Prediction of Molecular Subtypes Using Superb Microvascular Imaging and Shear Wave Elastography in Invasive Breast Carcinomas

      Rationale and Objectives

      To investigate the efficacy of the advanced imaging methods, superb microvascular imaging (SMI) and shear wave elastography (SWE) in predicting molecular subtypes in invasive breast carcinomas.

      Materials and Methods

      A total of 210 biopsy-proven breast carcinomas in 200 patients who underwent ultrasound (US) imaging with SMI and SWE were included in this study. Quantitative analyses were performed using mean elasticity (Emean) score by SWE and vascular index (VI) by SMI. For qualitative assessment of microvascularity, first, lesions were graded according to Adler's classification in four types. Then, a new morphological model was used to classify the microvascular architecture into six patterns: type one, no signal; type two, penetrant; type three, rim-like; type four, dot-like/linear/regional; type five, wheel-like and type six, irregular signals. The correlation between these variables and molecular subtypes, nuclear grade, the Ki-67 levels and axillary status was investigated.


      The average VI and Emean values were relatively higher in non-luminal subtypes (VI, p = 0.002; Emean, p > 0.05). The two microvascularisation models were significantly able to differentiate the molecular subtypes according to the Kruskal Wallis test (p < 0.05). Rim-like, penetrant and regional patterns were primarily observed in luminal subtypes. The dominant pattern in non-luminal subtypes was wheel-like pattern. VI, Emean, Adler's classification and morphological vascularisation model were not significantly correlated with the nuclear grade, Ki-67 index or axillary status.


      The proposed microvascular categorization model may be more valuable in predicting molecular subtypes of breast carcinomas compared to VI and Emean and may contribute to the management of breast carcinomas as a non-invasive variable.

      Key Words


      BI-RADS (breast imaging-reporting and data system), cSMI (color mode superb microvascular imaging), Emean (mean elasticity), ER (estrogen receptor), HER2 (human epidermal growth factor receptor 2), mSMI (monochromatic mode superb microvascular imaging), PR (progesterone receptor), ROI (region of interest), SMI (superb microvascular imaging), SWE (shear wave elastography), TNBC (tripple negative breast cancer), US (ultrasound), VI (vascular index)
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        • Yanagawa M
        • Ikemot K
        • Kawauchi S
        • et al.
        Luminal A and luminal B (HER2 negative) subtypes of breast cancer consist of a mixture of tumors with different genotype.
        BMC Res Notes. 2012; 5: 376
        • Curtis C
        • Shah SP
        • Chin SF
        • et al.
        The genomic and transcriptomic architecture of 2000 breast tumours reveals novel subgroups.
        Nature. 2012; 486: 346-352
        • Goldhirsch A
        • Winer EP
        • Coates AS
        • et al.
        Personalizing the treatment of women with early breast cancer: highlights of the st gallen international expert consensus on the primary therapy of early breast cancer 2013.
        Ann Oncol. 2013; 24: 2206-2223
        • Castaneda CA
        • Andres E
        • Barcena C
        • et al.
        Behavior of breast cancer molecular subtypes through tumour progression.
        Clin Transl Oncol. 2012; 14: 481-485
        • Park S
        • Koo JS
        • Kim MS
        • et al.
        Characteristics and outcomes according to molecular subtypes of breast cancer as classified by a panel of four biomarkers using immunohistochemistry.
        Breast. 2012; 21: 50-57
        • Yam C
        • Mani SA
        • Moulder SL.
        Targeting the molecular subtypes of triple negative breast cancer: understanding the diversity to progress the field.
        Oncologist. 2017; 22: 1086-1093
        • Cho N
        • Jang M
        • Lyou CY
        • et al.
        Distinguishing benign from malignant masses at breast US: combined US elastography and color doppler US-influence on radiologist accuracy.
        Radiology. 2012; 262: 80-90
        • Tekcan Sanli DE
        • Yildirim D
        • Kandemirli SG
        • et al.
        Evaluation of Multiparametric shear wave elastography indices in malignant and benign breast lesions.
        Acad Radiol. 2022; 29: S50-S61
        • Barr RG
        • Nakashima K
        • Amy D
        • et al.
        WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 2: breast.
        Ultrasound Med Biol. 2015; 41: 1148-1160
        • Youk JH
        • Gweon HM
        • Son EJ.
        Shear-wave elastography in breast ultrasonography: the state of the art.
        Ultrasonography. 2017; 36: 300-309
        • Berg WA
        • Cosgrove DO
        • Doré CJ
        • et al.
        Shear-wave elastography improves the specificity of breast US: the BE1 study of 939 masses.
        Radiology. 2012; 262: 435-449
        • Shiina T
        • Nightingale KR
        • Palmeri ML
        • et al.
        WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 1: basic principles and terminology.
        Ultrasound Med Biol. 2015; 41: 1126-1147
        • Chang J.M.
        • Park I.A.
        • Lee S.H.
        • et al.
        Stiffness of tumours measured by shear-wave elastography correlated with subtypes of breast cancer.
        Eur Radiol. 2013; 23: 2450-2458
        • Nishida N
        • Yano H
        • Nishida T
        • et al.
        Angiogenesis in cancer.
        Vasc Health Risk Manag. 2006; 2: 213-219
        • Zhu YC
        • Zhang Y
        • Deng SH
        • et al.
        Diagnostic Performance of superb microvascular imaging (smi) combined with shear-wave elastography in evaluating breast lesions.
        Med Sci Monit. 2018; 24: 5935-5942
        • Zhang XY
        • Zhang L
        • Li N
        • et al.
        Vascular index measured by smart 3-D superb microvascular imaging can help to differentiate malignant and benign breast lesion.
        Cancer Manag Res. 2019; 11: 5481-5487
        • Liang M
        • Ou B
        • Wu J
        • et al.
        Combined use of strain elastography and superb microvascular imaging with grayscale ultrasound according to the BI-RADS classification for differentiating benign from malignant solid breast masses.
        Clin Hemorheol Microcirc. 2020; 74: 391-403
        • Lee EJ
        • Chang YW.
        Combination of quantitative parameters of shear wave elastography and superb microvascular imaging to evaluate breast masses.
        Korean J Radiol. 2020; 21: 1045-1054
        • D'Orsi C
        • Sickles EA
        • Mendelson EB
        • et al.
        Breast imaging reporting and data system: ACR BI-RADS breast imaging atlas.
        5th ed. American College of Radiology, Reston, Va2013
        • Dietrich C
        • Bamber J
        • Berzigotti A
        • et al.
        EFSUMB guidelines and recommendations on the clinical use of liver ultrasound elastography, update 2017 (long version).
        Ultraschall Med. 2017; 38: e16-e47
        • Zhou BG
        • Wang D
        • Ren WW
        • et al.
        Value of shear wave arrival time contour display in shear wave elastography for breast masses diagnosis.
        Sci Rep. 2017; 7: 7036
        • Adler DD
        • Carson PL
        • Rubin JM
        • et al.
        Doppler ultrasound color flow imaging in the study of breast cancer: preliminary findings.
        Ultrasound Med Biol. 1990; 16: 553-559
        • Du J
        • Li FH
        • Fang H
        • et al.
        Microvascular architecture of breast lesions: evaluation with contrast-enhanced ultrasonographic micro flow imaging.
        J Ultrasound Med. 2008; 27 (quiz 844): 833-842
        • Xiao XY
        • Chen X
        • Guan XF
        • et al.
        Superb microvascular imaging in diagnosis of breast lesions: a comparative study with contrast-enhanced ultrasonographic microvascular imaging.
        Br J Radiol. 2016; 8920160546
        • Cai S
        • Wang H
        • Zhang X
        • et al.
        Superb microvascular imaging technology can improve the diagnostic efficiency of the BI-RADS system.
        Front Oncol. 2021; 24634752
        • WHO Classification of Tumors Editorial Board
        Breast tumors.
        5th Edition. International Agency for Research on Cancer, Lyon2019 (Volume 2)
        • Elston CW
        • Ellis IO.
        Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up.
        Histopathology. 1991; 19: 403-410
        • Zhong L
        • Wang C.
        Diagnostic accuracy of ultrasound superb microvascular imaging for breast tumor: a meta-analysis.
        Med Ultrason. 2020; 22: 313-318
        • Zheng X
        • Huang Y
        • Liu Y
        • et al.
        shear-wave elastography of the breast: added value of a quality map in diagnosis and prediction of the biological characteristics of breast cancer.
        Korean J Radiol. 2020; 21: 172-180
        • Liu H
        • Wan J
        • Xu G
        • et al.
        Conventional US and 2-D shear wave elastography of virtual touch tissue imaging quantification: correlation with immunohistochemical subtypes of breast cancer.
        Ultrasound Med Biol. 2019; 45: 2612-2622
        • Cho DH
        • Park CS
        • Kim SH
        • et al.
        Correlation of the strain elastography-derived elasticity scores with prognostic histologic features, Immunohistochemical markers, and molecular subtypes of invasive ductal carcinoma.
        J Korean Soc Radiol. 2019; 80: 717-727
        • Yongfeng Z
        • Ping Z
        • Wengang L
        • et al.
        Application of a novel microvascular imaging technique in breast lesion evaluation.
        Ultrasound Med Biol. 2016; 42: 2097-2105
      1. SEER Cancer Stat Facts: Female Breast Cancer Subtypes. National Cancer Institute. Bethesda, MD, 2021, Available at: Accessed February 8, 2022.