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Published in: Molecular Imaging and Biology 6/2018

Open Access 01-12-2018 | Research Article

A Simple Ultrasound Based Classification Algorithm Allows Differentiation of Benign from Malignant Breast Lesions by Using Only Quantitative Parameters

Authors: Panagiotis Kapetas, Ramona Woitek, Paola Clauser, Maria Bernathova, Katja Pinker, Thomas H. Helbich, Pascal A. Baltzer

Published in: Molecular Imaging and Biology | Issue 6/2018

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Abstract

Purpose

We hypothesized that different quantitative ultrasound (US) parameters may be used as complementary diagnostic criteria and aimed to develop a simple classification algorithm to distinguish benign from malignant breast lesions and aid in the decision to perform biopsy or not.

Procedures

One hundred twenty-four patients, each with one biopsy-proven, sonographically evident breast lesion, were included in this prospective, IRB-approved study. Each lesion was examined with B-mode US, Color/Power Doppler US and elastography (Acoustic Radiation Force Impulse–ARFI). Different quantitative parameters were recorded for each technique, including pulsatility (PI) and resistive Index (RI) for Doppler US and lesion maximum, intermediate, and minimum shear wave velocity (SWVmax, SWVinterm, and SWVmin) as well as lesion-to-fat SWV ratio for ARFI. Receiver operating characteristic curve (ROC) analysis was used to evaluate the diagnostic performance of each quantitative parameter. Classification analysis was performed using the exhaustive chi-squared automatic interaction detection method. Results include the probability for malignancy for every descriptor combination in the classification algorithm.

Results

Sixty-five lesions were malignant and 59 benign. Out of all quantitative indices, maximum SWV (SWVmax), and RI were included in the classification algorithm, which showed a depth of three ramifications (SWVmax ≤ or > 3.16; if SWVmax ≤ 3.16 then RI ≤ 0.66, 0.66–0.77 or > 0.77; if RI ≤ 0.66 then SWVmax ≤ or > 2.71). The classification algorithm leads to an AUC of 0.887 (95 % CI 0.818–0.937, p < 0.0001), a sensitivity of 98.46 % (95 % CI 91.7–100 %), and a specificity of 61.02 % (95 % CI 47.4–73.5 %). By applying the proposed algorithm, a false-positive biopsy could have been avoided in 61 % of the cases.

Conclusions

A simple classification algorithm incorporating two quantitative US parameters (SWVmax and RI) shows a high diagnostic performance, being able to accurately differentiate benign from malignant breast lesions and lower the number of unnecessary breast biopsies in up to 60 % of all cases, avoiding any subjective interpretation bias.
Literature
1.
go back to reference Nothacker M, Duda V, Hahn M, Warm M, Degenhardt F, Madjar H, Weinbrenner S, Albert US (2009) Early detection of breast cancer: benefits and risks of supplemental breast ultrasound in asymptomatic women with mammographically dense breast tissue. A systematic review. BMC Cancer 9:335CrossRef Nothacker M, Duda V, Hahn M, Warm M, Degenhardt F, Madjar H, Weinbrenner S, Albert US (2009) Early detection of breast cancer: benefits and risks of supplemental breast ultrasound in asymptomatic women with mammographically dense breast tissue. A systematic review. BMC Cancer 9:335CrossRef
2.
go back to reference Madjar H (2010) Role of breast ultrasound for the detection and differentiation of breast lesions. Breast Care 5:109–114CrossRef Madjar H (2010) Role of breast ultrasound for the detection and differentiation of breast lesions. Breast Care 5:109–114CrossRef
3.
go back to reference Cho N, Jang M, Lyou CY, Park JS, Choi HY, Moon WK (2012) Distinguishing benign from malignant masses at breast US: combined US elastography and color doppler US—influence on radiologist accuracy. Radiology 262:80–90CrossRef Cho N, Jang M, Lyou CY, Park JS, Choi HY, Moon WK (2012) Distinguishing benign from malignant masses at breast US: combined US elastography and color doppler US—influence on radiologist accuracy. Radiology 262:80–90CrossRef
4.
go back to reference Mendelson EB, Böhm-Vélez M, Berg WA, et al. (2013) ACR BI-RADS® Ultrasound. In ACR BI-RADS® Atlas, Breast Imaging Reporting and Data System, Eds D’Orsi CJ, Sickles EA, Mendelson EB, Morris EA Reston, VA: American College of Radiology, pp 216–355 Mendelson EB, Böhm-Vélez M, Berg WA, et al. (2013) ACR BI-RADS® Ultrasound. In ACR BI-RADS® Atlas, Breast Imaging Reporting and Data System, Eds D’Orsi CJ, Sickles EA, Mendelson EB, Morris EA Reston, VA: American College of Radiology, pp 216–355
5.
go back to reference Scaperrotta G, Ferranti C, Costa C, Mariani L, Marchesini M, Suman L, Folini C, Bergonzi S (2008) Role of sonoelastography in non-palpable breast lesions. Eur Radiol 18:2381–2389CrossRef Scaperrotta G, Ferranti C, Costa C, Mariani L, Marchesini M, Suman L, Folini C, Bergonzi S (2008) Role of sonoelastography in non-palpable breast lesions. Eur Radiol 18:2381–2389CrossRef
6.
go back to reference Calas MJ, Almeida RM, Gutfilen B, Pereira WC (2010) Intraobserver interpretation of breast ultrasonography following the BI-RADS classification. Eur J Radiol 74:525–528CrossRef Calas MJ, Almeida RM, Gutfilen B, Pereira WC (2010) Intraobserver interpretation of breast ultrasonography following the BI-RADS classification. Eur J Radiol 74:525–528CrossRef
7.
go back to reference Park CS, Kim SH, Jung NY, Choi JJ, Kang BJ, Jung HS (2015) Interobserver variability of ultrasound elastography and the ultrasound BI-RADS lexicon of breast lesions. Breast Cancer 22:153–160CrossRef Park CS, Kim SH, Jung NY, Choi JJ, Kang BJ, Jung HS (2015) Interobserver variability of ultrasound elastography and the ultrasound BI-RADS lexicon of breast lesions. Breast Cancer 22:153–160CrossRef
8.
go back to reference Berg WA, Cosgrove DO, Dore CJ et al (2012) Shear-wave elastography improves the specificity of breast US: the BE1 multinational study of 939 masses. Radiology 262:435–449CrossRef Berg WA, Cosgrove DO, Dore CJ et al (2012) Shear-wave elastography improves the specificity of breast US: the BE1 multinational study of 939 masses. Radiology 262:435–449CrossRef
9.
go back to reference Kumar A, Srivastava V, Singh S, Shukla RC (2010) Color Doppler ultrasonography for treatment response prediction and evaluation in breast cancer. Future Oncol 6:1265–1278CrossRef Kumar A, Srivastava V, Singh S, Shukla RC (2010) Color Doppler ultrasonography for treatment response prediction and evaluation in breast cancer. Future Oncol 6:1265–1278CrossRef
10.
go back to reference Cosgrove DO, Berg WA, Dore CJ et al (2012) Shear wave elastography for breast masses is highly reproducible. Eur Radiol 22:1023–1032CrossRef Cosgrove DO, Berg WA, Dore CJ et al (2012) Shear wave elastography for breast masses is highly reproducible. Eur Radiol 22:1023–1032CrossRef
11.
go back to reference Kapetas P, Pinker-Domenig K, Woitek R, Clauser P, Bernathova M, Spick C, Helbich T, Baltzer PA (2017) Clinical application of acoustic radiation force impulse imaging with virtual touch IQ in breast ultrasound: diagnostic performance and reproducibility of a new technique. Acta Radiol 58:140–147CrossRef Kapetas P, Pinker-Domenig K, Woitek R, Clauser P, Bernathova M, Spick C, Helbich T, Baltzer PA (2017) Clinical application of acoustic radiation force impulse imaging with virtual touch IQ in breast ultrasound: diagnostic performance and reproducibility of a new technique. Acta Radiol 58:140–147CrossRef
12.
go back to reference Bickel H, Pinker-Domenig K, Bogner W, Spick C, Bagó-Horváth Z, Weber M, Helbich T, Baltzer P (2015) Quantitative apparent diffusion coefficient as a noninvasive imaging biomarker for the differentiation of invasive breast cancer and ductal carcinoma in situ. Investig Radiol 50:95–100CrossRef Bickel H, Pinker-Domenig K, Bogner W, Spick C, Bagó-Horváth Z, Weber M, Helbich T, Baltzer P (2015) Quantitative apparent diffusion coefficient as a noninvasive imaging biomarker for the differentiation of invasive breast cancer and ductal carcinoma in situ. Investig Radiol 50:95–100CrossRef
13.
go back to reference Harper PR (2005) A review and comparison of classification algorithms for medical decision making. Health Policy 71:315–331CrossRef Harper PR (2005) A review and comparison of classification algorithms for medical decision making. Health Policy 71:315–331CrossRef
14.
go back to reference Baltzer PA, Dietzel M, Kaiser WA (2013) A simple and robust classification tree for differentiation between benign and malignant lesions in MR-mammography. Eur Radiol 23:2051–2060CrossRef Baltzer PA, Dietzel M, Kaiser WA (2013) A simple and robust classification tree for differentiation between benign and malignant lesions in MR-mammography. Eur Radiol 23:2051–2060CrossRef
15.
go back to reference Marino MA, Clauser P, Woitek R, Wengert GJ, Kapetas P, Bernathova M, Pinker-Domenig K, Helbich TH, Preidler K, Baltzer PAT (2016) A simple scoring system for breast MRI interpretation: does it compensate for reader experience? Eur Radiol 26:2529–2537CrossRef Marino MA, Clauser P, Woitek R, Wengert GJ, Kapetas P, Bernathova M, Pinker-Domenig K, Helbich TH, Preidler K, Baltzer PAT (2016) A simple scoring system for breast MRI interpretation: does it compensate for reader experience? Eur Radiol 26:2529–2537CrossRef
16.
go back to reference Woitek R, Spick C, Schernthaner M, Rudas M, Kapetas P, Bernathova M, Furtner J, Pinker K, Helbich TH, Baltzer PAT (2017) A simple classification system (the Tree flowchart) for breast MRI can reduce the number of unnecessary biopsies in MRI-only lesions. Eur Radiol 27:3799–3809CrossRef Woitek R, Spick C, Schernthaner M, Rudas M, Kapetas P, Bernathova M, Furtner J, Pinker K, Helbich TH, Baltzer PAT (2017) A simple classification system (the Tree flowchart) for breast MRI can reduce the number of unnecessary biopsies in MRI-only lesions. Eur Radiol 27:3799–3809CrossRef
17.
go back to reference Ozdemir A, Ozdemir H, Maral I et al (2001) Differential diagnosis of solid breast lesions: contribution of Doppler studies to mammography and gray scale imaging. J Ultrasound Med 20:1091–1101 quiz 1102CrossRef Ozdemir A, Ozdemir H, Maral I et al (2001) Differential diagnosis of solid breast lesions: contribution of Doppler studies to mammography and gray scale imaging. J Ultrasound Med 20:1091–1101 quiz 1102CrossRef
18.
go back to reference Golatta M, Schweitzer-Martin M, Harcos A et al (2014) Evaluation of virtual touch tissue imaging quantification, a new shear wave velocity imaging method, for breast lesion assessment by ultrasound. Biomed Res Int 2014:960262CrossRef Golatta M, Schweitzer-Martin M, Harcos A et al (2014) Evaluation of virtual touch tissue imaging quantification, a new shear wave velocity imaging method, for breast lesion assessment by ultrasound. Biomed Res Int 2014:960262CrossRef
19.
go back to reference Raza S, Baum JK (1997) Solid breast lesions: evaluation with power Doppler US. Radiology 203:164–168CrossRef Raza S, Baum JK (1997) Solid breast lesions: evaluation with power Doppler US. Radiology 203:164–168CrossRef
20.
go back to reference del Cura JL, Elizagaray E, Zabala R, Legórburu A, Grande D (2005) The use of unenhanced Doppler sonography in the evaluation of solid breast lesions. AJR Am J Roentgenol 184:1788–1794CrossRef del Cura JL, Elizagaray E, Zabala R, Legórburu A, Grande D (2005) The use of unenhanced Doppler sonography in the evaluation of solid breast lesions. AJR Am J Roentgenol 184:1788–1794CrossRef
21.
go back to reference Wojcinski S, Brandhorst K, Sadigh G, Hillemanns P, Degenhardt F (2013) Acoustic radiation force impulse imaging with virtual touch tissue quantification: measurements of normal breast tissue and dependence on the degree of pre-compression. Ultrasound Med Biol 39:2226–2232CrossRef Wojcinski S, Brandhorst K, Sadigh G, Hillemanns P, Degenhardt F (2013) Acoustic radiation force impulse imaging with virtual touch tissue quantification: measurements of normal breast tissue and dependence on the degree of pre-compression. Ultrasound Med Biol 39:2226–2232CrossRef
22.
go back to reference Li DD, Xu HX, Guo LH, Bo XW, Li XL, Wu R, Xu JM, Zhang YF, Zhang K (2016) Combination of two-dimensional shear wave elastography with ultrasound breast imaging reporting and data system in the diagnosis of breast lesions: a new method to increase the diagnostic performance. Eur Radiol 26:3290–3300CrossRef Li DD, Xu HX, Guo LH, Bo XW, Li XL, Wu R, Xu JM, Zhang YF, Zhang K (2016) Combination of two-dimensional shear wave elastography with ultrasound breast imaging reporting and data system in the diagnosis of breast lesions: a new method to increase the diagnostic performance. Eur Radiol 26:3290–3300CrossRef
23.
go back to reference Tozaki M, Saito M, Benson J, Fan L, Isobe S (2013) Shear wave velocity measurements for differential diagnosis of solid breast masses: a comparison between virtual touch quantification and virtual touch IQ. Ultrasound Med Biol 39:2233–2245CrossRef Tozaki M, Saito M, Benson J, Fan L, Isobe S (2013) Shear wave velocity measurements for differential diagnosis of solid breast masses: a comparison between virtual touch quantification and virtual touch IQ. Ultrasound Med Biol 39:2233–2245CrossRef
24.
go back to reference Gokalp G, Topal U, Kizilkaya E (2009) Power Doppler sonography: anything to add to BI-RADS US in solid breast masses? Eur J Radiol 70:77–85CrossRef Gokalp G, Topal U, Kizilkaya E (2009) Power Doppler sonography: anything to add to BI-RADS US in solid breast masses? Eur J Radiol 70:77–85CrossRef
25.
go back to reference 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 307:1394–1404CrossRef 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 307:1394–1404CrossRef
26.
go back to reference Athanasiou A, Tardivon A, Tanter M et al (2010) Breast lesions: quantitative elastography with supersonic shear imaging—preliminary results. Radiology 256:297–303CrossRef Athanasiou A, Tardivon A, Tanter M et al (2010) Breast lesions: quantitative elastography with supersonic shear imaging—preliminary results. Radiology 256:297–303CrossRef
27.
go back to reference Liu B, Zheng Y, Huang G, Lin M, Shan Q, Lu Y, Tian W, Xie X (2016) Breast lesions: quantitative diagnosis using ultrasound shear wave elastography—a systematic review and meta-analysis. Ultrasound Med Biol 42:835–847CrossRef Liu B, Zheng Y, Huang G, Lin M, Shan Q, Lu Y, Tian W, Xie X (2016) Breast lesions: quantitative diagnosis using ultrasound shear wave elastography—a systematic review and meta-analysis. Ultrasound Med Biol 42:835–847CrossRef
28.
go back to reference Kass GV (1980) An exploratory technique for investigating large quantities of categorical data. Appl Stat 29:119–127CrossRef Kass GV (1980) An exploratory technique for investigating large quantities of categorical data. Appl Stat 29:119–127CrossRef
29.
go back to reference Kim SY, Woo S, Hwang SI, Moon MH, Sung CK, Lee HJ, Cho JY, Kim SH (2014) Usefulness of resistive index on spectral Doppler ultrasonography in the detection of renal cell carcinoma in patients with end-stage renal disease. Ultrasonography 33:136–142CrossRef Kim SY, Woo S, Hwang SI, Moon MH, Sung CK, Lee HJ, Cho JY, Kim SH (2014) Usefulness of resistive index on spectral Doppler ultrasonography in the detection of renal cell carcinoma in patients with end-stage renal disease. Ultrasonography 33:136–142CrossRef
30.
go back to reference Stanzani D, Chala LF, Barros N, Cerri GG, Chammas MC (2014) Can Doppler or contrast-enhanced ultrasound analysis add diagnostically important information about the nature of breast lesions? Clinics (Sao Paulo) 69:87–92CrossRef Stanzani D, Chala LF, Barros N, Cerri GG, Chammas MC (2014) Can Doppler or contrast-enhanced ultrasound analysis add diagnostically important information about the nature of breast lesions? Clinics (Sao Paulo) 69:87–92CrossRef
31.
go back to reference Gupta K, Chandra T, Kumaresan M, et al. (2017) Role of Color Doppler for assessment of malignancy in solid breast masses: a prospective study. International Journal of Anatomy, Radiology and Surgery 6:RO59-RO65 Gupta K, Chandra T, Kumaresan M, et al. (2017) Role of Color Doppler for assessment of malignancy in solid breast masses: a prospective study. International Journal of Anatomy, Radiology and Surgery 6:RO59-RO65
32.
go back to reference Kettenbach J, Helbich TH, Huber S, Zuna I, Dock W (2005) Computer-assisted quantitative assessment of power Doppler US: effects of microbubble contrast agent in the differentiation of breast tumors. Eur J Radiol 53:238–244CrossRef Kettenbach J, Helbich TH, Huber S, Zuna I, Dock W (2005) Computer-assisted quantitative assessment of power Doppler US: effects of microbubble contrast agent in the differentiation of breast tumors. Eur J Radiol 53:238–244CrossRef
33.
go back to reference Hooley RJ, Scoutt LM, Philpotts LE (2013) Breast ultrasonography: state of the art. Radiology 268:642–659CrossRef Hooley RJ, Scoutt LM, Philpotts LE (2013) Breast ultrasonography: state of the art. Radiology 268:642–659CrossRef
34.
go back to reference Youssefzadeh S, Eibenberger K, Helbich T, Jakesz R, Wolf G (1996) Use of resistance index for the diagnosis of breast tumours. Clin Radiol 51:418–420CrossRef Youssefzadeh S, Eibenberger K, Helbich T, Jakesz R, Wolf G (1996) Use of resistance index for the diagnosis of breast tumours. Clin Radiol 51:418–420CrossRef
35.
go back to reference Ianculescu V, Ciolovan LM, Dunant A, Vielh P, Mazouni C, Delaloge S, Dromain C, Blidaru A, Balleyguier C (2014) Added value of Virtual Touch IQ shear wave elastography in the ultrasound assessment of breast lesions. Eur J Radiol 83:773–777CrossRef Ianculescu V, Ciolovan LM, Dunant A, Vielh P, Mazouni C, Delaloge S, Dromain C, Blidaru A, Balleyguier C (2014) Added value of Virtual Touch IQ shear wave elastography in the ultrasound assessment of breast lesions. Eur J Radiol 83:773–777CrossRef
36.
go back to reference Balleyguier C, Canale S, Ben Hassen W, Vielh P, Bayou EH, Mathieu MC, Uzan C, Bourgier C, Dromain C (2013) Breast elasticity: principles, technique, results: an update and overview of commercially available software. Eur J Radiol 82:427–434CrossRef Balleyguier C, Canale S, Ben Hassen W, Vielh P, Bayou EH, Mathieu MC, Uzan C, Bourgier C, Dromain C (2013) Breast elasticity: principles, technique, results: an update and overview of commercially available software. Eur J Radiol 82:427–434CrossRef
37.
go back to reference Zengin B, Elverici E, Barca N, Cavusoglu M, Duran S, Ozsoy A, Aktas H (2013) Positive predictive values of the sonographic BI-RADS final assessment categories for breast lesions. J Breast Health 9:125–129CrossRef Zengin B, Elverici E, Barca N, Cavusoglu M, Duran S, Ozsoy A, Aktas H (2013) Positive predictive values of the sonographic BI-RADS final assessment categories for breast lesions. J Breast Health 9:125–129CrossRef
38.
go back to reference Skerl K, Vinnicombe S, Thomson K, McLean D, Giannotti E, Evans A (2016) Anisotropy of solid breast lesions in 2D shear wave elastography is an indicator of malignancy. Acad Radiol 23:53–61CrossRef Skerl K, Vinnicombe S, Thomson K, McLean D, Giannotti E, Evans A (2016) Anisotropy of solid breast lesions in 2D shear wave elastography is an indicator of malignancy. Acad Radiol 23:53–61CrossRef
Metadata
Title
A Simple Ultrasound Based Classification Algorithm Allows Differentiation of Benign from Malignant Breast Lesions by Using Only Quantitative Parameters
Authors
Panagiotis Kapetas
Ramona Woitek
Paola Clauser
Maria Bernathova
Katja Pinker
Thomas H. Helbich
Pascal A. Baltzer
Publication date
01-12-2018
Publisher
Springer International Publishing
Published in
Molecular Imaging and Biology / Issue 6/2018
Print ISSN: 1536-1632
Electronic ISSN: 1860-2002
DOI
https://doi.org/10.1007/s11307-018-1187-x

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