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Erschienen in: European Radiology 2/2022

12.08.2021 | Breast

Machine learning with multiparametric breast MRI for prediction of Ki-67 and histologic grade in early-stage luminal breast cancer

verfasst von: Sung Eun Song, Kyu Ran Cho, Yongwon Cho, Kwangsoo Kim, Seung Pil Jung, Bo Kyoung Seo, Ok Hee Woo

Erschienen in: European Radiology | Ausgabe 2/2022

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Abstract

Objectives

To investigate whether machine learning–based prediction models using 3-T multiparametric MRI (mpMRI) can predict Ki-67 and histologic grade in stage I–II luminal cancer.

Methods

Between 2013 and 2019, consecutive women with luminal cancers who underwent preoperative MRI with diffusion-weighted imaging (DWI) and surgery were included. For prediction models, morphology, kinetic features using computer-aided diagnosis (CAD), and apparent diffusion coefficient (ADC) at DWI were evaluated by two radiologists. Logistic regression analysis was used to identify mpMRI features for predicting Ki-67 and grade. Diagnostic performance was assessed using eight machine learning algorithms incorporating mpMRI features and compared using the DeLong method.

Results

Of 300 women, 203 (67.7%) had low Ki-67 and 97 (32.3%) had high Ki-67; 242 (80.7%) had low grade and 58 (19.3%) had high grade. In multivariate analysis, independent predictors for higher Ki-67 were washout component > 13.5% (odds ratio [OR] = 4.16; p < 0.001) and intratumoral high SI on T2-weighted image (OR = 1.89; p = 0.022). Those for higher grade were washout component > 15.5% (OR = 7.22; p < 0.001), rim enhancement (OR = 2.59; p = 0.022), and ADC value < 0.945 × 10-3 mm2/s (OR = 2.47; p = 0.015). Among eight models using these predictors, six models showed the equivalent performance for Ki-67 (area under the receiver operating characteristic curve [AUC]: 0.70) and Naive Bayes classifier showed the highest performance for grade (AUC: 0.79).

Conclusions

A prediction model incorporating mpMRI features shows good diagnostic performance for predicting Ki-67 and histologic grade in patients with luminal breast cancers.

Key Points

• Among multiparametric MRI features, kinetic feature of washout component >13.5% and intratumoral high signal intensity on T2-weighted image were associated with higher Ki-67.
• Washout component >15.5%, rim enhancement, and mean apparent diffusion coefficient value < 0.945 × 10 -3 mm 2 /s were associated with higher histologic grade.
• Machine learning–based prediction models incorporating multiparametric MRI features showed good diagnostic performance for Ki-67 and histologic grade in luminal breast cancers.
Literatur
1.
Zurück zum Zitat Gabriel NH, James LC, Carl JD et al (2017) Breast. In: Amin MB, American Joint Committee on Cancer (eds) AJCC cancer staging manual, 8th edn. Springer, New York, pp 589–628 Gabriel NH, James LC, Carl JD et al (2017) Breast. In: Amin MB, American Joint Committee on Cancer (eds) AJCC cancer staging manual, 8th edn. Springer, New York, pp 589–628
2.
Zurück zum Zitat Konecny G, Pauletti G, Pegram M et al (2003) Quantitative association between HER-2/neu and steroid hormone receptors in hormone receptor-positive primary breast cancer. J Natl Cancer Inst 95(2):142–153CrossRef Konecny G, Pauletti G, Pegram M et al (2003) Quantitative association between HER-2/neu and steroid hormone receptors in hormone receptor-positive primary breast cancer. J Natl Cancer Inst 95(2):142–153CrossRef
3.
Zurück zum Zitat Eiermann W, Rezai M, Kümmel S et al (2013) The 21-gene recurrence score assay impacts adjuvant therapy recommendations for ER-positive, node-negative and node-positive early breast cancer resulting in a risk-adapted change in chemotherapy use. Ann Oncol 24:618–624CrossRef Eiermann W, Rezai M, Kümmel S et al (2013) The 21-gene recurrence score assay impacts adjuvant therapy recommendations for ER-positive, node-negative and node-positive early breast cancer resulting in a risk-adapted change in chemotherapy use. Ann Oncol 24:618–624CrossRef
4.
Zurück zum Zitat Inwald EC, Koller M, Klinkhammer-Schalke M et al (2015) 4-IHC classification of breast cancer subtypes in a large cohort of a clinical cancer registry: use in clinical routine for therapeutic decisions and its effect on survival. Breast Cancer Res Treat 153:647–658CrossRef Inwald EC, Koller M, Klinkhammer-Schalke M et al (2015) 4-IHC classification of breast cancer subtypes in a large cohort of a clinical cancer registry: use in clinical routine for therapeutic decisions and its effect on survival. Breast Cancer Res Treat 153:647–658CrossRef
5.
Zurück zum Zitat Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thürlimann B, Senn HJ (2011) Strategies for subtypes--dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol 22:1736–1747CrossRef Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thürlimann B, Senn HJ (2011) Strategies for subtypes--dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol 22:1736–1747CrossRef
6.
Zurück zum Zitat 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 24:2206–2223CrossRef 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 24:2206–2223CrossRef
7.
Zurück zum Zitat Weigelt B, Baehner FL, Reis-Filho JS (2010) The contribution of gene expression profiling to breast cancer classification, prognostication and prediction: a retrospective of the last decade. J Pathol 220:263–280CrossRef Weigelt B, Baehner FL, Reis-Filho JS (2010) The contribution of gene expression profiling to breast cancer classification, prognostication and prediction: a retrospective of the last decade. J Pathol 220:263–280CrossRef
8.
Zurück zum Zitat Onitilo AA, Engel JM, Greenlee RT, Mukesh BN (2009) Breast cancer subtypes based on ER/PR and Her2 expression: comparison of clinicopathologic features and survival. Clin Med Res 7:4–13CrossRef Onitilo AA, Engel JM, Greenlee RT, Mukesh BN (2009) Breast cancer subtypes based on ER/PR and Her2 expression: comparison of clinicopathologic features and survival. Clin Med Res 7:4–13CrossRef
9.
Zurück zum Zitat Hugh J, Hanson J, Cheang MC et al (2009) Breast cancer subtypes and response to docetaxel in node-positive breast cancer: use of an immunohistochemical definition in the BCIRG 001 trial. J Clin Oncol 27:1168–1176CrossRef Hugh J, Hanson J, Cheang MC et al (2009) Breast cancer subtypes and response to docetaxel in node-positive breast cancer: use of an immunohistochemical definition in the BCIRG 001 trial. J Clin Oncol 27:1168–1176CrossRef
10.
Zurück zum Zitat Ehinger A, Malmström P, Bendahl PO et al (2017) Histological grade provides significant prognostic information in addition to breast cancer subtypes defined according to St Gallen 2013. Acta Oncol 56:68–74CrossRef Ehinger A, Malmström P, Bendahl PO et al (2017) Histological grade provides significant prognostic information in addition to breast cancer subtypes defined according to St Gallen 2013. Acta Oncol 56:68–74CrossRef
11.
Zurück zum Zitat Koh J, Kim MJ (2019) Introduction of a new staging system of breast cancer for radiologists: an emphasis on the prognostic stage. Korean J Radiol 20:69–82CrossRef Koh J, Kim MJ (2019) Introduction of a new staging system of breast cancer for radiologists: an emphasis on the prognostic stage. Korean J Radiol 20:69–82CrossRef
12.
Zurück zum Zitat Mori N, Ota H, Mugikura S et al (2015) Luminal-type breast cancer: correlation of apparent diffusion coefficients with the Ki-67 labeling index. Radiology 274:66–73CrossRef Mori N, Ota H, Mugikura S et al (2015) Luminal-type breast cancer: correlation of apparent diffusion coefficients with the Ki-67 labeling index. Radiology 274:66–73CrossRef
13.
Zurück zum Zitat Surov A, Chang YW, Li L et al (2019) Apparent diffusion coefficient cannot predict molecular subtype and lymph node metastases in invasive breast cancer: a multicenter analysis. BMC Cancer 19:1043CrossRef Surov A, Chang YW, Li L et al (2019) Apparent diffusion coefficient cannot predict molecular subtype and lymph node metastases in invasive breast cancer: a multicenter analysis. BMC Cancer 19:1043CrossRef
14.
Zurück zum Zitat Holli-Helenius K, Salminen A, Rinta-Kiikka I et al (2017) MRI texture analysis in differentiating luminal A and luminal B breast cancer molecular subtypes - a feasibility study. BMC Med Imaging 17:69CrossRef Holli-Helenius K, Salminen A, Rinta-Kiikka I et al (2017) MRI texture analysis in differentiating luminal A and luminal B breast cancer molecular subtypes - a feasibility study. BMC Med Imaging 17:69CrossRef
15.
Zurück zum Zitat Grimm LJ, Zhang J, Mazurowski MA (2015) Computational approach to radiogenomics of breast cancer: luminal A and luminal B molecular subtypes are associated with imaging features on routine breast MRI extracted using computer vision algorithms. J Magn Reson Imaging 42:902–907CrossRef Grimm LJ, Zhang J, Mazurowski MA (2015) Computational approach to radiogenomics of breast cancer: luminal A and luminal B molecular subtypes are associated with imaging features on routine breast MRI extracted using computer vision algorithms. J Magn Reson Imaging 42:902–907CrossRef
16.
Zurück zum Zitat Pinker K, Helbich TH, Morris EA (2017) The potential of multiparametric MRI of the breast. Br J Radiol 90(1069):20160715CrossRef Pinker K, Helbich TH, Morris EA (2017) The potential of multiparametric MRI of the breast. Br J Radiol 90(1069):20160715CrossRef
17.
Zurück zum Zitat Morris EA, Comstock CE, Lee C et al (2013) ACR BI-RADS Magnetic resonance imaging. In: D'Orsi CJ, Sickles EA, Mendelson EB, Morris EA (eds) ACR BI-RADS Atlas, breast imaging and reporting data system, 5th edn. Reston, American College of Radiology Morris EA, Comstock CE, Lee C et al (2013) ACR BI-RADS Magnetic resonance imaging. In: D'Orsi CJ, Sickles EA, Mendelson EB, Morris EA (eds) ACR BI-RADS Atlas, breast imaging and reporting data system, 5th edn. Reston, American College of Radiology
18.
Zurück zum Zitat Baltzer PA, Yang F, Dietzel M et al (2010) Sensitivity and specificity of unilateral edema on T2w-TSE sequences in MR-mammography considering 974 histologically verified lesions. Breast J 16:233–239CrossRef Baltzer PA, Yang F, Dietzel M et al (2010) Sensitivity and specificity of unilateral edema on T2w-TSE sequences in MR-mammography considering 974 histologically verified lesions. Breast J 16:233–239CrossRef
19.
Zurück zum Zitat Uematsu T, Kasami M, Watanabe J (2014) Is evaluation of the presence of prepectoral edema on T2-weighted with fat-suppression 3 T breast MRI a simple and readily available noninvasive technique for estimation of prognosis in patients with breast cancer? Breast Cancer 21:684–692 Uematsu T, Kasami M, Watanabe J (2014) Is evaluation of the presence of prepectoral edema on T2-weighted with fat-suppression 3 T breast MRI a simple and readily available noninvasive technique for estimation of prognosis in patients with breast cancer? Breast Cancer 21:684–692
20.
Zurück zum Zitat Levman JE, Causer P, Warner E, Martel AL (2009) Effect of the enhancement threshold on the computer-aided detection of breast cancer using MRI. Acad Radiol 16:1064–1069CrossRef Levman JE, Causer P, Warner E, Martel AL (2009) Effect of the enhancement threshold on the computer-aided detection of breast cancer using MRI. Acad Radiol 16:1064–1069CrossRef
21.
Zurück zum Zitat Hammond ME, Hayes DF, Dowsett M et al (2010) American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol 28:2784–2795CrossRef Hammond ME, Hayes DF, Dowsett M et al (2010) American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol 28:2784–2795CrossRef
22.
Zurück zum Zitat Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRef Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRef
23.
Zurück zum Zitat Lee SH, Cho N, Kim SJ (2008) Correlation between high resolution dynamic MR features and prognostic factors in breast cancer. Korean J Radiol 9:10–18CrossRef Lee SH, Cho N, Kim SJ (2008) Correlation between high resolution dynamic MR features and prognostic factors in breast cancer. Korean J Radiol 9:10–18CrossRef
24.
Zurück zum Zitat Kim JJ, Kim JY, Kang HJ et al (2017) Computer-aided diagnosis-generated kinetic features of breast cancer at preoperative MR imaging: association with disease-free survival of patients with primary operable invasive breast cancer. Radiology 284:45–54CrossRef Kim JJ, Kim JY, Kang HJ et al (2017) Computer-aided diagnosis-generated kinetic features of breast cancer at preoperative MR imaging: association with disease-free survival of patients with primary operable invasive breast cancer. Radiology 284:45–54CrossRef
25.
Zurück zum Zitat Yi A, Cho N, Im SA et al (2013) Survival outcomes of breast cancer patients who receive neoadjuvant chemotherapy: association with dynamic contrast-enhanced MR imaging with computer-aided evaluation. Radiology 268:662–672CrossRef Yi A, Cho N, Im SA et al (2013) Survival outcomes of breast cancer patients who receive neoadjuvant chemotherapy: association with dynamic contrast-enhanced MR imaging with computer-aided evaluation. Radiology 268:662–672CrossRef
26.
Zurück zum Zitat Toi M, Inada K, Suzuki H, Tominaga T (1999) Tumor angiogenesis in breast cancer: its importance as a prognostic indicator and the association with vascular endothelial growth factor expression. Breast Cancer Res Treat 36:193–204CrossRef Toi M, Inada K, Suzuki H, Tominaga T (1999) Tumor angiogenesis in breast cancer: its importance as a prognostic indicator and the association with vascular endothelial growth factor expression. Breast Cancer Res Treat 36:193–204CrossRef
27.
Zurück zum Zitat Uzzan B, Nicolas P, Cucherat M, Perret GY (2004) Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res 64:2941–2955CrossRef Uzzan B, Nicolas P, Cucherat M, Perret GY (2004) Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res 64:2941–2955CrossRef
28.
Zurück zum Zitat Kim SY, Kim EK, Moon HJ et al (2018) Association among T2 signal intensity, necrosis, ADC and Ki-67 in estrogen receptor-positive and HER2-negative invasive ductal carcinoma. Magn Reson Imaging 54:176–182CrossRef Kim SY, Kim EK, Moon HJ et al (2018) Association among T2 signal intensity, necrosis, ADC and Ki-67 in estrogen receptor-positive and HER2-negative invasive ductal carcinoma. Magn Reson Imaging 54:176–182CrossRef
29.
Zurück zum Zitat Leek RD, Landers RJ, Harris AL, Lewis CE (1999) Necrosis correlates with high vascular density and focal macrophage infiltration in invasive carcinoma of the breast. Br J Cancer 79:991–995CrossRef Leek RD, Landers RJ, Harris AL, Lewis CE (1999) Necrosis correlates with high vascular density and focal macrophage infiltration in invasive carcinoma of the breast. Br J Cancer 79:991–995CrossRef
30.
Zurück zum Zitat Surov A, Clauser P, Chang YW et al (2018) Can diffusion-weighted imaging predict tumor grade and expression of Ki-67 in breast cancer? A multicenter analysis. Breast Cancer Res 20:58CrossRef Surov A, Clauser P, Chang YW et al (2018) Can diffusion-weighted imaging predict tumor grade and expression of Ki-67 in breast cancer? A multicenter analysis. Breast Cancer Res 20:58CrossRef
31.
Zurück zum Zitat Costantini M, Belli P, Rinaldi P et al (2010) Diffusion-weighted imaging in breast cancer: relationship between apparent diffusion coefficient and tumour aggressiveness. Clin Radiol 65:1005–1012CrossRef Costantini M, Belli P, Rinaldi P et al (2010) Diffusion-weighted imaging in breast cancer: relationship between apparent diffusion coefficient and tumour aggressiveness. Clin Radiol 65:1005–1012CrossRef
32.
Zurück zum Zitat Kim KW, Kuzmiak CM, Kim YJ, Seo JY, Jung HK, Lee MS (2018) Diagnostic usefulness of combination of diffusion-weighted imaging and T2WI, including apparent diffusion coefficient in breast lesions: assessment of histologic grade. Acad Radiol 25:643–652CrossRef Kim KW, Kuzmiak CM, Kim YJ, Seo JY, Jung HK, Lee MS (2018) Diagnostic usefulness of combination of diffusion-weighted imaging and T2WI, including apparent diffusion coefficient in breast lesions: assessment of histologic grade. Acad Radiol 25:643–652CrossRef
33.
Zurück zum Zitat Song SE, Shin SU, Moon HG, Ryu HS, Kim K, Moon WK (2017) MR imaging features associated with distant metastasis-free survival of patients with invasive breast cancer: a case-control study. Breast Cancer Res Treat 162:559–569CrossRef Song SE, Shin SU, Moon HG, Ryu HS, Kim K, Moon WK (2017) MR imaging features associated with distant metastasis-free survival of patients with invasive breast cancer: a case-control study. Breast Cancer Res Treat 162:559–569CrossRef
34.
Zurück zum Zitat Yamamoto S, Maki DD, Korn RL, Kuo MD (2012) Radiogenomic analysis of breast cancer using MRI: a preliminary study to define the landscape. AJR Am J Roentgenol 199:654–663CrossRef Yamamoto S, Maki DD, Korn RL, Kuo MD (2012) Radiogenomic analysis of breast cancer using MRI: a preliminary study to define the landscape. AJR Am J Roentgenol 199:654–663CrossRef
35.
Zurück zum Zitat Lo Gullo R, Eskreis-Winkler S, Morris EA, Pinker K (2020) Machine learning with multiparametric magnetic resonance imaging of the breast for early prediction of response to neoadjuvant chemotherapy. Breast 49:115–122CrossRef Lo Gullo R, Eskreis-Winkler S, Morris EA, Pinker K (2020) Machine learning with multiparametric magnetic resonance imaging of the breast for early prediction of response to neoadjuvant chemotherapy. Breast 49:115–122CrossRef
36.
Zurück zum Zitat Reig B, Heacock L, Geras KJ, Moy L (2020) Machine learning in breast MRI. J Magn Reson Imaging 52:998–1018CrossRef Reig B, Heacock L, Geras KJ, Moy L (2020) Machine learning in breast MRI. J Magn Reson Imaging 52:998–1018CrossRef
37.
Zurück zum Zitat Eun NL, Kang D, Son EJ et al (2020) Texture analysis with 3.0-T MRI for association of response to neoadjuvant chemotherapy in breast cancer. Radiology 294:31–41CrossRef Eun NL, Kang D, Son EJ et al (2020) Texture analysis with 3.0-T MRI for association of response to neoadjuvant chemotherapy in breast cancer. Radiology 294:31–41CrossRef
38.
Zurück zum Zitat Dalmiş MU, Gubern-Mérida A, Vreemann S et al (2019) Artificial intelligence-based classification of breast lesions imaged with a multiparametric breast MRI protocol with ultrafast DCE-MRI, T2, and DWI. Invest Radiol 54:325–332CrossRef Dalmiş MU, Gubern-Mérida A, Vreemann S et al (2019) Artificial intelligence-based classification of breast lesions imaged with a multiparametric breast MRI protocol with ultrafast DCE-MRI, T2, and DWI. Invest Radiol 54:325–332CrossRef
Metadaten
Titel
Machine learning with multiparametric breast MRI for prediction of Ki-67 and histologic grade in early-stage luminal breast cancer
verfasst von
Sung Eun Song
Kyu Ran Cho
Yongwon Cho
Kwangsoo Kim
Seung Pil Jung
Bo Kyoung Seo
Ok Hee Woo
Publikationsdatum
12.08.2021
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 2/2022
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-021-08127-x

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