Mammographic density and breast cancer risk: Current understanding and future prospects

Breast Cancer Research

Volumn 13, Issue 6, 2011, Pages

  Boyd, Norman F ^a   Martin, Lisa J ^a   Yaffe, Martin J ^b   Minkin, Salomon ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b SUNNYBROOK RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER; CANCER RISK; COMPUTER ASSISTED TOMOGRAPHY; DENSITY; HISTOPATHOLOGY; HUMAN; MAMMOGRAPHY; MEASUREMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; PERCENT MAMMOGRAPHIC DENSITY; PREDICTION; REVIEW; ULTRASOUND; BREAST TUMOR; FEMALE; PHOTON ABSORPTIOMETRY; RADIOGRAPHY; RISK ASSESSMENT; RISK FACTOR;

ABSORPTIOMETRY, PHOTON; BREAST NEOPLASMS; FEMALE; HUMANS; MAMMOGRAPHY; RISK ASSESSMENT; RISK FACTORS;

EID: 80755173295     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2942     Document Type: Review

References (94)

1. McCormack VA, dos Santos Silva I. Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2006, 15:1159-1169.
2. Boyd NF, Martin LJ, Bronskill MJ, Yaffe MJ, Duric N, Minkin S. Breast tissue composition and susceptibility to breast cancer. J Natl Cancer Inst 2010, 102:1224-1237.
3. Johns PC, Yaffe MJ. X-ray characterisation of normal and neoplastic breast tissues. Phys Med Biol 1987, 32:675-695.
4. Wolfe JN. Risk for breast cancer development determined by mammographic parenchymal pattern. Cancer 1976, 37:2486-2492.
5. Wolfe JN. Breast patterns as an index of risk for developing breast cancer. AJR Am J Roentgenol 1976, 126:1130-1139.
6. Byng JW, Boyd NF, Fishell E, Jong RA, Yaffe MJ. The quantitative analysis of mammographic densities. Phys Med Biol 1994, 39:1629-1638.
7. Kato I, Beinart C, Bleich A, Su S, Kim M, Toniolo PG. A nested case-control study of mammographic patterns, breast volume, and breast cancer (New York City, NY, United States). Cancer Causes Control 1995, 6:431-438.
8. Saftlas AF, Hoover RN, Brinton LA, Szklo M, Olson DR, Salane M, Wolfe JN. Mammographic densities and risk of breast cancer. Cancer 1991, 67:2833-2838.
9. Byrne C, Schairer C, Wolfe J, Parekh N, Salane M, Brinton LA, Hoover R, Haile R. Mammographic features and breast cancer risk: Effects with time, age, and menopause status. J Natl Cancer Inst 1995, 87:1622-1629.
10. Torres-Mejía G, De Stavola B, Allen DS, Pérez-Gavilán JJ, Ferreira JM, Fentiman IS, Dos Santos Silva I. Mammographic features and subsequent risk of breast cancer: A comparison of qualitative and quantitative evaluations in the Guernsey prospective studies. Cancer Epidemiol Biomarkers Prev 2005, 14:1052-1059.
11. van Gils CH, Hendriks JH, Otten JD, Holland R, Verbeek AL. Parity and mammographic breast density in relation to breast cancer risk: indication of interaction. Eur J Cancer Prev 2000, 9:105-111.
12. Thomas DB, Carter RA, Bush WH, Ray RM, Stanford JL, Lehman CD, Daling JR, Malone K, Davis S. Risk of subsequent breast cancer in relation to characteristics of screening mammograms from women less than 50 years of age. Cancer Epidemiol Biomarkers Prev 2002, 11:565-571.
13. Maskarinec G, Pagano I, Lurie G, Kolonel LN. A longitudinal investigation of mammographic density: the multiethnic cohort. Cancer Epidemiol Biomarkers Prev 2006, 15:732-739.
14. Boyd NF, Byng JW, Jong RA, Fishell EK, Little LE, Miller AB, Lockwood GA, Tritchler DL, Yaffe MJ. Quantitative classification of mammographic densities and breast cancer risk: results from the Canadian National Breast Screening Study. J Natl Cancer Inst 1995, 87:670-675.
15. Boyd NF, Guo H, Martin LJ, Sun L, Stone J, Fishell E, Jong RA, Hislop G, Chiarelli A, Minkin S, Yaffe MJ. Mammographic density and the risk and detection of breast cancer. N Engl J Med 2007, 356:227-236.
16. American College of Radiology Breast Imaging Reporting and Data System Atlas 2003, Reston, VA: American College of Radiology, 4, American College of Radiology.
17. Cummings SR, Tice JA, Bauer S, Browner WS, Cuzick J, Ziv E, Vogel V, Shepherd J, Vachon C, Smith-Bindman R, Kerlikowske K. Prevention of breast cancer in postmenopausal women: approaches to estimating and reducing risk. J Natl Cancer Inst 2009, 101:384-398.
18. Kerlikowske K, Grady D, Barclay J, Frankel SD, Ominsky SH, Sickles EA, Ernster V. Variability and accuracy in mammographic interpretation using the American college of radiology breast imaging reporting and data system. J Natl Cancer Inst 1998, 90:1801-1809.
19. Veronesi U, Boyle P, Goldhirsch A, Orecchia R, Viale G. Breast cancer. Lancet 2005, 365:1727-1741.
20. Newman B, Mu H, Butler LM, Millikan R, Moorman PG, King M-C. Frequency of breast cancer attributable to BRCA1 in a population-based series of American women. JAMA 1998, 279:915-921.
21. Peto J, Collins N, Barfoot R, Seal S, Warren W, Rahman N, Easton DF, Evans C, Deacon J, Stratton MR. Prevalence of BRCA1 and BRCA2 gene mutations in patients with early-onset breast cancer. J Natl Cancer Inst 1999, 91(11):943-949.
22. Martin LJ, Boyd N. Potential mechanisms of breast cancer risk associated with mammographic density: hypotheses based on epidemiological evidence. Breast Cancer Res 2008, 10:201.
23. Boyd NF, Rommens JM, Vogt K, Lee V, Hopper JL, Yaffe MJ, Paterson AD. Mammographic breast density as an intermediate phenotype for breast cancer. Lancet Oncol 2005, 6:798-808.
24. Martin LJ, Melnichouk O, Guo H, Chiarelli AM, Hislop TG, Yaffe MJ, Minkin S, Hopper JL, Boyd NF. Family history, mammographic density, and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2010, 19:456-463.
25. Sellers TA, Vachon CM, Pankratz VS, Janney CA, Fredericksen Z, Brandt KR, Huang Y, Couch FJ, Kushi LH, Cerhan JR. Association of childhood and adolescent anthropometric factors, physical activity, and diet with adult mammographic breast density. Am J Epidemiol 2007, 166:456-464.
26. Brisson J, Morrison AS, Kopans DB. Height and weight, mammographic features of breast tissue, and breast cancer risk. Am J Epidemiol 1984, 119:371-381.
27. Hunter DJ, Willett WC. Diet, body size, and breast cancer. Epidemiol Rev 1993, 15:110-132.
28. Boyd N, Martin L, Chavez S, Gunasekara A, Salleh A, Melnichouk O, Yaffe M, Friedenreich C, Minkin S, Bronskill M. Breast-tissue composition and other risk factors for breast cancer in young women: a cross-sectional study. Lancet Oncol 2009, 10:569-580.
29. Guo YP, Martin LJ, Hanna W, Banerjee D, Miller N, Fishell E, Khokha R, Boyd NF. Growth factors and stromal matrix proteins associated with mammographic densities. Cancer Epidemiol Biomarkers Prev 2001, 10:243-248.
30. Vachon CM, Sasano H, Ghosh K, Brandt KR, Watson DA, Reynolds C, Lingle WL, Goss PE, Li R, Aiyar SE, Scott CG, Pankratz VS, Santen RJ, Ingle JN. Aromatase immunoreactivity is increased in mammographically dense regions of the breast. Breast Cancer Res Treat 2011, 125:243-252.
31. Alowami S, Troup S, Al-Haddad S, Kirkpatrick I, Watson PH. Mammographic density is related to stroma and stromal proteoglycan expression. Breast Cancer Res 2003, 5:R129-R135.
32. Bartow SA, Mettler FA, Black WC. Correlations between radiographic patterns and morphology of the female breast. Rad Patterns Morph 1997, 13:263-275.
33. Li T, Sun L, Miller N, Nicklee T, Woo J, Hulse-Smith L, Tsao MS, Khokha R, Martin L, Boyd N. The association of measured breast tissue characteristics with mammographic density and other risk factors for breast cancer. Cancer Epidemiol Biomarkers Prev 2005, 14:343-349.
34. Boyd NF, Jensen H, Cooke G, Lee Han HW. Relationship between mammographic and histological risk factors for breast cancer. J Natl Cancer Inst 1992, 84:1170-1179.
35. Reinier KS, Vacek PM, Geller BM. Risk factors for breast carcinoma in situ versus invasive breast cancer in a prospective study of pre- and postmenopausal women. Breast Cancer Res Treat 2006, 103:343-348.
36. MacKenzie TA, Vacek PM, Geller B, Weiss JE, Goodrich ME, Carney PA. Breast density in relation to risk of ductal carcinoma in situ of the breast in women undergoing screening mammography. Cancer Causes Control 2007, 18:939-945.
37. Turashvili G, McKinney S, Martin L, Gelmon KA, Watson P, Boyd N, Aparicio S. Columnar cell lesions, mammographic density and breast cancer risk. Breast Cancer Res Treat 2009, 115:561-571.
38. Ghosh K, Hartmann LC, Reynolds C, Visscher DW, Brandt KR, Vierkant RA, Scott CG, Radisky DC, Sellers TA, Pankratz VS, Vachon CM. Association between mammographic density and age-related lobular involution of the breast. J Clin Oncol 2010, 28:2207-2212.
39. Ghosh K, Vachon CM, Pankratz VS, Vierkant RA, Anderson SS, Brandt KR, Visscher DW, Reynolds C, Frost MH, Hartmann LC. Independent association of lobular involution and mammographic breast density with breast cancer risk. J Natl Cancer Inst 2010, 102:1716-1723.
40. Aitken Z, McCormack VA, Highnam RP, Martin L, Gunasekara A, Melnichouk O, Mawdsley G, Peressotti C, Yaffe M, Boyd NF, dos Santos Silva I. Screen-film mammographic density and breast cancer risk: a comparison of the volumetric standard mammogram form and the interactive threshold measurement methods. Cancer Epidemiol Biomarkers Prev 2010, 19:418-428.
41. Boyd N, Martin L, Gunasekara A, Melnichouk O, Maudsley G, Peressotti C, Yaffe M, Minkin S. Mammographic density and breast cancer risk: evaluation of a novel method of measuring breast tissue volumes. Cancer Epidemiol Biomarkers Prev 2009, 18:1754-1762.
42. Shepherd JA, Kerlikowske K, Ma L, Duewer F, Fan B, Wang J, Malkov S, Vittinghoff E, Cummings SR. Volume of dense breast tissue and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2011, 20:1473-1482.
43. Heine JJ, Cao K, Rollison DE. Calibrated measures for breast density estimation. Acad Radiol 2011, 18:547-555.
44. Heine JJ, Cao K, Rollison DE, Tiffenberg G, Thomas JA. A quantitative description of the percentage of breast density measurement using fullfield digital mammography. Acad Radiol 2011, 18:556-564.
45. Graham SJ, Bronskill MJ, Byng JW, Yaffe MJ, Boyd NF. Quantitative correlation of breast tissue parameters using magnetic resonance and X-ray mammography. Br J Cancer 1996, 73:162-168.
46. Glide-Hurst CK, Duric N, Littrup P. Volumetric breast density evaluation from ultrasound tomography images. Med Phys 2008, 35:3988-3997.
47. Vachon CM, Kuni CC, Anderson K. Association of mammographically defined percent breast density with epidemiologic risk factors for breast cancer (United States). Cancer Causes Control 2000, 11:653-662.
48. Boyd NF, Dite GS, Stone J, Gunasekara A, English DR, McCredie MR, Giles GG, Tritchler D, Chiarelli A, Yaffe MJ, Hopper JL. Heritability of mammographic density, a risk factor for breast cancer. N Engl J Med 2002, 347:886-894.
49. Ursin G, Lillie EO, Lee E, Cockburn M, Schork NJ, Cozen W, Parisky YR, Hamilton AS, Astrahan MA, Mack T. The relative importance of genetics and environment on mammographic density. Cancer Epidemiol Biomarkers Prev 2009, 18:102-112.
50. Lindström S, Vachon CM, Li J, Varghese J, Thompson D, Warren R, Brown J, Leyland J, Audley T, Wareham NJ, Loos RJ, Paterson AD, Rommens J, Waggott D, Martin LJ, Scott CG, Pankratz VS, Hankinson SE, Hazra A, Hunter DJ, Hopper JL, Southey MC, Chanock SJ, Silva Idos S, Liu J, Eriksson L, Couch FJ, Stone J, Apicella C, Czene K, et al. Common variants in ZNF365 are associated with both mammographic density and breast cancer risk. Nat Genet 2011, 43:185-187.
51. Odefrey F, Stone J, Gurrin LC, Byrnes GB, Apicella C, Dite GS, Cawson JN, Giles GG, Treloar SA, English DR, Hopper JL, Southey MC, . Australian Twins and Sisters Mammographic Density Study Common genetic variants associated with breast cancer and mammographic density measures that predict disease. Cancer Res 2010, 70:1449-1458. Australian Twins and Sisters Mammographic Density Study.
52. Nelson CM, Bissell MJ. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 2006, 22:287-309.
53. Kass L, Erler JT, Dembo M, Weaver VM. Mammary epithelial cell: Influence of extracellular matrix composition and organization during development and tumorigensis. Int J Biochem Cell Biol 2007, 39:1987-1994.
54. Butcher DT, Alliston T, Weaver VM. A tense situation: forcing tumour progression. Nat Rev Cancer 2009, 9:108-122.
55. Bhowmick NA, Neilson EG, Moses HL. Stromal fibroblasts in cancer initiation and progression. Nature 2004, 432:332-337.
56. Schousboe JT, Kerlikowske K, Loh A, Cummings SR. Personalizing mammography by breast density and other risk factors for breast cancer: analysis of health benefits and cost-effectiveness. Ann Intern Med 2011, 155:10-20.
57. Mandelblatt JS, Stout N, Trentham-Dietz A. To screen or not to screen women in their 40s for breast cancer: is personalized risk-based screening the answer?. Ann Intern Med 2011, 155:58-60.
58. Gail MH, Brinton LA, Byar DP, Corle DK, Green SB, Schairer C, Mulvihill JJ. Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J Natl Cancer Inst 1989, 81:1879-1886.
59. Chen J, Pee D, Ayyagari R, Graubard B, Schairer C, Byrne C, Benichou J, Gail MH. Projecting absolute invasive breast cancer risk in white women with a model that includes mammographic density. J Natl Cancer Inst 2006, 98:1215-1226.
60. Tice JA, Cummings SR, Smith-Bindman R, Ichikawa L, Barlow WE, Kerlikowske K. Using clinical risk factors and mammographic breast density to estimate breast cancer risk: development and validation of a new predictive model. Ann Intern Med 2008, 148:337-347.
61. Martin LJ, Li Q, Melnichouk O, Greenberg C, Minkin S, Hislop G, Boyd NF. A randomized trial of dietary intervention for breast cancer prevention. Cancer Res 2011, 71:123-133.
62. Prentice RL. Surrogate endpoints in clinical trials: Definition and operational criteria. Stat Med 1988, 8:431-440.
63. Schatzkin A, Gail M. The promise and peril of surrogate end points in cancer research. Nat Rev Cancer 2002, 2:19-27.
64. Cuzick J, Warwick J, Pinney E, Duffy SW, Cawthorn S, Howell A, Forbes JF, Warren RM. Tamoxifen-induced reduction in mammographic density and breast cancer risk reduction: a nested case-control study. J Natl Cancer Inst 2011, 103:744-752.
65. Woolcott CG, Courneya KS, Boyd NF, Yaffe MJ, Terry T, McTiernan A, Brant R, Ballard-Barbash R, Irwin ML, Jones CA, Brar S, Campbell KL, McNeely ML, Karvinen KH, Friedenreich CM. Mammographic density change with 1 year of aerobic exercise among postmenopausal women: a randomized controlled trial. Cancer Epidemiol Biomarkers Prev 2010, 19:1112-1121.
66. Kerlikowske K, Cook AJ, Buist DS, Cummings SR, Vachon C, Vacek P, Miglioretti DL. Breast cancer risk by breast density, menopause, and postmenopausal hormone therapy use. J Clin Oncol 2010, 28:3830-3837.
67. Greendale GA, Reboussin BA, Slone S, Wasilauskas C, Pike MC, Ursin G. Postmenopausal hormone therapy and change in mammographic density. J Natl Cancer Inst 2003, 95:30-37.
68. Chlebowski RT, Hendrix SL, Langer RD, Stefanick ML, Gass M, Lane D, Rodabough RJ, Gilligan MA, Cyr MG, Thomson CA, Khandekar J, Petrovitch H, McTiernan A, . WHI Investigators Influence of estrogen plus progestin on breast cancer and mammography in healthy postmenopausal women. The Women's Health Initiative Randomized Trial. JAMA 1989, 289(24):3243-3253. WHI Investigators.
69. Spicer DV, Ursin G, Parisky YR, Pearce JG, Shoupe D, Pike A, Pike MC. Changes in mammographic densities induced by a hormonal contraceptive designed to reduce breast cancer risk. J Natl Cancer Inst 1994, 86:431-436.
70. Yaghjyan L, Colditz GA, Collins LC, Schnitt SJ, Rosner B, Vachon C, Tamimi RM. Mammographic breast density and subsequent risk of breast cancer in postmenopausal women according to tumor characteristics. J Natl Cancer Inst 2011, 103:1179-1189.
71. Conroy SM, Pagano I, Kolonel LN, Maskarinec G. Mammographic density and hormone receptor expression in breast cancer: The Multiethnic Cohort Study. Cancer Epidemiol 2011, 35:448-52.
72. Ding J, Warren R, Girling A, Thompson D, Easton D. Mamographic density, estrogen receptor status and other breast cancer tumor characteristics. Breast J 2010, 16:279-289.
73. Olsen AH, Bihrmann K, Jensen MB, Vejborg I, Lynge E. Breast density and outcome of mammography screening: a cohort study. Br J Cancer 2009, 100:1205-1208.
74. Ziv E, Tice J, Smith-Bindman R, Shepherd J, Cummings S, Kerlikowske K. Mammographic density and estrogen receptor status of breast cancer. Cancer Epidemiol Biomarkers Prev 2004, 13:2090-2095.
75. Ma H, Luo J, Press MF, Wang Y, Berstein L, Ursin G. Is there a difference in the association between percent mammographic density and subtypes of breast cancer? Luminal A and triple-negative breast cancer. Cancer Epidemiol Biomarkers Prev 2009, 18:479-485.
76. Gierach GL, Lissowska J, Garcia-Closas M, Yang XR, Figueroa JD, Anzick S, Wesolowska E, Brinton LA, Meltzer PS, Boyd NF, Sherman ME. Relationship of mammographic density with breast cancer subtypes. Paper presented at: American Association for Cancer Research 101st Annual Meeting; 17-21 April 2010; Washington, DC Abstract 2779.
77. Arora N, King TA, Jacks LM, Stempel MM, Patil S, Morris E, Morrow M. Impact of breast density on the presenting features of malignancy. Ann Surg Oncol 2010, 17:211-218.
78. Yang WT, Dryden M, Broglio K, Gilcrease M, Dawood S, Dempsey PJ, Valero V, Hortobagyi G, Atchley D, Arun B. Mammographic features of triple receptor-negative primary breast cancers in young premenopausal women. Breast Cancer Res Treat 2008, 111:405-410.
79. Cil T, Fishell E, Hanna W, Sun P, Rawlinson E, Narod SA, McCready DR. Mammographic density and the risk of breast cancer recurrence after breast-conserving surgery. Cancer 2009, 115:5780-5787.
80. Ghosh K, Brandt KR, Sellers TA, Reynolds C, Scott CG, Maloney SD, Carston MJ, Pankratz VS, Vachon CM. Association of mammographic density with the pathology of subsequent breast cancer among postmenopausal women. Cancer Epidemiol Biomarkers Prev 2008, 17:872-879.
81. Fasching PA, Heusinger K, Loehberg CR, Wenkel E, Lux MP, Schrauder M, Koscheck T, Bautz W, Schulz-Wendtland R, Beckmann MW, Bani MR. Influence of mammographic density on the diagnostic accuracy of tumor size assessment and association with breast cancer tumor characteristics. Eur J Radiol 2006, 60:398-404.
82. Aiello EJ, Buist DSM, White E, Porter PL. Association between mammographic breast density and breast cancer tumor characteristics. Cancer Epidemiol Biomarkers Prev 2005, 14:662-668.
83. Morishita M, Ohtsuru A, Hayashi T, Isomoto I, Itoyanagi N, Maeda S, Honda S, Yano H, Uga T, Nagayasu T, Kanematsu T, Yamashita S. Clinical significance of categorisation of mammographic density for breast cancer prognosis. Int J Oncol 2005, 26:1307-1312.
84. Roubidoux MA, Bailey JE, Wray LA, Helvie MA. Invasive cancers detected after breast cancer screening yielded a negative result: relationship of mammographic density to tumor prognostic factors. Radiology 2004, 230:42-48.
85. Hinton CP, Roebuck EJ, Williams MR, Blamey RW, Glaves J, Nicholson RI, Griffiths K. Mammographic parenchymal patterns: value as a predictor of hormone dependency and survival in breast cancer. AJR Am J Roentgenol 1985, 144:1103-1107.
86. Nickson C, Kavanagh AM. Tumour size at detection according to different measures of mammographic breast density. J Med Screen 2009, 16:140-146.
87. Porter GJ, Evans AJ, Cornford EJ, Burrell HC, James JJ, Lee AH, Chakrabarti J. Influence of mammographic parenchymal pattern in screening-detected and interval invasive breast cancers on pathologic features, mammographic features, and patient survival. AJR Am J Roentgenol 2007, 188:676-683.
88. Sala E, Solomon L, Warren R, McCann J, Duffy S, Luben R, Day N. Size, node status and grade of breast tumors: association with mammographic parenchymal patterns. Eur Radiol 2000, 10:157-162.
89. Boyd NF, O'Sullivan B, Campbell JE, Fishell E, Simor I, Cooke G, Germanson T. Mammographic patterns and bias in breast cancer detection. Radiology 1982, 143:671-674.
90. Habel LA, Dignam JJ, Land SR, Salane M, Capra AM, Juliano RL. Mammographic density and breast cancer after ductal carcinoma in situ. J Natl Cancer Inst 2004, 96:1467-1472.
91. Habel LA, Capra AM, Achacoso NS, Janga A, Acton L, Puligandla B, Quesenberry CP. Mammographic density and risk of second breast cancer after ductal carcinoma in situ. Cancer Epidemiol Biomarkers Prev 2010, 19:2488-2495.
92. Park CC, Rembert J, Chew K, Moore D, Kerlikowske K. High mammographic breast density is independent predictor of local but not distant recurrence after lumpectomy and radiotherapy for invasive breast cancer. Int J Radiat Oncol Biol Phys 2009, 73:75-79.
93. Hwang ES, Miglioretti DL, Ballard-Barbash R, Weaver DL, Kerlikowske K, . National Cancer Institute Breast Cancer Surveillance Consortium Association between breast density and subsequent breast cancer following treatment for ductal carcinoma in situ. Cancer Epidemiol Biomark Prev 2007, 16(12):2587-2593. National Cancer Institute Breast Cancer Surveillance Consortium.
94. Chiu SY, Duffy S, Yen AM, Tabár L, Smith RA, Chen HH. Effect of baseline breast density on breast cancer incidence, stage, mortality, and screening parameters: 25-year follow-up of a Swedish mammographic screening. Cancer Epidemiol Biomarkers Prev 2010, 19:1219-1228.