Skip to main content
Top
Published in: European Radiology 3/2019

01-03-2019 | Magnetic Resonance

Added value of mean and entropy of apparent diffusion coefficient values for evaluating histologic phenotypes of invasive ductal breast cancer with MR imaging

Authors: Shiteng Suo, Dandan Zhang, Fang Cheng, Mengqiu Cao, Jia Hua, Jinsong Lu, Jianrong Xu

Published in: European Radiology | Issue 3/2019

Login to get access

Abstract

Objectives

To study the added value of mean and entropy of apparent diffusion coefficient (ADC) values at standard (800 s/mm2) and high (1500 s/mm2) b-values obtained with diffusion-weighted imaging in identifying histologic phenotypes of invasive ductal breast cancer (IDC) with MR imaging.

Methods

One hundred thirty-four IDC patients underwent diffusion-weighted imaging with b-values of 800 and 1500 s/mm2, and corresponding ADC800 and ADC1500 maps were generated. Mean and entropy of volumetric ADC values were compared with molecular markers (estrogen receptor [ER], progesterone receptor [PR], human epidermal growth factor receptor 2 [HER2], and Ki-67). Associations among morphologic features, ADC metrics, and phenotypes (luminal A, luminal B [HER2 negative], luminal B [HER2 positive], HER2 positive, and triple negative) were evaluated.

Results

Mean ADC values were significantly decreased in ER-positive, PR-positive, and HER2-negative tumors (p < 0.01). Ki-67 ≥ 20% tumors demonstrated significantly higher ADC entropy values compared with Ki-67 < 20% tumors (p < 0.001). Luminal A subtype tended to display lower ADC entropy values compared with other subtypes, while HER2-positive subtype tended to display higher mean ADC values. ADC1500 entropy provided superior diagnostic performance over ADC800 entropy (p = 0.04). Independent risk factors were ADC1500 entropy (p = 0.002) associated with luminal A, irregular mass shape (p = 0.018) and ADC1500 entropy (p = 0.022) with luminal B (HER2 positive), mean ADC1500 (p = 0.018) with HER2 positive, and smooth mass margin (p = 0.012) and rim enhancement (p = 0.003) with triple negative.

Conclusions

Mean and entropy of ADC values provided complementary information and added value for evaluating IDC histologic phenotypes. High-b-value ADC1500 may facilitate better phenotype discrimination.

Key Points

• ADC metrics are associated with molecular marker status in IDC.
• ADC 1500 improves differentiation of histologic phenotypes compared with ADC 800 .
• ADC metrics add value to morphologic features in IDC phenotyping.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lam SW, Jimenez CR, Boven E (2014) Breast cancer classification by proteomic technologies: current state of knowledge. Cancer Treat Rev 40:129–138CrossRefPubMed Lam SW, Jimenez CR, Boven E (2014) Breast cancer classification by proteomic technologies: current state of knowledge. Cancer Treat Rev 40:129–138CrossRefPubMed
2.
go back to reference Goldhirsch A, Winer EP, Coates AS et al (2013) 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 24:2206–2223CrossRefPubMedPubMedCentral Goldhirsch A, Winer EP, Coates AS et al (2013) 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 24:2206–2223CrossRefPubMedPubMedCentral
3.
go back to reference Marusyk A, Polyak K (2010) Tumor heterogeneity: causes and consequences. Biochim Biophys Acta 1805:105–117PubMed Marusyk A, Polyak K (2010) Tumor heterogeneity: causes and consequences. Biochim Biophys Acta 1805:105–117PubMed
4.
go back to reference O'Connor JP, Rose CJ, Waterton JC, Carano RA, Parker GJ, Jackson A (2015) Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res 21:249–257CrossRefPubMed O'Connor JP, Rose CJ, Waterton JC, Carano RA, Parker GJ, Jackson A (2015) Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res 21:249–257CrossRefPubMed
5.
go back to reference Catalano OA, Horn GL, Signore A et al (2017) PET/MR in invasive ductal breast cancer: correlation between imaging markers and histological phenotype. Br J Cancer 116:893–902CrossRefPubMedPubMedCentral Catalano OA, Horn GL, Signore A et al (2017) PET/MR in invasive ductal breast cancer: correlation between imaging markers and histological phenotype. Br J Cancer 116:893–902CrossRefPubMedPubMedCentral
6.
go back to reference Jeh SK, Kim SH, Kim HS et al (2011) Correlation of the apparent diffusion coefficient value and dynamic magnetic resonance imaging findings with prognostic factors in invasive ductal carcinoma. J Magn Reson Imaging 33:102–109CrossRefPubMed Jeh SK, Kim SH, Kim HS et al (2011) Correlation of the apparent diffusion coefficient value and dynamic magnetic resonance imaging findings with prognostic factors in invasive ductal carcinoma. J Magn Reson Imaging 33:102–109CrossRefPubMed
7.
go back to reference Kim EJ, Kim SH, Park GE et al (2015) Histogram analysis of apparent diffusion coefficient at 3.0t: Correlation with prognostic factors and subtypes of invasive ductal carcinoma. J Magn Reson Imaging 42:1666–1678CrossRefPubMed Kim EJ, Kim SH, Park GE et al (2015) Histogram analysis of apparent diffusion coefficient at 3.0t: Correlation with prognostic factors and subtypes of invasive ductal carcinoma. J Magn Reson Imaging 42:1666–1678CrossRefPubMed
8.
go back to reference Martincich L, Deantoni V, Bertotto I et al (2012) Correlations between diffusion-weighted imaging and breast cancer biomarkers. Eur Radiol 22:1519–1528CrossRefPubMed Martincich L, Deantoni V, Bertotto I et al (2012) Correlations between diffusion-weighted imaging and breast cancer biomarkers. Eur Radiol 22:1519–1528CrossRefPubMed
9.
go back to reference Guvenc I, Akay S, Ince S et al (2016) Apparent diffusion coefficient value in invasive ductal carcinoma at 3.0 Tesla: is it correlated with prognostic factors? Br J Radiol 89:20150614CrossRefPubMedPubMedCentral Guvenc I, Akay S, Ince S et al (2016) Apparent diffusion coefficient value in invasive ductal carcinoma at 3.0 Tesla: is it correlated with prognostic factors? Br J Radiol 89:20150614CrossRefPubMedPubMedCentral
10.
go back to reference Karan B, Pourbagher A, Torun N (2016) Diffusion-weighted imaging and (18) F-fluorodeoxyglucose positron emission tomography/computed tomography in breast cancer: Correlation of the apparent diffusion coefficient and maximum standardized uptake values with prognostic factors. J Magn Reson Imaging 43:1434–1444CrossRefPubMed Karan B, Pourbagher A, Torun N (2016) Diffusion-weighted imaging and (18) F-fluorodeoxyglucose positron emission tomography/computed tomography in breast cancer: Correlation of the apparent diffusion coefficient and maximum standardized uptake values with prognostic factors. J Magn Reson Imaging 43:1434–1444CrossRefPubMed
12.
go back to reference Suo S, Zhang K, Cao M et al (2016) Characterization of breast masses as benign or malignant at 3.0T MRI with whole-lesion histogram analysis of the apparent diffusion coefficient. J Magn Reson Imaging 43:894–902CrossRefPubMed Suo S, Zhang K, Cao M et al (2016) Characterization of breast masses as benign or malignant at 3.0T MRI with whole-lesion histogram analysis of the apparent diffusion coefficient. J Magn Reson Imaging 43:894–902CrossRefPubMed
13.
go back to reference Shin HJ, Kim SH, Lee HJ et al (2016) Tumor apparent diffusion coefficient as an imaging biomarker to predict tumor aggressiveness in patients with estrogen-receptor-positive breast cancer. NMR Biomed 29:1070–1078CrossRefPubMed Shin HJ, Kim SH, Lee HJ et al (2016) Tumor apparent diffusion coefficient as an imaging biomarker to predict tumor aggressiveness in patients with estrogen-receptor-positive breast cancer. NMR Biomed 29:1070–1078CrossRefPubMed
14.
go back to reference American College of Radiology (2013) Breast Imaging Reporting and Data System (BI-RADS), 5th edn. American College of Radiology, Reston, VA American College of Radiology (2013) Breast Imaging Reporting and Data System (BI-RADS), 5th edn. American College of Radiology, Reston, VA
15.
go back to reference Uematsu T, Kasami M, Yuen S (2009) Triple-negative breast cancer: correlation between MR imaging and pathologic findings. Radiology 250:638–647CrossRefPubMed Uematsu T, Kasami M, Yuen S (2009) Triple-negative breast cancer: correlation between MR imaging and pathologic findings. Radiology 250:638–647CrossRefPubMed
16.
go back to reference Arponen O, Masarwah A, Sutela A et al (2016) Incidentally detected enhancing lesions found in breast MRI: analysis of apparent diffusion coefficient and T2 signal intensity significantly improves specificity. Eur Radiol 26:4361–4370CrossRefPubMed Arponen O, Masarwah A, Sutela A et al (2016) Incidentally detected enhancing lesions found in breast MRI: analysis of apparent diffusion coefficient and T2 signal intensity significantly improves specificity. Eur Radiol 26:4361–4370CrossRefPubMed
17.
go back to reference Fujimoto K, Tonan T, Azuma S et al (2011) Evaluation of the mean and entropy of apparent diffusion coefficient values in chronic hepatitis C: correlation with pathologic fibrosis stage and inflammatory activity grade. Radiology 258:739–748CrossRefPubMed Fujimoto K, Tonan T, Azuma S et al (2011) Evaluation of the mean and entropy of apparent diffusion coefficient values in chronic hepatitis C: correlation with pathologic fibrosis stage and inflammatory activity grade. Radiology 258:739–748CrossRefPubMed
18.
go back to reference Kim JH, Ko ES, Lim Y et al (2017) Breast Cancer Heterogeneity: MR Imaging Texture Analysis and Survival Outcomes. Radiology 282:665–675CrossRefPubMed Kim JH, Ko ES, Lim Y et al (2017) Breast Cancer Heterogeneity: MR Imaging Texture Analysis and Survival Outcomes. Radiology 282:665–675CrossRefPubMed
19.
go back to reference Bustreo S, Osella-Abate S, Cassoni P et al (2016) Optimal Ki67 cut-off for luminal breast cancer prognostic evaluation: a large case series study with a long-term follow-up. Breast Cancer Res Treat 157:363–371CrossRefPubMedPubMedCentral Bustreo S, Osella-Abate S, Cassoni P et al (2016) Optimal Ki67 cut-off for luminal breast cancer prognostic evaluation: a large case series study with a long-term follow-up. Breast Cancer Res Treat 157:363–371CrossRefPubMedPubMedCentral
20.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRefPubMed DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRefPubMed
21.
go back to reference Iima M, Kataoka M, Kanao S et al (2018) Intravoxel incoherent motion and quantitative non-Gaussian diffusion MR imaging: evaluation of the diagnostic and prognostic value of several markers of malignant and benign breast lesions. Radiology 287:432–441CrossRefPubMed Iima M, Kataoka M, Kanao S et al (2018) Intravoxel incoherent motion and quantitative non-Gaussian diffusion MR imaging: evaluation of the diagnostic and prognostic value of several markers of malignant and benign breast lesions. Radiology 287:432–441CrossRefPubMed
22.
go back to reference Ludovini V, Sidoni A, Pistola L et al (2003) Evaluation of the prognostic role of vascular endothelial growth factor and microvessel density in stages I and II breast cancer patients. Breast Cancer Res Treat 81:159–168CrossRefPubMed Ludovini V, Sidoni A, Pistola L et al (2003) Evaluation of the prognostic role of vascular endothelial growth factor and microvessel density in stages I and II breast cancer patients. Breast Cancer Res Treat 81:159–168CrossRefPubMed
23.
go back to reference Jarque F, Lluch A, Vera FJ et al (1990) Intratumoral variation of estrogen and progesterone receptors in breast cancer: relationship with histopathological characteristics of the tumor. Oncology 47:9–13CrossRefPubMed Jarque F, Lluch A, Vera FJ et al (1990) Intratumoral variation of estrogen and progesterone receptors in breast cancer: relationship with histopathological characteristics of the tumor. Oncology 47:9–13CrossRefPubMed
24.
go back to reference Järvinen TA, Pelto-Huikko M, Holli K, Isola J (2000) Estrogen receptor beta is coexpressed with ERalpha and PR and associated with nodal status, grade, and proliferation rate in breast cancer. Am J Pathol 156:29–35CrossRefPubMedPubMedCentral Järvinen TA, Pelto-Huikko M, Holli K, Isola J (2000) Estrogen receptor beta is coexpressed with ERalpha and PR and associated with nodal status, grade, and proliferation rate in breast cancer. Am J Pathol 156:29–35CrossRefPubMedPubMedCentral
25.
go back to reference Vazquez-Martin A, Colomer R, Menendez JA (2007) Protein array technology to detect HER2 (erbB-2)-induced 'cytokine signature' in breast cancer. Eur J Cancer 43:1117–1124CrossRefPubMed Vazquez-Martin A, Colomer R, Menendez JA (2007) Protein array technology to detect HER2 (erbB-2)-induced 'cytokine signature' in breast cancer. Eur J Cancer 43:1117–1124CrossRefPubMed
26.
go back to reference Kontzoglou K, Palla V, Karaolanis G et al (2013) Correlation between Ki67 and breast cancer prognosis. Oncology 84:219–225CrossRefPubMed Kontzoglou K, Palla V, Karaolanis G et al (2013) Correlation between Ki67 and breast cancer prognosis. Oncology 84:219–225CrossRefPubMed
27.
go back to reference Suo S, Cheng F, Cao M et al (2017) Multiparametric diffusion-weighted imaging in breast lesions: Association with pathologic diagnosis and prognostic factors. J Magn Reson Imaging 46:740–750CrossRefPubMed Suo S, Cheng F, Cao M et al (2017) Multiparametric diffusion-weighted imaging in breast lesions: Association with pathologic diagnosis and prognostic factors. J Magn Reson Imaging 46:740–750CrossRefPubMed
28.
go back to reference Lee HS, Kim SH, Kang BJ, Baek JE, Song BJ (2016) Perfusion parameters in dynamic contrast-enhanced MRI and apparent diffusion coefficient value in diffusion-weighted MRI: association with prognostic factors in breast cancer. Acad Radiol 23:446–456CrossRefPubMed Lee HS, Kim SH, Kang BJ, Baek JE, Song BJ (2016) Perfusion parameters in dynamic contrast-enhanced MRI and apparent diffusion coefficient value in diffusion-weighted MRI: association with prognostic factors in breast cancer. Acad Radiol 23:446–456CrossRefPubMed
29.
go back to reference Surov A, Meyer HJ, Wienke A (2017) Associations between apparent diffusion coefficient (ADC) and KI 67 in different tumors: a meta-analysis. Part 1: ADCmean. Oncotarget 8:75434–75444PubMedPubMedCentral Surov A, Meyer HJ, Wienke A (2017) Associations between apparent diffusion coefficient (ADC) and KI 67 in different tumors: a meta-analysis. Part 1: ADCmean. Oncotarget 8:75434–75444PubMedPubMedCentral
30.
31.
go back to reference Youk JH, Son EJ, Chung J, Kim JA, Kim EK (2012) Triple-negative invasive breast cancer on dynamic contrast-enhanced and diffusion-weighted MR imaging: comparison with other breast cancer subtypes. Eur Radiol 22:1724–1734CrossRefPubMed Youk JH, Son EJ, Chung J, Kim JA, Kim EK (2012) Triple-negative invasive breast cancer on dynamic contrast-enhanced and diffusion-weighted MR imaging: comparison with other breast cancer subtypes. Eur Radiol 22:1724–1734CrossRefPubMed
32.
go back to reference Takanaga M, Hayashi N, Miyati T et al (2012) Influence of b value on the measurement of contrast and apparent diffusion coefficient in 3.0 Tesla breast magnetic resonance imaging. Nihon Hoshasen Gijutsu Gakkai Zasshi 68:201–208CrossRefPubMed Takanaga M, Hayashi N, Miyati T et al (2012) Influence of b value on the measurement of contrast and apparent diffusion coefficient in 3.0 Tesla breast magnetic resonance imaging. Nihon Hoshasen Gijutsu Gakkai Zasshi 68:201–208CrossRefPubMed
33.
go back to reference Tamura T, Murakami S, Naito K, Yamada T, Fujimoto T, Kikkawa T (2014) Investigation of the optimal b-value to detect breast tumors with diffusion weighted imaging by 1.5-T MRI. Cancer Imaging 14:11PubMedPubMedCentral Tamura T, Murakami S, Naito K, Yamada T, Fujimoto T, Kikkawa T (2014) Investigation of the optimal b-value to detect breast tumors with diffusion weighted imaging by 1.5-T MRI. Cancer Imaging 14:11PubMedPubMedCentral
Metadata
Title
Added value of mean and entropy of apparent diffusion coefficient values for evaluating histologic phenotypes of invasive ductal breast cancer with MR imaging
Authors
Shiteng Suo
Dandan Zhang
Fang Cheng
Mengqiu Cao
Jia Hua
Jinsong Lu
Jianrong Xu
Publication date
01-03-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 3/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5667-9

Other articles of this Issue 3/2019

European Radiology 3/2019 Go to the issue