breast cancer/Advanced breast cancer. In: London, UK: National Institute for Health and Clinical Excellence; 2009.
48. ONS. (2008) Registrations of cancer diagnosed in 2006, England. Cancer Statistics Registrations, The Office for National Statistics.
49. Heijnsdijk EA, Warner E, Gilbert FJ, et al. Differences in natural history between breast cancers in BRCA1 and BRCA2 mutation carriers and effects of MRI screening-MRISC, MARIBS, and Canadian studies combined. Cancer Epidemiol Biomarkers Prev. 2012;21(9):1458-1468.
50. NICE. Clinical Guideline (CG81) - Advanced breast cancer: diagnosis and treatment. In: Cardiff, Wales, UK: National Collaborating Centre for Cancer, National Institute for Health and Clinical Excellence; 2009.
51. Peasgood T, Ward SE, Brazier J. Health-state utility values in breast cancer. Expert review of pharmacoeconomics & outcomes research. 2010;10(5):553-566.
52. Gennari A, Conte P, Rosso R, et al. Survival of metastatic breast carcinoma patients over a 20-year period: a retrospective analysis based on individual patient data from six consecutive studies. Cancer. 2005;104(8):1742-1750.
53. NICE. Social value judgements: principles for the development of NICE guidance. In: (NICE) NIfHaCE, (ed). 2nd ed: National Institute for Health and Clinical Excellence (NICE); 2008.
54. Andronis L, Barton P, Bryan S. Sensitivity analysis in economic evaluation: an audit of NICE current practice and a review of its use and value in decision-making. Health technology assessment. 2009;13(29):iii, ix-xi, 1-61.
55. Briggs A. Probabilistic analysis of cost-effectiveness models: statistical representation of parameter uncertainty. Value Health. 2005;8(1):1-2.
56. NICE. Familial breast cancer: The classification and careof women at risk of familial breast cancer in primary, secondary and tertiary care. In. London: National Institute for Health and Clinical Excellence; 2006.
57. Griebsch I, Brown J, Boggis C, et al. Cost-effectiveness of screening with contrast enhanced magnetic resonance imaging vs X-ray mammography of women at a high familial risk of breast cancer. Br J Cancer. 2006;95(7):801-810.
58. Dedes KJ, Bramkamp M, Szucs TD. Paclitaxel: cost-effectiveness in ovarian cancer. Expert Rev Pharmacoecon Outcomes Res. 2005;5(3):235-243.
59. NICE. (2003) Guidance on the use of paclitaxel in the treatment of ovarian cancer.
60. Roa BB, Boyd AA, Volcik K, et al. Ashkenazi Jewish population frequencies for common mutations in BRCA1 and BRCA2. Nat Genet 1996;14(2):185-187.
61. Chen S, Parmigiani G. Meta-analysis of BRCA1 and BRCA2 penetrance. J Clin Oncol. 2007;25(11):1329-1333.
62. Manchanda R, Burnell M, Abdelraheim A, et al. Factors influencing uptake and timing of risk-reducing salpingooophorectomy in women at risk of familial ovarian cancer: a competing risk time to event analysis. BJOG. 2012;119(5):527-536.
63. Finch A, Metcalfe KA, Chiang JK, et al. The impact of prophylactic salpingo-oophorectomy on menopausal symptoms and sexual function in women who carry a BRCA mutation. Gynecol Oncol. 2011;121(1):163-168.
64. Robson M, Hensley M, Barakat R, et al. Quality of life in women at risk for ovarian cancer who have undergone riskreducing oophorectomy. Gynecol Oncol. 2003;89(2):281-287.
65. Lokkegaard E, Jovanovic Z, Heitmann BL, et al. The association between early menopause and risk of ischaemic heart disease: influence of Hormone Therapy. Maturitas. 2006;53(2):226-233.
66. Michelsen TM, Dorum A, Dahl AA. A controlled study of mental distress and somatic complaints after risk-reducing salpingooophorectomy in women at risk for hereditary breast ovarian cancer. Gynecol Oncol. 2009;113(1):128-133.
67. Madalinska JB, van Beurden M, Bleiker EM, et al. The impact of hormone replacement therapy on menopausal symptoms in younger high-risk women after prophylactic salpingooophorectomy. J Clin Oncol. 2006;24(22):3576-3582.
68. MacLennan AH. Hormone replacement therapy: a 2008 perspective. Obstet Gynecol Reprod Med. 2008;19(1):13-18.
69. Sturdee DW, Pines A, Archer DF, et al. Updated IMS recommendations on postmenopausal hormone therapy and preventive strategies for midlife health. Climacteric. 2011;14(3):302-320.
70. Rebbeck TR, Friebel T, Wagner T, et al. Effect of short-term hormone replacement therapy on breast cancer risk reduction after bilateral prophylactic oophorectomy in BRCA1 and BRCA2 mutation carriers: the PROSE Study Group. J Clin Oncol. 2005;23(31):7804-7810.
71. Evans DG, Lalloo F, Ashcroft L, et al. Uptake of risk-reducing surgery in unaffected women at high risk of breast and ovarian cancer is risk, age, and time dependent. Cancer Epidemiol Biomarkers Prev. 2009;18(8):2318-2324.
72. Skytte AB, Gerdes AM, Andersen MK, et al. Risk-reducing mastectomy and salpingo-oophorectomy in unaffected BRCA mutation carriers: uptake and timing. Clin Genet. 2010;77(4):342-349.
73. Friebel TM, Domchek SM, Neuhausen SL, et al. Bilateral prophylactic oophorectomy and bilateral prophylactic mastectomy in a prospective cohort of unaffected BRCA1 and BRCA2 mutation carriers. Clin Breast Cancer. 2007;7(11):875-882.
74. Sigal BM, Munoz DF, Kurian AW, et al. A Simulation Model to Predict the Impact of Prophylactic Surgery and Screening on the Life Expectancy of BRCA1 and BRCA2 Mutation Carriers. Cancer Epidemiol Biomarkers Prev. 2012;21(7):1066-1077.
75. Brandberg Y, Sandelin K, Erikson S, et al. Psychological reactions, quality of life, and body image after bilateral prophylactic mastectomy in women at high risk for breast cancer: a prospective 1-year follow-up study. J Clin Oncol. 2008;26(24):3943-3949.
76. Isern AE, Tengrup I, Loman N, et al. Aesthetic outcome, patient satisfaction, and health-related quality of life in women at high risk undergoing prophylactic mastectomy and immediate breast reconstruction. J Plast Reconstr Aesthet Surg. 2008;61(10):1177-1187.
77. Brandberg Y, Arver B, Johansson H, et al. Less correspondence between expectations before and cosmetic results after riskreducing mastectomy in women who are mutation carriers: a prospective study. Eur J Surg Oncol. 2012;38(1):38-43.
78. Metcalfe KA, Esplen MJ, Goel V, et al. Psychosocial functioning in women who have undergone bilateral prophylactic mastectomy. Psychooncology. 2004;13(1):14-25.
79. Wasteson E, Sandelin K, Brandberg Y, et al. High satisfaction rate ten years after bilateral prophylactic mastectomy - a longitudinal study. Eur J Cancer Care (Engl). 2011;20(4):508-513.
80. Chaliki H, Loader S, Levenkron JC, et al. Women's receptivity to testing for a genetic susceptibility to breast cancer. Am J Public Health. 1995;85(8 Pt 1):1133-1135.
81. Tambor ES, Rimer BK, Strigo TS. Genetic testing for breast cancer susceptibility: awareness and interest among women in the general population. Am J Med Genet. 1997;68(1):43-49.
82. Press NA, Yasui Y, Reynolds S, et al. Women's interest in genetic testing for breast cancer susceptibility may be based on unrealistic expectations. Am J Med Genet. 2001;99(2):99-110.
83. Phillips KA, Warner E, Meschino WS, et al. Perceptions of Ashkenazi Jewish breast cancer patients on genetic testing for mutations in BRCA1 and BRCA2. Clin Genet. 2000;57(5):376-383.
84. CRUK. Ovarian Cancer - UK Incidence Statistics. Available at: http://info.cancerresearchuk.org/cancerstats/types/ovary/incidence/. Accessed March 2013.
85. ONS. (2013) Cancer Registration Statistics, England, 2011. Office for National Statistics.
86. Bahar AY, Taylor PJ, Andrews L, 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(2):440-445.
87. Evans DG, Shenton A, Woodward E, et al. Penetrance estimates for BRCA1 and BRCA2 based on genetic testing in a Clinical Cancer Genetics service setting: risks of breast/ovarian cancer quoted should reflect the cancer burden in the family. BMC Cancer. 2008;8:155.
88. Bradbury AR, Ibe CN, Dignam JJ, et al. Uptake and timing of bilateral prophylactic salpingo-oophorectomy among BRCA1 and BRCA2 mutation carriers. Genet Med. 2008;10(3):161-166.
89. Curtis L. Unit Costs of Health and Social Care 2010. In: Personal Social Services Research Unit (PSSRU); 2010.
90. Department of Health PbR Team. NHS 2010-11 reference costs publication. In: Department of Health; 2011.
91. BNF. British National Formulary 67. London, UK: BMJ Group, and the Pharmaceutical Press (Royal Pharmaceutical Society of Great Britain); 2014.
92. NICE. Ovarian cancer: the recognition and initial management of ovarian cancer. In: London: National Institute for Health and Clinical Excellence (NICE); 2011.
93. NAO. End of life care. In: Burr TCaAG, ed. London: National Audit Office (NAO), House of Commons; 2008.
94. Robertson C, Arcot Ragupathy SK, Boachie C, et al. The clinical effectiveness and cost-effectiveness of different surveillance mammography regimens after the treatment for primary breast cancer: systematic reviews registry database analyses and economic evaluation. Health Technol Assess. 2011;15(34):v-vi, 1-322.
95. Contant CM, Menke-Pluijmers MB, Seynaeve C, et al. Clinical experience of prophylactic mastectomy followed by immediate breast reconstruction in women at hereditary risk of breast cancer (HB (O) C) or a proven BRCA1 and BRCA2 germ-line mutation. Eur J Surg Oncol. 2002;28(6):627-632.
96. NICE. Early and locally advanced breast cancer: diagnosis and treatment. In. NICE Clinical Guideline, CG80. Cardiff, Wales, UK: National Collaborating Centre for Cancer, National Institute for Health and Clinical Excellence; 2009.
97. Manchanda R, Loggenberg K, Burnell M, et al. Dvdbased genetic counseling is as effective and more costefficient than standard-counseling for BRCA testing: results from a randomized trial. Int J Gynecol Cancer. 2012;22(8, Suppl 3):E413. Presented at IGCS, conference Vancouver, October 2012.
98. Waldron J. Breast Screening Program, England 2008-09. In: UK: The NHS Information Centre, for Health and Social Care, Government Statistical Service; 2010.
99. Bates T, Kearins O, Monypenny I, et al. Clinical outcome data for symptomatic breast cancer: the Breast Cancer Clinical Outcome Measures (BCCOM) Project. Br J Cancer. 2009;101(3):395-402.
100. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomized trials. Lancet. 2005;365(9472):1687-1717.
101. Cortesi L, Turchetti D, Marchi I, et al. Breast cancer screening in women at increased risk according to different family histories: an update of the Modena Study Group experience. BMC Cancer. 2006;6:210.
102. Leach MO, Boggis CR, Dixon AK, et al. Screening with magnetic resonance imaging and mammography of a UK population at high familial risk of breast cancer: a prospective multicentre cohort study (MARIBS). Lancet. 2005;365(9473):1769-1778.
103. Robson ME, Chappuis PO, Satagopan J, et al. A combined analysis of outcome following breast cancer: differences in survival based on BRCA1/BRCA2 mutation status and administration of adjuvant treatment. Breast Cancer Res. 2004;6(1):R8-R17.
104. Blamey RW, Ellis IO, Pinder SE, et al. Survival of invasive breast cancer according to the Nottingham Prognostic Index in cases diagnosed in 1990-1999. Eur J Cancer. 2007;43(10):1548-1555.
105. Gribbin J, Dewis R. (2009) Adjuvant! Online: review of evidence concerning its validity, and other considerations relating to its use in the NHS. NICE Clinical Guidelines, No. 80: Early and Locally Advanced Breast Cancer: Diagnosis and Treatment.
106. Comen E, Davids M, Kirchhoff T, et al. Relative contributions of BRCA1 and BRCA2 mutations to "triple-negative" breast cancer in Ashkenazi Women. Breast Cancer Res Treat. 2011;129(1):185-190.
107. Tung N, Garber JE, Lincoln A, et al. Frequency of triplenegative breast cancer in BRCA1 mutation carriers: comparison between common Ashkenazi Jewish and other mutations. J Clin Oncol. 2012;30(35):4447-4448.
108. Chappuis PO, Nethercot V, Foulkes WD. Clinico-pathological characteristics of BRCA1- and BRCA2-related breast cancer. Semin Surg Oncol. 2000;18(4):287-295.
109. Kozlow W, Guise TA. Breast cancer metastasis to bone: mechanisms of osteolysis and implications for therapy. J Mammary Gland Biol Neoplasia. 2005;10(2):169-180.
110. Lipton A, Hershey S. (2006) Bone Metastases in Breast Cancer. Business Briefing: US Oncology Review.
111. Wapnir IL, Anderson SJ, Mamounas EP, et al. Prognosis after ipsilateral breast tumor recurrence and locoregional recurrences in five National Surgical Adjuvant Breast and Bowel Project node-positive adjuvant breast cancer trials. J Clin Oncol. 2006;24(13):2028-2037.
112. Anderson SJ, Wapnir I, Dignam JJ, et al. Prognosis after ipsilateral breast tumor recurrence and locoregional recurrences in patients treated by breast-conserving therapy in five National Surgical Adjuvant Breast and Bowel Project protocols of node-negative breast cancer. J Clin Oncol. 2009;27(15):2466-2473.