Advertisement

European Radiology

, Volume 29, Issue 4, pp 1762–1777 | Cite as

Breast density implications and supplemental screening

  • Athina VourtsisEmail author
  • Wendie A. Berg
Breast

Abstract

Digital breast tomosynthesis (DBT) has been widely implemented in place of 2D mammography, although it is less effective in women with extremely dense breasts. Breast ultrasound detects additional early-stage, invasive breast cancers when combined with mammography; however, its relevant limitations, including the shortage of trained operators, operator dependence and small field of view, have limited its widespread implementation. Automated breast sonography (ABS) is a promising technique but the time to interpret and false-positive rates need to be improved. Supplemental screening with contrast-enhanced magnetic resonance imaging (MRI) in high-risk women reduces late-stage disease; abbreviated MRI protocols may reduce cost and increase accessibility to women of average risk with dense breasts. Contrast-enhanced digital mammography (CEDM) and molecular breast imaging improve cancer detection but require further validation for screening and direct biopsy guidance should be implemented for any screening modality. This article reviews the status of screening women with dense breasts.

Key Points

• The sensitivity of mammography is reduced in women with dense breasts. Supplemental screening with US detects early-stage, invasive breast cancers.

• Tomosynthesis reduces recall rate and increases cancer detection rate but is less effective in women with extremely dense breasts.

• Screening MRI improves early diagnosis of breast cancer more than ultrasound and is currently recommended for women at high risk. Risk assessment is needed, to include breast density, to ascertain who should start early annual MRI screening.

Keywords

Breast density Screening ultrasound Breast cancer Tomosynthesis Magnetic resonance imaging 

Abbreviations

ABS

Three-Dimensional Automated Breast Sonography

ACRIN

American College of Radiology Imaging Network

ASTOUND

Adjunct Screening with Tomosynthesis or Ultrasound in women with mammography-Negative Dense breasts trial

BCSC

Breast Cancer Surveillance Consortium

BI-RADS

Breast Imaging Reporting and Data System

CESM

Contrast-enhanced spectral mammography

DBT

Digital breast tomosynthesis

DCIS

Ductal carcinoma in situ

EASY

European Asymptomatic Screening Study

ER

Estrogen receptor

EUSOBI

European Society of Breast Imaging

GC-HBOC

German Consortium for Hereditary Breast and Ovarian Cancer

HHUS

Hand-held ultrasound

ICDR

Incremental cancer detection rate

MBI

Molecular breast imaging

MRI

Magnetic resonance imaging

NCCN

National Comprehensive Cancer Network

PHBC

Personal history of breast cancer

PPV

Positive predictive value

STORM

Screening with Tomosynthesis or Standard Mammography trial

US

Ultrasound

Notes

Funding

WAB received support from National Institutes of Health grant 1R01CA187593.

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is: Wendie A. Berg, MD, PhD, Department of Radiology, University of Pittsburgh School of Medicine, Magee-Womens Hospital of UPMC, Pittsburgh, PA, USA.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was not required for this study because this is a review article.

Ethical approval

Institutional Review Board approval was not required because this is a review article.

Methodology

• Review article

References

  1. 1.
    Oeffinger KC, Fontham ET, Etzioni R et al (2015) Breast cancer screening for women at average risk: 2015 guideline update from the american cancer society. JAMA 314:1599–1614CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Tabár L, Vitak B, Chen TH et al (2011) Swedish two-county trial: impact of mammographic screening on breast cancer mortality during 3 decades. Radiology 260:658–663CrossRefPubMedGoogle Scholar
  3. 3.
    Coldman A, Phillips N, Wilson C et al (2014) Pan-Canadian study of mammography screening and mortality from breast cancer. J Natl Cancer Inst 106:dju404.  https://doi.org/10.1093/jnci/dju404
  4. 4.
    Broeders M, Moss S, Nyström L et al (2012) The impact of mammographic screening on breast cancer mortality in Europe: a review of observational studies. J Med Screen 19(Suppl 1):14–25CrossRefPubMedGoogle Scholar
  5. 5.
    Tabár L, Yen AM, Wu WY et al (2015) Insights from the breast cancer screening trials: how screening affects the natural history of breast cancer and implications for evaluating service screening programs. Breast J 21:13–20CrossRefPubMedGoogle Scholar
  6. 6.
    Brekelmans CT, Seynaeve C, Bartels CC et al (2001) Effectiveness of breast cancer surveillance in BRCA1/2 gene mutation carriers and women with high familial risk. J Clin Oncol 19:924–930CrossRefPubMedGoogle Scholar
  7. 7.
    Tilanus-Linthorst M, Verhoog L, Obdeijn IM et al (2002) A BRCA1/2 mutation, high breast density and prominent pushing margins of a tumor independently contribute to a frequent false-negative mammography. Int J Cancer 102:91–95CrossRefPubMedGoogle Scholar
  8. 8.
    Komenaka IK, Ditkoff BA, Joseph KA et al (2004) The development of interval breast malignancies in patients with BRCA mutations. Cancer 100:2079–2083CrossRefPubMedGoogle Scholar
  9. 9.
    Boyd NF, Guo H, Martín LJ et al (2007) Mammographic density and the risk and detection of breast cancer. N Engl J Med 356:227–236CrossRefPubMedGoogle Scholar
  10. 10.
    Houssami N, Abraham LA, Miglioretti DL et al (2011) Accuracy and outcomes of screening mammography in women with a personal history of early-stage breast cancer. JAMA 305:790–799CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Berg WA (2016) Current status of supplemental screening in dense breasts. J Clin Oncol 34:1840–1843Google Scholar
  12. 12.
    Wolfe JN (1976) Breast patterns as an index of risk for developing breast cancer. AJR Am J Roentgenol 126:1130–1137CrossRefPubMedGoogle Scholar
  13. 13.
    van der Waal D, Ripping TM, Verbeek AL, Broeders MJ (2017) Breast cancer screening effect across breast density strata: a case-control study. Int J Cancer 140:41–49CrossRefPubMedGoogle Scholar
  14. 14.
    Gram IT, Funkhouser E, Tabár L (1997) The Tabár classification of mammographic parenchymal patterns. Eur J Radiol 24:131–136CrossRefPubMedGoogle Scholar
  15. 15.
    Chiu SY, Duffy S, Yen AM, Tabár L, Smith RA, Chen HH (2010) 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 19:1219–1228CrossRefPubMedGoogle Scholar
  16. 16.
    McCormack VA, dos Santos Silva I (2006) Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 15:1159–1169CrossRefPubMedGoogle Scholar
  17. 17.
    Sickles EA, D'Orsi CJ, Bassett LW et al (2013) ACR BI-RADS Mammography. In: D’Orsi CJ, Sickles EA, Mendelson EB, Morris EA (eds) ACR BI-RADS Atlas, Breast Imaging Reporting and Data System. American College of Radiology, Reston, VAGoogle Scholar
  18. 18.
    Sprague BL, Gangnon RE, Burt V et al (2014) Prevalence of mammographically dense breasts in the United States. J Natl Cancer Inst 106:ju255Google Scholar
  19. 19.
    Gubern-Mérida A, Kallenberg M, Platel B, Mann RM, Martí R, Karssemeijer N (2014) Volumetric breast density estimation from full-field digital mammograms: a validation study. PLoS One 9:e85952CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Alonzo-Proulx O, Mawdsley GE, Patrie JT, Yaffe MJ, Harvey JA (2015) Reliability of automated breast density measurements. Radiology 275:366–376CrossRefPubMedGoogle Scholar
  21. 21.
    Ekpo EU, McEntee MF (2014) Measurement of breast density with digital breast tomosynthesis--a systematic review. Br J Radiol 87:20140460CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Destounis S, Arieno A, Morgan R, Roberts C, Chan A (2017) Qualitative versus quantitative mammographic breast density assessment: Applications for the US and abroad. Diagnostics (Basel) 7:30Google Scholar
  23. 23.
    Engmann NJ, Golmakani MK, Miglioretti DL, Sprague BL, Kerlikowske K, for the Breast Cancer Surveillance Consortium (2017) Population-attributable risk proportion of clinical risk factors for breast cancer. JAMA Oncol 3:1228–1236Google Scholar
  24. 24.
    Warwick J, Birke H, Stone J et al (2014) Mammographic breast density refines Tyrer-Cuzick estimates of breast cancer risk in high-risk women: findings from the placebo arm of the International Breast Cancer Intervention Study I. Breast Cancer Res 16:451CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Kerlikowske K, Ma L, Scott CG et al (2017) Combining quantitative and qualitative breast density measures to assess breast cancer risk. Breast Cancer Res 19:97CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bae MS, Moon WK, Chang JM et al (2014) Breast cancer detected with screening US: reasons for nondetection at mammography. Radiology 270:369–377CrossRefPubMedGoogle Scholar
  27. 27.
    Hooley RJ, Greenberg KL, Stackhouse RM, Geisel JL, Butler RS, Philpotts LE (2012) Screening US in patients with mammographically dense breasts: initial experience with Connecticut Public Act 09-41. Radiology 265:59–69CrossRefPubMedGoogle Scholar
  28. 28.
    Kolb TM, Lichy J, Newhouse JH (2002) Comparison of the performance of screening mammography, physical examination, and breast US and evaluation of factors that influence them: an analysis of 27,825 patient evaluations. Radiology 225:165–175CrossRefPubMedGoogle Scholar
  29. 29.
    Carney PA, Miglioretti DL, Yankaskas BC et al (2003) Individual and combined effects of age, breast density, and hormone replacement therapy use on the accuracy of screening mammography. Ann Intern Med 138:168–175CrossRefPubMedGoogle Scholar
  30. 30.
    Kerlikowske K, Hubbard RA, Miglioretti DL et al (2011) Comparative effectiveness of digital versus film-screen mammography in community practice in the United States: a cohort study. Ann Intern Med 155:493–502CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Berg WA (2009) Tailored supplemental screening for breast cancer: what now and what next? AJR Am J Roentgenol 192:390–399CrossRefPubMedGoogle Scholar
  32. 32.
    Roubidoux MA, Bailey JE, Wray LA, Helvie MA (2004) Invasive cancers detected after breast cancer screening yielded a negative result: relationship of mammographic density to tumor prognostic factors. Radiology 230:42–48CrossRefPubMedGoogle Scholar
  33. 33.
    Pisano ED, Gatsonis C, Hendrick E et al (2005) Diagnostic performance of digital versus film mammography for breast-cancer screening. N Engl J Med 353:1773–1783CrossRefPubMedGoogle Scholar
  34. 34.
    Sardanelli F, Aase HS, Álvarez M et al (2017) Position paper on screening for breast cancer by the European Society of Breast Imaging (EUSOBI) and 30 national breast radiology bodies from Austria, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, Czech Republic, Denmark, Estonia, Finland, France, Germany, Greece, Hungary, Iceland, Ireland, Italy, Israel, Lithuania, Moldova, The Netherlands, Norway, Poland, Portugal, Romania, Serbia, Slovakia, Spain, Sweden, Switzerland and Turkey. Eur Radiol 27:2737–2743CrossRefPubMedGoogle Scholar
  35. 35.
    Niklason LT, Christian BT, Niklason LE et al (1997) Digital tomosynthesis in breast imaging. Radiology 205:399–406CrossRefPubMedGoogle Scholar
  36. 36.
    Machida Y, Saita A, Namba H, Fukuma E (2016) Automated volumetric breast density estimation out of digital breast tomosynthesis data: feasibility study of a new software version. Springerplus 5:780CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Ciatto S, Houssami N, Bernardi D et al (2013) Integration of 3D digital mammography with tomosynthesis for population breast-cancer screening (STORM): a prospective comparison study. Lancet Oncol 14:583–589CrossRefPubMedGoogle Scholar
  38. 38.
    Skaane P, Bandos AI, Gullien R et al (2013) Prospective trial comparing full-field digital mammography (FFDM) versus combined FFDM and tomosynthesis in a population-based screening programme using independent double reading with arbitration. Eur Radiol 23:2061–2071CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Lång K, Andersson I, Rosso A, Tingberg A, Timberg P, Zackrisson S (2016) Performance of one-view breast tomosynthesis as a stand-alone breast cancer screening modality: results from the Malmö Breast Tomosynthesis Screening Trial, a population-based study. Eur Radiol 26:184–190Google Scholar
  40. 40.
    Friedewald SM, Rafferty EA, Rose SL et al (2014) Breast cancer screening using tomosynthesis in combination with digital mammography. JAMA 311:2499–2507CrossRefPubMedGoogle Scholar
  41. 41.
    Rafferty EA, Durand MA, Conant EF et al (2016) Breast cancer screening using tomosynthesis and digital mammography in mense and nondense breasts. JAMA 315:1784–1786Google Scholar
  42. 42.
    Kim WH, Chang JM, Lee J et al (2017) Diagnostic performance of tomosynthesis and breast ultrasonography in women with dense breasts: a prospective comparison study. Breast Cancer Res Treat 162:85–94CrossRefPubMedGoogle Scholar
  43. 43.
    Houssami N (2015) Digital breast tomosynthesis (3D-mammography) screening: data and implications for population screening. Expert Rev Med Devices 12:377–379CrossRefPubMedGoogle Scholar
  44. 44.
    McDonald ES, Oustimov A, Weinstein SP, Synnestvedt MB, Schnall M, Conant EF (2016) Effectiveness of digital breast tomosynthesis compared with digital mammography: Outcomes analysis from 3 years of breast cancer screening. JAMA Oncol 2:737–743CrossRefPubMedGoogle Scholar
  45. 45.
    Corsetti V, Houssami N, Ferrari A et al (2008) Breast screening with ultrasound in women with mammography-negative dense breasts: evidence on incremental cancer detection and false positives. and associated cost. Eur J Cancer 44:539–544CrossRefPubMedGoogle Scholar
  46. 46.
    Scheel JR, Lee JM, Sprague BL, Lee CI, Lehman CD (2015) Screening ultrasound as an adjunct to mammography in women with mammographically dense breasts. Am J Obstet Gynecol 212:9–17CrossRefPubMedGoogle Scholar
  47. 47.
    Berg WA, Blume JD, Cormack JB et al (2008) Combined screening with ultrasound and mammography vs mammography alone in women at elevated risk of breast cancer. JAMA 299:2151–2163CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Berg WA, Zhang Z, Lehrer D et al (2012) Detection of breast cancer with addition of annual screening ultrasound or a single screening MRI to mammography in women with elevated breast cancer risk. JAMA 307:1394–1404CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Buchberger W, Niehoff A, Obrist P, DeKoekkoek-Doll P, Dünser M (2000) Clinically and mammographically occult breast lesions: detection and classification with high-resolution sonography. Semin Ultrasound CT MR 21:325–336CrossRefPubMedGoogle Scholar
  50. 50.
    Sprague BL, Stout NK, Schechter C et al (2015) Benefits, harms, and cost-effectiveness of supplemental ultrasonography screening for women with dense breasts. Ann Intern Med 162:157–166CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Gordon PB, Goldenberg SL (1995) Malignant breast masses detected only by ultrasound. A retrospective review. Cancer 76:626–630CrossRefPubMedGoogle Scholar
  52. 52.
    Kaplan SS (2001) Clinical utility of bilateral whole-breast US in the evaluation of women with dense breast tissue. Radiology 221:641–649CrossRefPubMedGoogle Scholar
  53. 53.
    Leconte I, Feger C, Galant C et al (2003) Mammography and subsequent whole-breast sonography of nonpalpable breast cancers: the importance of radiologic breast density. AJR Am J Roentgenol 180:1675–1679CrossRefPubMedGoogle Scholar
  54. 54.
    Crystal P, Strano SD, Shcharynski S, Koretz MJ (2003) Using sonography to screen women with mammographically dense breasts. AJR Am J Roentgenol 181:177–182CrossRefPubMedGoogle Scholar
  55. 55.
    Wilczek B, Wilczek HE, Rasouliyan L, Leifland K (2016) Adding 3D automated breast ultrasound to mammography screening in women with heterogeneously and extremely dense breasts: Report from a hospital-based, high-volume, single-center breast cancer screening program. Eur J Radiol 85:1554–1563CrossRefPubMedGoogle Scholar
  56. 56.
    Kelly KM, Dean J, Comulada WS, Lee SJ (2010) Breast cancer detection using automated whole breast ultrasound and mammography in radiographically dense breasts. Eur Radiol 20:734–742CrossRefPubMedGoogle Scholar
  57. 57.
    Brem RF, Tabár L, Duffy SW et al (2015) Assessing improvement in detection of breast cancer with three-dimensional automated breast US in women with dense breast tissue: the SomoInsight Study. Radiology 274:663-673.Google Scholar
  58. 58.
    Ohuchi N, Suzuki A, Sobue T et al (2016) Sensitivity and specificity of mammography and adjunctive ultrasonography to screen for breast cancer in the Japan Strategic Anti-cancer Randomized Trial (J-START): a randomised controlled trial. Lancet 387:341–348CrossRefPubMedGoogle Scholar
  59. 59.
    Weigert JM (2017) The connecticut experiment; the third installment: 4 years of screening women with dense breasts with bilateral ultrasound. Breast J 23:34–39CrossRefPubMedGoogle Scholar
  60. 60.
    Bae MS, Han W, Koo HR et al (2011) Characteristics of breast cancers detected by ultrasound screening in women with negative mammograms. Cancer Sci 102:1862–1867CrossRefPubMedGoogle Scholar
  61. 61.
    Parris T, Wakefield D, Frimmer H (2013) Real world performance of screening breast ultrasound following enactment of Connecticut Bill 458. Breast J 19:64–70Google Scholar
  62. 62.
    Chang JM, Koo HR, Moon WK (2015). Radiologist-performed hand-held ultrasound screening at average risk of breast cancer: results from a single health screening center. Acta Radiol 56:652–658Google Scholar
  63. 63.
    Moon HJ, Jung I, Park SJ, Kim MJ, Youk JH, Kim EK (2015) Comparison of cancer yields and diagnostic performance of screening mammography vs. supplemental screening ultrasound in 4394 women with average risk for breast cancer. Ultraschall Med 36:255–263Google Scholar
  64. 64.
    Kim SY, Han BK, Kim EK et al (2017) Breast cancer detected at screening us: survival rates and clinical-pathologic and imaging factors associated with recurrence. Radiology 284:354–364CrossRefPubMedGoogle Scholar
  65. 65.
    Corsetti V, Houssami N, Ghirardi M et al (2011) Evidence of the effect of adjunct ultrasound screening in women with mammography-negative dense breasts: interval breast cancers at 1 year follow-up. Eur J Cancer 47:1021–1026CrossRefPubMedGoogle Scholar
  66. 66.
    Berg WA, Mendelson EB (2014) Technologist-performed handheld screening breast US imaging: how is it performed and what are the outcomes to date? Radiology 272:12–27CrossRefPubMedGoogle Scholar
  67. 67.
    Bosch AM, Kessels AG, Beets GL et al (2003) Interexamination variation of whole breast ultrasound. Br J Radiol 76:328–331CrossRefPubMedGoogle Scholar
  68. 68.
    Berg WA, Blume JD, Cormack JB, Mendelson EB (2006) Operator dependence of physician-performed whole-breast US: lesion detection and characterization. Radiology 241:355–365CrossRefPubMedGoogle Scholar
  69. 69.
    Berg WA, Blume JD, Cormack JB, Mendelson EB, Madsen EL, Investigators A (2006) Lesion detection and characterization in a breast US phantom: results of the ACRIN 6666 Investigators. Radiology 239:693–702CrossRefPubMedGoogle Scholar
  70. 70.
    Vourtsis A, Kachulis A (2018) The performance of 3D ABUS versus HHUS in the visualisation and BI-RADS characterisation of breast lesions in a large cohort of 1,886 women. Eur Radiol 28:592–601CrossRefPubMedGoogle Scholar
  71. 71.
    Skaane P, Gullien R, Eben EB, Sandhaug M, Schulz-Wendtland R, Stoeblen F (2015) Interpretation of automated breast ultrasound (ABUS) with and without knowledge of mammography: a reader performance study. Acta Radiol 56:404–412CrossRefPubMedGoogle Scholar
  72. 72.
    Moon WK, Shen YW, Huang CS et al (2011) Comparative study of density analysis using automated whole breast ultrasound and MRI. Med Phys 38:382–389CrossRefPubMedGoogle Scholar
  73. 73.
    Moon WK, Lo CM, Chang JM et al (2013) Rapid breast density analysis of partial volumes of automated breast ultrasound images. Ultrason Imaging 35:333–343CrossRefPubMedGoogle Scholar
  74. 74.
    Giger ML, Inciardi MF, Edwards A et al (2016) Automated Breast Ultrasound in Breast Cancer Screening of Women With Dense Breasts: Reader Study of Mammography-Negative and Mammography-Positive Cancers. AJR Am J Roentgenol 206:1341–1350CrossRefPubMedGoogle Scholar
  75. 75.
    Kim EJ, Kim SH, Kang BJ, Kim YJ (2014) Interobserver agreement on the interpretation of automated whole breast ultrasonography. Ultrasonography 33:252–258CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Wang HY, Jiang YX, Zhu QL et al (2012) Differentiation of benign and malignant breast lesions: a comparison between automatically generated breast volume scans and handheld ultrasound examinations. Eur J Radiol 81:3190–3200CrossRefPubMedGoogle Scholar
  77. 77.
    Jiang Y, Inciardi MF, Edwards AV, Papaioannou J (2018) Interpretation time using a concurrent-read computer-aided detection system for automated breast ultrasound in breast cancer screening of women with dense breast tissue. AJR Am J Roentgenol 211:452–461Google Scholar
  78. 78.
    van Zelst JCM, Tan T, Clauser P et al (2018) Dedicated computer-aided detection software for automated 3D breast ultrasound; an efficient tool for the radiologist in supplemental screening of women with dense breasts. Eur Radiol 28:2996-3006Google Scholar
  79. 79.
    Tagliafico AS, Calabrese M, Mariscotti G et al (2016) Adjunct Screening with Tomosynthesis or ultrasound in women with Mammography-Negative Dense Breasts: Interim report of a prospective comparative trial. J Clin Oncol 34:1882–1888Google Scholar
  80. 80.
    Destounis S, Arieno A, Morgan R (2017) Comparison of cancers detected by screening ultrasound and digital breast tomosynthesis. Abstract 3162. The American Roentgen Ray Society (ARRS) 2017 Annual Meeting (2017) New Orleans, LAGoogle Scholar
  81. 81.
    Dense-Breast.Info (2017) Comparison of Cancers Detected by Screening Breast Ultrasound and Digital Breast Tomosynthesis. http://densebreast-info.org/img/hottopic_destounis_arrs_2017_comparisonbymodality.pdf (accessed on Jan 30, 2018)
  82. 82.
    Saslow D, Boetes C, Burke W et al (2007) American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin 57:75–89CrossRefPubMedGoogle Scholar
  83. 83.
    National Comprehensive Cancer Network (NCCN) (2018) NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines). Genetic/Familial High-Risk Assessment: Breast and Ovarian. NCCN, Fort Washington, PAGoogle Scholar
  84. 84.
    National Comprehensive Cancer Network (NCCN) (2018) NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines). Breast Cancer Screening and Diagnosis. NCCN, Fort Washington, PAGoogle Scholar
  85. 85.
    Monticciolo DL, Newell MS, Moy L, Niell B, Monsees B, Sickles EA (2018) Breast cancer screening in women at higher-than-average risk: recommendations from the ACR. J Am Coll Radiol 15:408–414CrossRefPubMedGoogle Scholar
  86. 86.
    King V, Brooks JD, Bernstein JL, Reiner AS, Pike MC, Morris EA (2011) Background parenchymal enhancement at breast MR imaging and breast cancer risk. Radiology 260:50–60CrossRefPubMedGoogle Scholar
  87. 87.
    Sak MA, Littrup PJ, Duric N, Mullooly M, Sherman ME, Gierach GL (2015) Current and future methods for measuring breast density: a brief comparative review. Breast Cancer Manag 4:209–221CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Warner E, Messersmith H, Causer P, Eisen A, Shumak R, Plewes D (2008) Systematic review: using magnetic resonance imaging to screen women at high risk for breast cancer. Ann Intern Med 148:671–679CrossRefPubMedGoogle Scholar
  89. 89.
    Lo G, Scaranelo AM, Aboras H et al (2017) Evaluation of the Utility of Screening Mammography for High-Risk Women Undergoing Screening Breast MR Imaging. Radiology 285:36–43CrossRefPubMedGoogle Scholar
  90. 90.
    Riedl CC, Luft N, Bernhart C et al (2015) Triple-modality screening trial for familial breast cancer underlines the importance of magnetic resonance imaging and questions the role of mammography and ultrasound regardless of patient mutation status, age, and breast density. J Clin Oncol 33:1128–1135CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    van Zelst JCM, Mus RDM, Woldringh G et al (2017) Surveillance of women with the BRCA1 or BRCA2 mutation by using biannual automated breast US, MR imaging, and mammography. Radiology 285:376–388CrossRefPubMedGoogle Scholar
  92. 92.
    Heijnsdijk EA, Warner E, Gilbert FJ et al (2012) 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 21:1458–1468CrossRefPubMedGoogle Scholar
  93. 93.
    Lehman CD, Blume JD, Weatherall P et al (2005) Screening women at high risk for breast cancer with mammography and magnetic resonance imaging. Cancer 103:1898–1905CrossRefPubMedGoogle Scholar
  94. 94.
    Leach MO, Boggis CR, Dixon AK et al (2005) 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 365:1769–1778CrossRefPubMedGoogle Scholar
  95. 95.
    Kuhl CK, Schrading S, Leutner CC et al (2005) Mammography, breast ultrasound, and magnetic resonance imaging for surveillance of women at high familial risk for breast cancer. J Clin Oncol 23:8469–8476CrossRefPubMedGoogle Scholar
  96. 96.
    National Institute for Health and Care Excellence (2013) Familial breast cancer: classification, care and managing breast cancer and related risks in people with a family history of breast cancer. (Clinical guideline 164). https://www.nice.org.uk/guidance/CG164 (accessed on September 01, 2017)
  97. 97.
    Meindl A, Ditsch N, Kast K, Rhiem K, Schmutzler RK (2011) Hereditary breast and ovarian cancer: new genes, new treatments, new concepts. Dtsch Arztebl Int 108:323–330PubMedPubMedCentralGoogle Scholar
  98. 98.
    Foulkes WD, Chappuis PO, Wong N et al (2000) Primary node negative breast cancer in BRCA1 mutation carriers has a poor outcome. Ann Oncol 11:307–313CrossRefPubMedGoogle Scholar
  99. 99.
    Tilanus-Linthorst MM, Kriege M, Boetes C et al (2005) Hereditary breast cancer growth rates and its impact on screening policy. Eur J Cancer 41:1610–1617CrossRefPubMedGoogle Scholar
  100. 100.
    Bick U (2015) Intensified surveillance for early detection of breast cancer in high-risk patients. Breast Care (Basel) 10:13–20CrossRefGoogle Scholar
  101. 101.
    Le-Petross HT, Whitman GJ, Atchley DP et al (2011) Effectiveness of alternating mammography and magnetic resonance imaging for screening women with deleterious BRCA mutations at high risk of breast cancer. Cancer 117:3900–3907CrossRefPubMedGoogle Scholar
  102. 102.
    Cott Chubiz JE, Lee JM, Gilmore ME et al (2013) Cost-effectiveness of alternating magnetic resonance imaging and digital mammography screening in BRCA1 and BRCA2 gene mutation carriers. Cancer 119:1266–1276CrossRefPubMedGoogle Scholar
  103. 103.
    Phi XA, Houssami N, Hooning MJ et al (2017) Accuracy of screening women at familial risk of breast cancer without a known gene mutation: Individual patient data meta-analysis. Eur J Cancer 85:31–38Google Scholar
  104. 104.
    Kuhl CK, Strobel K, Bieling H, Leutner C, Schild HH, Schrading S (2017) Supplemental breast MR imaging screening of women with average risk of breast cancer. Radiology 283:361–370CrossRefPubMedGoogle Scholar
  105. 105.
    O'Neill SM, Rubinstein WS, Sener SF et al (2009) Psychological impact of recall in high-risk breast MRI screening. Breast Cancer Res Treat 115:365–371CrossRefPubMedGoogle Scholar
  106. 106.
    Lehman CD (2006) Role of MRI in screening women at high risk for breast cancer. J Magn Reson Imaging 24:964–970CrossRefPubMedGoogle Scholar
  107. 107.
    Warren RM, Pointon L, Caines R et al (2002) What is the recall rate of breast MRI when used for screening asymptomatic women at high risk? Magn Reson Imaging 20:557–565CrossRefPubMedGoogle Scholar
  108. 108.
    Warner E, Hill K, Causer P et al (2011) Prospective study of breast cancer incidence in women with a BRCA1 or BRCA2 mutation under surveillance with and without magnetic resonance imaging. J Clin Oncol 29:1664–1669CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Schacht DV, Yamaguchi K, Lai J, Kulkarni K, Sennett CA, Abe H (2014) Importance of a personal history of breast cancer as a risk factor for the development of subsequent breast cancer: results from screening breast MRI. AJR Am J Roentgenol 202:289–292CrossRefPubMedGoogle Scholar
  110. 110.
    Weinstock C, Campassi C, Goloubeva O et al (2015) Breast magnetic resonance imaging (MRI) surveillance in breast cancer survivors. Springerplus 4:459CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Giess CS, Poole PS, Chikarmane SA, Sippo DA, Birdwell RL (2015) Screening breast MRI in patients previously treated for breast cancer: diagnostic yield for cancer and abnormal interpretation rate. Acad Radiol 22:1331–1337CrossRefPubMedGoogle Scholar
  112. 112.
    Gweon HM, Cho N, Han W et al (2014) Breast MR imaging screening in women with a history of breast conservation therapy. Radiology 272:366–373CrossRefPubMedGoogle Scholar
  113. 113.
    Lehman CD, Lee JM, DeMartini WB et al (2016) Screening MRI in women with a personal history of breast cancer. J Natl Cancer Inst 108:djv349Google Scholar
  114. 114.
    Cho N, Han W, Han BK et al (2017) Breast cancer screening with mammography plus ultrasonography or magnetic resonance imaging in women 50 years or younger at diagnosis and treated with breast conservation therapy. JAMA Oncol 3:1495–1502CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Berg WA, Blume JD, Adams AM et al (2010) Reasons women at elevated risk of breast cancer refuse breast MR imaging screening: ACRIN 6666. Radiology 254:79-87.Google Scholar
  116. 116.
    U.S. Food and Drug Administration (2017) FDA Drug Safety Communication: FDA warns that gadolinium-based contrast agents (GBCAs) are retained in the body; requires new class warnings. https://www.fda.gov/Drugs/DrugSafety/ucm589213.htm (accessed on April 03, 2018)
  117. 117.
    Radbruch A (2018) Gadolinium deposition in the brain: We need to differentiate between chelated and dechelated gadolinium. Radiology 288:434–435Google Scholar
  118. 118.
    Kuhl CK, Schrading S, Strobel K, Schild HH, Hilgers RD, Bieling HB (2014) Abbreviated breast magnetic resonance imaging (MRI): first postcontrast subtracted images and maximum-intensity projection-a novel approach to breast cancer screening with MRI. J Clin Oncol 32:2304–2310CrossRefPubMedGoogle Scholar
  119. 119.
    Jain M, Jain A, Hyzy MD, Werth G (2017) Fast MRI breast screening revisited. J Med Imaging Radiat Oncol 61:24–28CrossRefPubMedGoogle Scholar
  120. 120.
    Strahle DA, Pathak DR, Sierra A, Saha S, Strahle C, Devisetty K (2017) Systematic development of an abbreviated protocol for screening breast magnetic resonance imaging. Breast Cancer Res Treat 162:283–295CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Panigrahi B, Mullen L, Falomo E, Panigrahi B, Harvey S (2017) An abbreviated protocol for high-risk screening breast magnetic resonance imaging: impact on performance metrics and BI-RADS assessment. Acad Radiol 24:1132–1138CrossRefPubMedGoogle Scholar
  122. 122.
    Choi BH, Choi N, Kim MY, Yang JH, Yoo YB, Jung HK (2018) Usefulness of abbreviated breast MRI screening for women with a history of breast cancer surgery. Breast Cancer Res Treat 167:495–502CrossRefPubMedGoogle Scholar
  123. 123.
    Chen SQ, Huang M, Shen YY, Liu CL, Xu CX (2017) Abbreviated MRI protocols for detecting breast cancer in women with dense breasts. Korean J Radiol 18:470–475CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Mori M, Akashi-Tanaka S, Suzuki S et al (2017) Diagnostic accuracy of contrast-enhanced spectral mammography in comparison to conventional full-field digital mammography in a population of women with dense breasts. Breast Cancer 24:104–110CrossRefPubMedGoogle Scholar
  125. 125.
    Jochelson MS, Pinker K, Dershaw DD et al (2017) Comparison of screening CEDM and MRI for women at increased risk for breast cancer: A pilot study. Eur J Radiol 97:37–43CrossRefPubMedGoogle Scholar
  126. 126.
    McDonald ES, Hammersley JA, Chou SH et al (2016) Performance of DWI as a rapid unenhanced technique for detecting mammographically occult breast cancer in elevated-risk women with dense breasts. AJR Am J Roentgenol 207:205–216CrossRefPubMedGoogle Scholar
  127. 127.
    Partridge S (2018) Breast DWI Potential and Pitfalls: Results of ACRIN 6702 and 6698 Multicenter Trials. The 6th International Congress on Magnetic Resonance ImagingGoogle Scholar
  128. 128.
    Hruska CB (2017) Molecular breast imaging for screening in dense breasts: state of the art and future directions. AJR Am J Roentgenol 208:275–283CrossRefPubMedGoogle Scholar
  129. 129.
    Rhodes DJ, Hruska CB, Phillips SW, Whaley DH, O'Connor MK (2011) Dedicated dual-head gamma imaging for breast cancer screening in women with mammographically dense breasts. Radiology 258:106–118CrossRefPubMedGoogle Scholar
  130. 130.
    Rhodes DJ, Hruska CB, Conners AL et al (2015) Journal club: molecular breast imaging at reduced radiation dose for supplemental screening in mammographically dense breasts. AJR Am J Roentgenol 204:241–251CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    Shermis RB, Wilson KD, Doyle MT et al (2016) Supplemental breast cancer screening with molecular breast imaging for women with dense breast tissue. AJR Am J Roentgenol 207:450–457CrossRefPubMedGoogle Scholar
  132. 132.
    DenseBreast-info. Legislation and Regulations - What is required? http://densebreastinfo.org/legislation.aspx. Accessed 14 Aug 2018

Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  1. 1.“Diagnostic Mammography”, Medical Diagnostic Imaging Unit, Founding President of the Hellenic Breast Imaging SocietyAthensGreece
  2. 2.Department of Radiology, Magee-Womens Hospital of UPMCUniversity of Pittsburgh School of MedicinePittsburghUSA

Personalised recommendations