European Radiology

, Volume 27, Issue 6, pp 2443–2450 | Cite as

Diagnosis of sub-centimetre breast lesions: combining BI-RADS-US with strain elastography and contrast-enhanced ultrasound—a preliminary study in China

  • Xiaoyun Xiao
  • Qiongchao Jiang
  • Huan Wu
  • Xiaofeng Guan
  • Wei Qin
  • Baoming LuoEmail author



To compare the diagnostic efficacies of B-mode ultrasound (US), strain elastography (SE), contrast-enhanced ultrasound (CEUS) and the combination of these modalities for breast lesions <1 cm in size.


Between January 2013 and October 2015, 203 inpatients with 209 sub-centimetre breast lesions categorised as BI-RADS-US (Breast Imaging Reporting and Data System for Ultrasound) 3-5 were included. US, SE and CEUS were performed to evaluate each lesion. The diagnostic performances of different ultrasonic modalities were compared. The diagnostic efficacies of BI-RADS-US and our re-rating systems were also compared. The pathology findings were used as the reference standard.


The specificities of US, SE and CEUS for tumour differentiation were 17.4 %, 56.2 % and 86.0 %, respectively (P < 0.05); and the sensitivities were 100 %, 93.2 % and 93.2 % for US, SE and CEUS, respectively (P < 0.05). The area under the curve (AUC) of the receiver operating characteristic (ROC) curve was 0.867 for original BI-RADS-US, 0.882 for BI-RADS-US combined with only SE, 0.953 for BI-RADS-US combined with only CEUS and 0.924 for BI-RADS-US combined with both SE and CEUS. The best combination was BI-RADS-US combined with only CEUS.


Evaluating sub-centimetre breast lesions with SE and CEUS could increase the diagnostic specificity while retaining high sensitivity compared with B-mode ultrasound.

Key Points

Evaluating breast lesions with SE and CEUS could increase the diagnostic specificity

SE and CEUS offer alternatives to biopsy and possibly allow shorter-interval follow-ups

BI-RADS-US combined with CEUS exhibited the best diagnostic performance


Breast Ultrasound Contrast media Elastography Diagnosis 



B-mode ultrasound


Strain elastography


Contrast-enhanced ultrasound


Breast Imaging Reporting and Data system for Ultrasound



The scientific guarantor of this publication is Baoming Luo. 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.

The authors state that this work has not received any funding. No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained. Written informed consent was waived by the Institutional Review Board. No study subjects or cohorts have been previously reported. Methodology: retrospective, diagnostic or prognostic study, performed at one institution.


  1. 1.
    Ellis I (2008) Prognosis of small screen-detected invasive breast cancers. Breast Cancer Res 10:P1CrossRefPubMedCentralGoogle Scholar
  2. 2.
    Tabar L, Yen MF, Vitak B et al (2003) Mammography service screening and mortality in breast cancer patients: 20-year follow-up before and after introduction of screening. Lancet 361:1405–1410CrossRefPubMedGoogle Scholar
  3. 3.
    Tabar L, Chen HH, Duffy SW et al (2000) A novel method for prediction of long-term outcome of women with T1a, T1b, and 10-14 mm invasive breast cancers: a prospective study. Lancet 355:429–433CrossRefPubMedGoogle Scholar
  4. 4.
    Tabar L, Tony CH, Amy YM et al (2004) Mammographic tumor features can predict long-term outcomes reliably in women with 1-14-mm invasive breast carcinoma. Cancer 101:1745–1759CrossRefPubMedGoogle Scholar
  5. 5.
    Mainiero MB, Lourenco A, Mahoney MC et al (2013) ACR appropriateness criteria breast cancer screening. J Am Coll Radiol 10:11–14CrossRefPubMedGoogle Scholar
  6. 6.
    Freer PE (2015) Mammographic breast density: impact on breast cancer risk and implications for screening. Radiographics 35:302–315CrossRefPubMedGoogle Scholar
  7. 7.
    Lee JH, Kim SH, Kang BJ et al (2011) Role and clinical usefulness of elastography in small breast masses. Acad Radiol 18:74–80CrossRefPubMedGoogle Scholar
  8. 8.
    Sadigh G, Carlos RC, Neal CH et al (2012) Ultrasonographic differentiation of malignant from benign breast lesions: a meta-analytic comparison of elasticity and BIRADS scoring. Breast Cancer Res Treat 133:23–35CrossRefPubMedGoogle Scholar
  9. 9.
    Garra BS (2007) Imaging and estimation of tissue elasticity by ultrasound. Ultrasound Q 23:255–268CrossRefPubMedGoogle Scholar
  10. 10.
    Hatzung G, Grunwald S, Zygmunt M et al (2010) Sonoelastography in the diagnosis of malignant and benign breast lesions: initial clinical experiences. Ultraschall Med 31:596–603CrossRefPubMedGoogle Scholar
  11. 11.
    Itoh A, Ueno E, Tohno E et al (2006) Breast disease: clinical application of US elastography for diagnosis. Radiology 239:341–350CrossRefPubMedGoogle Scholar
  12. 12.
    Wells PN, Liang HD (2011) Medical ultrasound: imaging of soft tissue strain and elasticity. J R Soc Interface 8:1521–1549CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Wojcinski S, Farrokh A, Weber S et al (2010) Multicenter study of ultrasound real-time tissue elastography in 779 cases for the assessment of breast lesions: improved diagnostic performance by combining the BI-RADS(R)-US classification system with sonoelastography. Ultraschall Med 31:484–491CrossRefPubMedGoogle Scholar
  14. 14.
    Sadigh G, Carlos RC, Neal CH et al (2012) Accuracy of quantitative ultrasound elastography for differentiation of malignant and benign breast abnormalities: a meta-analysis. Breast Cancer Res Treat 134:923–931CrossRefPubMedGoogle Scholar
  15. 15.
    Wan C, Du J, Fang H et al (2012) Evaluation of breast lesions by contrast enhanced ultrasound: qualitative and quantitative analysis. Eur J Radiol 81:e444–e450CrossRefPubMedGoogle Scholar
  16. 16.
    Caproni N, Marchisio F, Pecchi A et al (2010) Contrast-enhanced ultrasound in the characterisation of breast masses: utility of quantitative analysis in comparison with MRI. Eur Radiol 20:1384–1395CrossRefPubMedGoogle Scholar
  17. 17.
    Hu Q, Wang XY, Zhu SY et al (2015) Meta-analysis of contrast-enhanced ultrasound for the differentiation of benign and malignant breast lesions. Acta Radiol 56:25–33CrossRefPubMedGoogle Scholar
  18. 18.
    Liu H, Jiang Y, Dai Q et al (2015) Differentiation of benign and malignant sub-1-cm breast lesions using contrast-enhanced sonography. J Ultrasound Med 34:117–123CrossRefPubMedGoogle Scholar
  19. 19.
    Zhi H, Ou B, Xiao XY et al (2013) Ultrasound elastography of breast lesions in chinese women: a multicenter study in China. Clin Breast Cancer 13:392–400CrossRefPubMedGoogle Scholar
  20. 20.
    Liu H, Jiang YX, Liu JB et al (2008) Evaluation of breast lesions with contrast-enhanced ultrasound using the microvascular imaging technique: initial observations. Breast 17:532–539CrossRefPubMedGoogle Scholar
  21. 21.
    Jiang YX, Liu H, Liu JB et al (2007) Breast tumor size assessment: comparison of conventional ultrasound and contrast-enhanced ultrasound. Ultrasound Med Biol 33:1873–1881CrossRefPubMedGoogle Scholar
  22. 22.
    Du J, Li FH, Fang H et al (2008) Correlation of real-time gray scale contrast-enhanced ultrasonography with microvessel density and vascular endothelial growth factor expression for assessment of angiogenesis in breast lesions. J Ultrasound Med 27:821–831CrossRefPubMedGoogle Scholar
  23. 23.
    Xiao X, Ou B, Yang H et al (2014) Breast contrast-enhanced ultrasound: is a scoring system feasible? A preliminary study in China. PLoS One 9:e105517CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Thomas A, Fischer T, Frey H et al (2006) Real-time elastography—an advanced method of ultrasound: first results in 108 patients with breast lesions. Ultrasound Obstet Gynecol 28:335–340CrossRefPubMedGoogle Scholar
  25. 25.
    Moon WK, Im JG, Noh DY et al (2000) Nonpalpable breast lesions: evaluation with power Doppler US and a microbubble contrast agent-initial experience. Radiology 217:240–246CrossRefPubMedGoogle Scholar
  26. 26.
    Balleyguier C, Opolon P, Mathieu MC et al (2009) New potential and applications of contrast-enhanced ultrasound of the breast: Own investigations and review of the literature. Eur J Radiol 69:14–23CrossRefPubMedGoogle Scholar
  27. 27.
    Zhi H, Xiao XY, Ou B et al (2012) Could ultrasonic elastography help the diagnosis of small (≤2 cm) breast cancer with the usage of sonographic BI-RADS classification? Eur J Radiol 81:3216–3221CrossRefPubMedGoogle Scholar
  28. 28.
    Giuseppetti GM, Martegani A, Di Cioccio B et al (2005) Elastosonography in the diagnosis of the nodular breast lesions: preliminary report. Radiol Med 110:69–76PubMedGoogle Scholar
  29. 29.
    Vinnicombe SJ, Whelehan P, Thomson K et al (2014) What are the characteristics of breast cancers misclassified as benign by quantitative ultrasound shear wave elastography? Eur Radiol 24:921–926CrossRefPubMedGoogle Scholar
  30. 30.
    Raza S, Odulate A, Ong EM et al (2010) Using real-time tissue elastography for breast lesion evaluation: our initial experience. J Ultrasound Med 29:551–563CrossRefPubMedGoogle Scholar
  31. 31.
    Ciurea AI, Bolboaca SD, Ciortea CA et al (2011) The influence of technical factors on sonoelastographic assessment of solid breast nodules. Ultraschall Med 32:S27–S34CrossRefPubMedGoogle Scholar
  32. 32.
    Weidner N, Semple JP, Welch WR et al (1991) Tumor angiogenesis and metastasis—correlation in invasive breast carcinoma. N Engl J Med 324:1–8CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2016

Authors and Affiliations

  • Xiaoyun Xiao
    • 1
  • Qiongchao Jiang
    • 1
  • Huan Wu
    • 1
  • Xiaofeng Guan
    • 1
  • Wei Qin
    • 1
  • Baoming Luo
    • 1
    Email author
  1. 1.Department of Ultrasound, Sun Yat-sen Memorial HospitalSun Yat-sen UniversityGuangzhouChina

Personalised recommendations