Ultrasound Viscoelasticity for Breast Tumor: High Diagnostic Performance at the Peritumoral Boundary

doi:10.26599/AUDT.2025.250075

Abstract

Abstract:

Objectives Conventional ultrasound (US) elastography lacks specificity in distinguishing benign from malignant breast lesions. This study employed US to assess breast tissue viscosity and elasticity. The primary objective was to evaluate the diagnostic performance of US-derived viscoelasticity parameters. Secondary objectives included investigating the consistency of parameters in the mechanical properties of breast tissue.
Materials and methods Two doctors independently measured the viscosity and elasticity of specific positions in the breasts of 20 health females for consistency assessment. Then the doctors selected region of interest (ROI) to measure viscoelasticity. ROI-1, ROI-2, and ROI-3 represent the tumor, peritumoral, and peripheral areas, respectively. The viscosity modulus and elasticity modulus of 3 ROIs were analyzed. The viscosity and elasticity parameters with the highest area under the curve (AUC) were selected as the optimal ones. Finally, elasticity and viscosity parameters were combined to assess their diagnostic performance in differentiating breast lesions.
Results US viscoelasticity parameters can be measured with high consistency. Among conventional US elasticity parameters, 1-Emax demonstrated the highest AUC (0.746) for differentiating benign and malignant breast lesions. In US viscoelasticity parameters, 2-Emax achieved the highest AUC of 0.801, while 2-Vmax showed the highest AUC of 0.835. The highest specificity (0.903) was observed when both 2-Emax and 2-Vmax exceeded their respective cutoff values (P < 0.05 for all).
Conclusion Quantitative ultrasound viscoelasticity parameters play a crucial role in breast cancer diagnosis, with tumor boundary parameters being particularly significant for cancer screening and prevention strategies.

Key words: Viscoelasticity; Viscosity; Elasticity; Ultrasound; Breast cancer

Shi Junni, Xu Jiatong, Chen Chuanjian, Xiang Guanghua, Zheng Wen, Chen Man. Ultrasound Viscoelasticity for Breast Tumor: High Diagnostic Performance at the Peritumoral Boundary. Advanced Ultrasound in Diagnosis and Therapy, 2025, 9(3): 270-276.

Figures/Tables 9

Figure 1

Figure 2

Table 1

Table 2

Figure 3

Table 3

Figure 4

Table 4

Table 5

References 26

[1]	Wilkinson L, Gathani T. Understanding breast cancer as a global health concern. Br J Radiol 2022; 95: 20211033.
[2]	Zhang L, Dong YJ, Zhou JQ, Jia XH, Li S, Zhan WW. Similar reproducibility for strain and shear wave elastography inbreast mass evaluation: a prospective study using the same ultrasound system. Ultrasound Med Biol 2020; 46: 981-991.
[3]	Barr RG, Nakashima K, Amy D, Cosgrove D, Farrokh A, Schafer F, et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 2: breast. Ultrasound Med Biol 2015; 41: 1148-1160.
[4]	Shiina T, Nightingale KR, Palmeri ML, Hall TJ, Bamber JC, Barr RG, 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.
[5]	Zheng X, Li F, Xuan ZD, Wang Y, Zhang L. Combination of shear wave elastography and BI-RADS in identification of solid breast masses. BMC Med Imaging 2021; 21: 183.
[6]	Dong M, Xing B, Zhang B, Xu X, Zhou Q. Diagnostic performance and accuracy of strain elastography for BI-RADS category 4 lesions among Asian females. J Coll Physicians Surg Pak 2023; 33: 1181-1187.
[7]	Rus G, Faris IH, Torres J, Callejas A, Melchor J. Why are viscosity and nonlinearity bound to make an impact in clinical elastographic diagnosis? Sensors (Basel) 2020; 20.
[8]	Bhatt M, Moussu MAC, Chayer B, Destrempes F, Gesnik M, Allard L, et al. Reconstruction of viscosity maps in ultrasound shear wave elastography. IEEE Trans Ultrason Ferroelectr Freq Control 2019.
[9]	Kumar V, Denis M, Gregory A, Bayat M, Mehrmohammadi M, Fazzio R, et al. Viscoelastic parameters as discriminators of breast masses: initial human study results. PLoS One 2018; 13: e0205717.
[10]	Jia W, Xia S, Jia X, Tang B, Cheng S, Nie M, et al. Ultrasound viscosity imaging in breast lesions: a multicenter prospective study. Acad Radiol 2024; 31: 3499-3510.
[11]	Berg WA, Cosgrove DO, Doré CJ, Schäfer FK, Svensson WE, Hooley RJ, et al. Shear-wave elastography improves the specificity of breast US: the BE1 multinational study of 939 masses. Radiology 2012; 262: 435-449.
[12]	Zhang L, Xu J, Wu H, Liang W, Ye X, Tian H, et al. Screening breast lesions using shear modulus and its 1-mm shell in sound touch elastography. Ultrasound Med Biol 2019; 45: 710-719.
[13]	Condeelis J, Segall JE. Intravital imaging of cell movement in tumours. Nat Rev Cancer 2003; 3: 921-930.
[14]	Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med 2006; 4: 38.
[15]	Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009; 139: 891-906.
[16]	Wang ZL, Sun L, Li Y, Li N. Relationship between elasticity and collagen fiber content in breast disease: a preliminary report. Ultrasonics 2015; 57: 44-49.
[17]	Soby L, Jamieson AM, Blackwell J, Choi HU, Rosenberg LC. Viscoelastic and rheological properties of concentrated solutions of proteoglycan subunit and proteoglycan aggregate. Biopolymers 1990; 29: 1587-1592.
[18]	Karousou E, D'Angelo ML, Kouvidi K, Vigetti D, Viola M, Nikitovic D, et al. Collagen VI and hyaluronan: the common role in breast cancer. Biomed Res Int 2014; 2014: 606458.
[19]	Chan CJ, Costanzo M, Ruiz-Herrero T, Mönke G, Petrie RJ, Bergert M, et al. Hydraulic control of mammalian embryo size and cell fate. Nature 2019; 571: 112-116.
[20]	Nelson CM, Gleghorn JP, Pang MF, Jaslove JM, Goodwin K, Varner VD, et al. Microfluidic chest cavities reveal that transmural pressure controls the rate of lung development. Development 2017; 144: 4328-4335.
[21]	Shyer AE, Huycke TR, Lee C, Mahadevan L, Tabin CJ. Bending gradients: how the intestinal stem cell gets its home. Cell 2015; 161: 569-580.
[22]	Harris AR, Peter L, Bellis J, Baum B, Kabla AJ, Charras GT. Characterizing the mechanics of cultured cell monolayers. Proc Natl Acad Sci U S A 2012; 109: 16449-16454.
[23]	Bera K, Kiepas A, Godet I, Li Y, Mehta P, Ifemembi B, et al. Extracellular fluid viscosity enhances cell migration and cancer dissemination. Nature 2022; 611: 365-373.
[24]	Elosegui-Artola A, Gupta A, Najibi AJ, Seo BR, Garry R, Tringides CM, et al. Matrix viscoelasticity controls spatiotemporal tissue organization. Nat Mater 2023; 22: 117-127.
[25]	Morla-Barcelo PM, Laguna-Macarrilla D, Cordoba O, Matheu G, Oliver J, Roca P, et al. Unraveling malignant phenotype of peritumoral tissue: transcriptomic insights into early-stage breast cancer. Breast Cancer Res 2024; 26: 89.
[26]	Barr RG. Future of breast elastography. Ultrasonography 2019; 38: 93-105.

Items	Mean ± SD
Pathological diagnosis (n = 2613)
Benign	2054 (78.6%)
Malignant	559 (21.4%)
Age (y)	45 ± 16
Menarche age (y)	14 ± 2
Menopause age (n = 513, y)	51 ± 4
First childbearing age (n = 2016, y)	25 ± 7
1-Emean (kPa)	40.0 ± 14.3
1-Emax (kPa)	106.4 ± 56.3
1-Emin (kPa)	13.0 ± 9.3
1-ESD (kPa)	10.3 ± 3.5

Items	Mean ± SD
Pathological diagnosis (n = 377)
Benign	258 (68.4%)
Malignant	119 (31.6%)
Age (y)	48 ± 15
Menarche age (y)	14 ± 2
Menopause age (n = 114, y)	51 ± 3
First childbearing age (n = 308, y)	25 ± 7
1-Emean (kPa)	20.3 ± 12.6
1-Emax (kPa)	92.5 ± 70.4
1-Emin (kPa)	4.1 ± 3.6
1-ESD (kPa)	12.3 ± 9.2
2-Emean (kPa)	30.3 ± 47.4
2-Emax (kPa)	38.0 ± 45.1
2-Emin (kPa)	20.1 ± 22.9
2-ESD (kPa)	5.3 ± 9.4
3-Emean (kPa)	14.4 ± 10.8
3-Emax (kPa)	17.5 ± 13.3
3-Emin (kPa)	11.2 ± 7.9
3-ESD (kPa)	1.7 ± 2.3
1-Vmean (Pa.s)	2.5 ± 1.7
1-Vmax (Pa.s)	9.1 ± 6.8
1-Vmin (Pa.s)	0.4 ± 1.4
1-VSD (Pa.s)	1.4 ± 0.9
2-Vmean (Pa.s)	2.8 ± 3.1
2-Vmax (Pa.s)	3.8 ± 4.0
2-Vmin (Pa.s)	1.9 ± 2.2
2-VSD (Pa.s)	0.5 ± 0.7
3-Vmean (Pa.s)	1.3 ± 1.3
3-Vmax (Pa.s)	1.7 ± 1.7
3-Vmin (Pa.s)	1.0 ± 1.0
3-VSD (Pa.s)	0.2 ± 0.3

Items	Cut off (kPa)	Sensitivity	Specificity	AUC	P value
1-Emean	36	0.762	0.417	0.609	< 0.001
1-Emax	80	0.878	0.429	0.746	< 0.001
1-Emin	47	0.002	0.998	0.307	< 0.001

Items	Cut off	Sensitivity	Specificity	AUC	P value
Elasticity (kPa)
2-Emean	38	0.521	0.945	0.773	< 0.001
2-Emax	36	0.612	0.875	0.801	< 0.001
2-Emin	24	0.545	0.886	0.736	< 0.001
Viscosity (Pa.s)
2-Vmean	3	0.617	0.886	0.827	< 0.001
2-Vmax	3	0.717	0.846	0.835	< 0.001
2-Vmin	2	0.542	0.923	0.756	< 0.001

Items	P value	Sensitivity	Specificity	AUC
2-Emax ≥ 36 kPa and 2-Vmax ≥ 3Pa.s	< 0.001	0.597	0.903	0.75
2-Emax ≥ 36 kPa or 2-Vmax ≥ 3Pa.s	< 0.001	0.739	0.791	0.765