Complex radiologic imaging of early breast cancer (literature review)


Clinicoroentgenological diagnosis of early breast cancer - BC (non-invasive or invasive small-sized cancers) is difficult due to the absence of any characteristic clinical symptoms and pathognomonic roentgenological signs of the malignant process. Screening of BC has shown to be one of the most successful projects for early diagnosis of malignancies, but the probability to receive false negative results using screening mammography reaches 12%, and, on the one hand, this is due to interval cancers, and on the other hand - to defects in the primary screening. Among the factors associated with the likelihood of ineffective screening of BC, the most authors highlight such as high breast density, preceding the breast biopsy for a benign process, young age, as well as the use of hormone replacement therapy. The main methods of instrumental BC diagnostics are mammography, ultrasound (US), magnetic resonance imaging (MRI) and positron emission tomography (PET). Mammography is the "gold standard" for both screening and best diagnostics, but is characterized by a high proportion of both false positive and false negative results, and this can be partially solved by the use of digital mammography with tomosynthesis (performing a series of mammography images obtained at different angles and producing the focused 3-D images). Contrast enhanced mammography allows to identify angiogenesis in the area of the predicted malignancy, but is characterized by a high radiation exposure. Breast ultrasound is characterized by low specificity of the method and the high dependence of the result of data interpretation depending on physician qualifications. MRI of the breast for screening is characterized by high sensitivity, but also high cost and high proportion of false positive results. The role of PET/computer tomography in the diagnosis of early BC remains unclear, and the informative value of research in patients with nonpalpable tumors is extremely low. The roentgenological picture of early BC is widely variable; characteristic features include the presence of clustered calcifications, lumps with jagged edges, rough multinodular lumps. However, in a significant proportion of women the only manifestation of early BC is the presence of microcalcinates. Careful analysis of the localization and the shape of microcalcinates and basic characteristics allows correctly interpret the roentgenological diagnosis and helps to choose the optimal diagnostic and treatment algorithm.

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About the authors

Giunel S Aliyeva

Blokhin National Medical Research Center of Oncology

Moscow, Russia radiologist

Galina P Korzhenkova

Blokhin National Medical Research Center of Oncology

Moscow, Russia D. Sci. (Med.)

Irina V Kolyadina

Russian Medical Academy of Continuous Professional Education

Moscow, Russia D. Sci. (Med.), Prof.


  1. GLOBOCAN 2018; IACR, WHO, 2018.
  2. Злокачественные новообразования в России в 2017 году (заболеваемость и смертность). Под ред. А.Д.Каприна, В.В.Старинского, Г.В.Петровой. М.: МНИОИ им. П.А. Герцена - филиал ФГБУ «НМИЦ радиологии» Минздрава России, 2018. @@Malignant neoplasms in Russia in 2017 (morbidity and mortality). Ed. A.D.Kaprin, V.V.Stalinskii, G.V.Petrov. Moscow, Herzen MNIOI - branch of NMHC, 2018 (in Russian)
  3. Gotzsche P.C, Jorgensen K.J. Screening for breast cancer with mammography. Cochrane Database Syst Rev 2013; 6: CD001877.
  4. Humphrey L.L, Helfand M, Chan B.K et al. Breast cancer screening: a summary of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med 2002; 137 (5 Part 1): 347-60.
  5. Slawson D.C, Coates M.L. Efficacy of screening mammography. J Fam Pract 1995; 40 (6): 602-3.
  6. Nelson H.D, O'Meara E.S, Kerlikowske K et al. Factors Associated With Rates of False-Positive and False-Negative Results From Digital Mammography Screening: An Analysis of Registry Data. Ann Intern Med 2016; 164 (4): 226-35.
  7. Chan C.H, Coopey S.B, Freer P.E et al. False-negative rate of combined mammography and ultrasound for women with palpable breast masses. Breast Cancer Res Treat 2015; 153 (3): 699-702.
  8. Christiansen C.L, Wang F, Barton M.B et al. Predicting the cumulative risk of false-positive mammograms. J Natl Cancer Ins 2000; 92 (20): 1657-66.
  9. Lång K, Nergården M, Andersson I et al. False positives in breast cancer screening with one-view breast tomosynthesis: An analysis of findings leading to recall, work-up and biopsy rates in the Malmö Breast Tomosynthesis Screening Trial. Eur Radiol 2016; 26 (11): 3899-907.
  10. Hofvind S, Skaane P, Vitak B et al. Influence of review design on percentages of missed interval breast cancers: retrospective study of interval cancers in a population-based screening program. Radiology 2005; 237 (2): 437-43.
  11. Rosenberg K. Ten-year risk of false positive screening mammograms and clinical breast examinations. J Nurse Midwifery 1998; 43 (5): 394-5.
  12. Колядина И.В., Поддубная И.В., Комов Д.В. Скрининг рака молочной железы: мировой опыт и перспективы. Рос. онкологический журн. 2015; 20 (1): 42-6. @@Kolyadina I.V., Poddubnaya I.V., Komov D.V. Skrining raka molochnoi zhelezy: mirovoi opyt i perspektivy. Ros. onkologicheskii zhurn. 2015; 20 (1): 42-6 (in Russian)
  13. Chiou S.Y, Chou Y.H, Chiou H.J et al. Sonographic features of nonpalpable breast cancer: a study based on ultrasound-guided wire-localized surgical biopsies. Ultrasound Med Biol 2006; 32 (9): 1299-306.
  14. Hoff S.R, Abrahamsen A.L, Samset J.H et al. Breast cancer: missed interval and screening-detected cancer at full-field digital mammography and screen-film mammography - results from a retrospective review. Radiology 2012; 264 (2): 378-86.
  15. Mandelson M.T, Oestreicher N, Porter P.L et al. Breast density as a predictor of mammographic detection: comparison of interval- and screen-detected cancers. J Natl Cancer Inst 2000; 92 (13): 1081-7.
  16. Holm J, Humphreys K, Li J et al. Risk factors and tumor characteristics of interval cancers by mammographic density. J Clin Oncol 2015; 33 (9): 1030-7.
  17. Henderson L.M, Hubbard R.A, Sprague B.L et al. Increased Risk of Developing Breast Cancer after a False-Positive Screening Mammogram. Cancer Epidemiol Biomarkers Prev 2015; 24 (12): 1882-9.
  18. Wanders J.O.P, Holland K, Karssemeijer N et al. The effect of volumetric breast density on the risk of screen-detected and interval breast cancers: a cohort study. Breast Cancer Res 2017; 19 (1): 67.
  19. Pettersson A, Graff R.E, Ursin G et al. Mammographic density phenotypes and risk of breast cancer: a meta-analysis. J Natl Cancer Inst 2014; 106 (5).
  20. Meeson S, Young K.C, Wallis M.G et al. Image features of true positive and false negative cancers in screening mammograms. Br J Radiol 2003; 76 (901): 13-21.
  21. Boyd N.F, Huszti E, Melnichouk O et al. Mammographic features associated with interval breast cancers in screening programs. Breast Cancer Res 2014; 16 (4): 417.
  22. Boyd N.F. Mammographic density and risk of breast cancer. Am Soc Clin Oncol Educ Book 2013.
  23. Melnikow J, Fenton J.J, Whitlock E.P et al. Supplemental Screening for Breast Cancer in Women With Dense Breasts: A Systematic Review for the U.S. Preventive Services Task Force. Ann Intern Med 2016; 164 (4): 268-78.
  24. Sickles E, D'Orsi C, Bassett L et al. ACR BI-RADSR Atlas, Breast imaging reporting and data system. Reston, VA: American College of Radiology, 2013; p. 39-48.
  25. Gubern-Merida A, Kallenberg M, Platel B et al. Volumetric breast density estimation from full-field digital mammograms: a validation study. PLoS One 2014; 9 (1): e85952.
  26. Strand F, Humphreys K, Cheddad A et al. Novel mammographic image features differentiate between interval and screen-detected breast cancer: a case-case study. Breast Cancer Res 2016; 18 (1): 100.
  27. Wang L. Early Diagnosis of Breast Cancer. Sensors (Basel) 2017; 17 (7).
  28. Gilbert F.J, Tucker L, Gillan M.G et al. The TOMMY trial: a comparison of TOMosynthesis with digital MammographY in the UK NHS Breast Screening Programme - a multicentre retrospective reading study comparing the diagnostic performance of digital breast tomosynthesis and digital mammography with digital mammography alone. Health Technol Assess 2015; 19 (4): 1-136.
  29. Ciatto S, Houssami N, Bernardi D et al. Integration of 3D digital mammography with tomosynthesis for population breast-cancer screening (STORM): a prospective comparison study. Lancet Oncol 2013; 14 (7): 583-9.
  30. Lalji U.C, Houben I.P, Prevos R et al. Contrast-enhanced spectral mammography in recalls from the Dutch breast cancer screening program: validation of results in a large multireader, multicase study. Eur Radiol 2016; 26 (12): 4371-9.
  31. Lobbes M.B, Smidt M.L, Houwers J et al. Contrast enhanced mammography: techniques, current results, and potential indications. Clin Radiol 2013; 68 (9): 935-44.
  32. Tagliafico S, Bignotti B, Rossi F et al. Diagnostic performance of contrast-enhanced spectral mammography: Systematic review and meta-analysis. Breast 2016; 28: 13-9.
  33. Ohuchi N, Suzuki A, Sobue T et al. 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 2016; 387 (10016): 341-8.
  34. Hooley R.J, Scoutt L.M, Philpotts L.E. Breast ultrasonography: state of the art. Radiology 2013; 268 (3): 642-59.
  35. Gong X, Xu Q, Xu Z et al. Real-time elastography for the differentiation of benign and malignant breast lesions: a meta-analysis. Breast Cancer Res Treat 2011; 130 (1): 11-8.
  36. Колядина И.В., Комов Д.В., Поддубная И.В. и др. Клиническая семиотика и предоперационная хирургическая диагностика рака молочной железы I стадии. Рос. онкологический журн. 2013; 4: 17-20. @@Kolyadina I.V., Komov D.V., Poddubnaya I.V. et al. Klinicheskaia semiotika i predoperatsionnaia khirurgicheskaia diagnostika raka molochnoi zhelezy I stadii. Ros. onkologicheskii zhurn. 2013; 4: 17-20 (in Russian)
  37. Ricci P, Maggini E, Mancuso E et al. Clinical application of breast elastography: state of the art. Eur J Radiol 2014; 83 (3): 429-37.
  38. Itoh A, Ueno E, Tohno E et al. Breast disease: clinical application of US elastography for diagnosis. Radiology 2006; 239 (2): 341-50.
  39. Fleury Ede F, Fleury J.C, Piato S et al. New elastographic classification of breast lesions during and after compression. Diagn Interv Radiol 2009; 15 (2): 96-103.
  40. Raza S, Odulate A, Ong E.M et al. Using real-time tissue elastography for breast lesion evaluation: our initial experience. J Ultrasound Med 2010; 29 (4): 551-63.
  41. Ciurea A.I, Bolboaca S.D, Ciortea C.A et al. The influence of technical factors on sonoelastographic assessment of solid breast nodules. Ultraschall Med 2011; 32 (Suppl. 1): S27-34.
  42. Zhao Q.L, Ruan L.T, Zhang H et al. Diagnosis of solid breast lesions by elastography 5-point score and strain ratio method. Eur J Radiol 2012; 81 (11): 3245-9.
  43. Strigel R.M, Rollenhagen JBurnside E.S et al. Screening Breast MRI Outcomes in Routine Clinical Practice: Comparison to BI-RADS Benchmarks. Acad Radiol 2017; 24 (4): 411-7.
  44. Ontario H.Q. Cancer screening with digital mammography for women at average risk for breast cancer, magnetic resonance imaging (MRI) for women at high risk: an evidence-based analysis. Ont Health Technol Assess Ser 2010; 10 (3): 1.
  45. Raikhlin A, Curpen B, Warner E et al. Breast MRI as an adjunct to mammography for breast cancer screening in high-risk patients: retrospective review. AJR Am J Roentgenol 2015; 204 (4): 889-97.
  46. Warner E, Plewes D.B, Hill K.A et al. Surveillance of BRCA1 and BRCA2 mutation carriers with magnetic resonance imaging, ultrasound, mammography, and clinical breast examination. JAMA 2004; 292 (11): 1317-25.
  47. Peng N.J, Chou C.P, Pan H.B et al. FDG-PET/CT detection of very early breast cancer in women with breast microcalcification lesions found in mammography screening. J Med Imaging Radiat Oncol 2015; 59 (4): 445-52.
  48. Groves A.M, Shastry M, Ben-Haim S et al. Defining the role of PET-CT in staging early breast cancer. Oncologist 2012; 17 (5): 613-9.
  49. Groheux D, Giacchetti S, Moretti J.L et al. Correlation of high 18F-FDG uptake to clinical, pathological and biological prognostic factors in breast cancer. Eur J Nucl Med Mol Imaging 2011; 38 (3): 426-35.
  50. Carkaci S, Macapinlac H.A, Cristofanilli M et al. Retrospective study of 18F-FDG PET/CT in the diagnosis of inflammatory breast cancer: preliminary data. J Nucl Med 2009; 50 (2): 231-8.
  51. Alberini J.L, Lerebours F, Wartski M et al. 18F-fluorodeoxyglucose positron emission tomography/computed tomography (FDG-PET/CT) imaging in the staging and prognosis of inflammatory breast cancer. Cancer 2009; 115 (21): 5038-47.
  52. Tchou J, Sonnad S.S Bergey M.R et al. Degree of tumor FDG uptake correlates with proliferation index in triple negative breast cancer. Mol Imaging Biol 2010; 12 (6): 657-62.
  53. Straver M.E, Aukema T.S, Olmos R.A et al. Feasibility of FDG PET/CT to monitor the response of axillary lymph node metastases to neoadjuvant chemotherapy in breast cancer patients. Eur J Nucl Med Mol Imaging 2010; 37 (6): 1069-76.
  54. Hodgson N.C, Gulenchyn K.Y. Is there a role for positron emission tomography in breast cancer staging? J Clin Oncol 2008; 26 (5): 712-20.
  55. Vercher-Conejero J.L, Pelegri-Martinez L, Lopez-Aznar D et al. Positron Emission Tomography in Breast Cancer. Diagnostics (Basel) 2015; 5 (1): 61-83.
  56. Sickles E.A. Mammographic features of "early" breast cancer. Am J Roentgenol 1984; 143 (3): 461-4.
  57. Колядина И.В. Гетерогенность раннего рака молочной железы: биологическое, популяционное и прогностическое значение. Дис. … д-ра мед. наук. М., 2015. @@Kolyadina I.V. Geterogennost' rannego raka molochnoi zhelezy: biologicheskoe, populiatsionnoe i prognosticheskoe znachenie. Dis. … d-ra med. nauk. Moscow, 2015 (in Russian)
  58. Корженкова Г.П. Стандартизация интерпретации маммографического изображения. Кубан. науч. мед. вестн. 2013 (1). @@Korzhenkova G.P. Standartizatsiia interpretatsii mammograficheskogo izobrazheniia. Kuban. nauch. med. vestn. 2013 (1) (in Russian)
  59. Корженкова Г.П. Совершенствование диагностики рака молочной железы в условиях массового маммографического обследования женского населения. Автореф. дис. … д-ра мед. наук. М., 2013. @@Korzhenkova G.P. Sovershenstvovanie diagnostiki raka molochnoi zhelezy v usloviiakh massovogo mammograficheskogo obsledovaniia zhenskogo naseleniia. Avtoref. dis. … d-ra med. nauk. Moscow, 2013 (in Russian)
  60. Корженкова Г.П. Комплексная рентгено-сонографическая диагностика заболеваний молочной железы. М.: СТРОМ, 2004. @@Korzhenkova G.P. Complex x-ray sonographic diagnosis of breast diseases. Moscow: STROM, 2004 (in Russian)
  61. Villeirs G, Mortier M, De Potter C et al. Breast calcifications. J Belge Radiol 1995; 78 (1): 11-7.
  62. Оксанчук Е.А., Меских Е.В., Колесник А.Ю. и др. Кальцинаты молочной железы: дифференциальная диагностика и прогностическое значение. Мед. визуализация. 2017; 5: 120-7. @@Oksanchuk E.A., Meskikh E.V., Kolesnik A.Iu. et al. Kal'tsinaty molochnoi zhelezy: differentsial'naia diagnostika i prognosticheskoe znachenie. Med. vizualizatsiia. 2017; 5: 120-7 (in Russian)
  63. Demetri-Lewis A, Slanetz P.J, Eisenberg R.L. Breast calcifications: the focal group. AJR Am J Roentgenol 2012; 198 (4): W325-43.
  64. Solomon A. Beitrage zur pathologie und klinik des mammakarzinoms. Arch F Kun Chir 1913; 101: 573.
  65. Leborgne R. Diagnosis of tumors of the breast by simple roentgenography; calcifications in carcinomas. Am J Roentgenol Radium Ther 1951; 65 (1): 1-11.
  66. Burnside E.S, Ochsner J.E, Fowler K.J et al. Use of microcalcification descriptors in BI-RADS 4th edition to stratify risk of malignancy. Radiology 2007; 242 (2): 388-95.
  67. Понедельникова Н., Корженкова Г., Летягин В. и др. Возможности чрескожных методов биопсии в верификации микрокальцинатов молочной железы на дооперационном этапе. Опухоли женской репродуктивной системы. 2011; 2. @@Ponedel'nikova N., Korzhenkova G., Letiagin V. et al. Vozmozhnosti chreskozhnykh metodov biopsii v verifikatsii mikrokal'tsinatov molochnoi zhelezy na dooperatsionnom etape. Opukholi zhenskoi reproduktivnoi sistemy. 2011; 2 (in Russian)
  68. Бухарин Д.Г., Фролова И.Г. Возможности рентгеновской маммографии «малых» форм рака молочной железы на фоне фиброзно-кистозной болезни. Бюл. сиб. мед. 2014; 13 (1). @@Bukharin D.G., Frolova I.G. Vozmozhnosti rentgenovskoi mammografii "malykh" form raka molochnoi zhelezy na fone fibrozno-kistoznoi bolezni. Biul. sib. med. 2014; 13 (1) (in Russian)
  69. Бухарин Д., Величко С., Слонимская Е. и др. Особенности маммографической визуализации «малых» форм рака молочной железы, развившегося на фоне фиброзно-кистозной болезни. Вопр. онкологии. 2011; 57 (5): 664-7. @@Bukharin D., Velichko S., Slonimskaia E. et al. Osobennosti mammograficheskoi vizualizatsii "malykh" form raka molochnoi zhelezy, razvivshegosia na fone fibrozno-kistoznoi bolezni. Vopr. onkologii. 2011; 57 (5): 664-7 (in Russian)
  70. Корженкова Г. Диагностическое значение категорий BI-RADS в ведении пациенток с доброкачественной патологией молочных желез. Опухоли женской репродуктивной системы. 2016; 4. @@Korzhenkova G. Diagnosticheskoe znachenie kategorii BI-RADS v vedenii patsientok s dobrokachestvennoi patologiei molochnykh zhelez. Opukholi zhenskoi reproduktivnoi sistemy. 2016; 4 (in Russian)
  71. Пасынков Д.В., Клюшкин И.В., Бусыгина О.В. Контурный анализ маммографических изображений доброкачественной и злокачественной патологии молочной железы. Казан. мед. журн. 2015; 96 (3). @@Pasynkov D.V., Kliushkin I.V., Busygina O.V. Konturnyi analiz mammograficheskikh izobrazhenii dobrokachestvennoi i zlokachestvennoi patologii molochnoi zhelezy. Kazan. med. zhurn. 2015; 96 (3) (in Russian)
  72. Борисова М.С., Мартынова Н.В., Богданов С.Н. Рентгеновская маммография в диагностике рака молочной железы. Вестник Российского научного центра рентгенорадиологии Минздрава России. 2013; 3 (13).@@Borisova M.S., Martynova N.V., Bogdanov S.N. Rentgenovskaia mammografiia v diagnostike raka molochnoi zhelezy. Vestnik Rossiiskogo nauchnogo tsentra rentgenoradiologii Minzdrava Rossii. 2013; 3 (13) (in Russian)
  73. Bassett L.W. Mammographic analysis of calcifications. Radiol Clin North Am 1992; 30 (1): 93-105.
  74. Rao A.A Feneis J, Lalonde C et al. A pictorial review of changes in the BI-RADS fifth edition. Radiographics 2016; 36 (3): 623-39.



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