Combining multiparametric MRI with receptor information to optimize prediction of pathologic response to neoadjuvant therapy in breast cancer: preliminary results

Abstract Pathologic complete response following neoadjuvant therapy (NAT) is used as a short-term surrogate marker of eventual outcome in patients with breast cancer. Analyzing voxel-level heterogeneity in MRI-derived parametric maps, obtained before and after the first cycle of NAT (n=33), in conjunction with receptor status, may improve the predictive accuracy of tumor response to NAT. Toward that end, we incorporated two MRI-derived parameters, the apparent diffusion coefficient and efflux rate constant, with receptor status in a logistic ridge-regression model. The area under the curve (AUC) and Brier score of the model computed via 10-fold cross validation were 0.94 (95% CI: 0.85, 0.99) and 0.11 (95% CI: 0.06, 0.16), respectively. These two statistics strongly support the hypothesis that our proposed model outperforms the other models that we investigated (namely, models without either receptor information or voxel-level information). The contribution of the receptor information was manifested by an 8% to 15% increase in AUC and a 14% to 21% decrease in Brier score. These data indicate that combining multiparametric MRI with hormone receptor status has a high likelihood of improved prediction of pathologic response to NAT in breast cancer.

[1]  C. Meyer,et al.  Evaluation of the functional diffusion map as an early biomarker of time-to-progression and overall survival in high-grade glioma. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[2]  A. L. V. D. Wollenberg Redundancy analysis an alternative for canonical correlation analysis , 1977 .

[3]  T. Nagaoka,et al.  Neoadjuvant chemotherapy in breast cancer: prediction of pathologic response with PET/CT and dynamic contrast-enhanced MR imaging--prospective assessment. , 2012, Radiology.

[4]  Thomas E Yankeelov,et al.  Integration of quantitative DCE-MRI and ADC mapping to monitor treatment response in human breast cancer: initial results. , 2007, Magnetic resonance imaging.

[5]  Matthew Blackledge,et al.  Evaluating the diagnostic sensitivity of computed diffusion‐weighted MR imaging in the detection of breast cancer , 2016, Journal of magnetic resonance imaging : JMRI.

[6]  H Putter,et al.  Accuracy of MRI for treatment response assessment after taxane- and anthracycline-based neoadjuvant chemotherapy in HER2-negative breast cancer. , 2014, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[7]  Xia Li,et al.  Analyzing Spatial Heterogeneity in DCE- and DW-MRI Parametric Maps to Optimize Prediction of Pathologic Response to Neoadjuvant Chemotherapy in Breast Cancer. , 2014, Translational oncology.

[8]  Jia Huajie,et al.  Can diffusion-weighted MR imaging and contrast-enhanced MR imaging precisely evaluate and predict pathological response to neoadjuvant chemotherapy in patients with breast cancer? , 2012 .

[9]  Steinar Lundgren,et al.  Prognostic value of pretreatment dynamic contrast-enhanced MR imaging in breast cancer patients receiving neoadjuvant chemotherapy: Overall survival predicted from combined time course and volume analysis , 2010, Acta radiologica.

[10]  S. Cessie,et al.  Ridge Estimators in Logistic Regression , 1992 .

[11]  J C Gore,et al.  Effects of cell volume fraction changes on apparent diffusion in human cells. , 2000, Magnetic resonance imaging.

[12]  Andreas Makris,et al.  Early Changes in Functional Dynamic Magnetic Resonance Imaging Predict for Pathologic Response to Neoadjuvant Chemotherapy in Primary Breast Cancer , 2008, Clinical Cancer Research.

[13]  G. Fan,et al.  Usefulness of diffusion/perfusion-weighted MRI in rat gliomas: correlation with histopathology. , 2005, Academic radiology.

[14]  Oliver Geier,et al.  Diffusion-weighted magnetic resonance imaging for pretreatment prediction and monitoring of treatment response of patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy , 2010, Acta oncologica.

[15]  Steinar Lundgren,et al.  Predicting survival and early clinical response to primary chemotherapy for patients with locally advanced breast cancer using DCE‐MRI , 2009, Journal of magnetic resonance imaging : JMRI.

[16]  Yoshitsugu Matsumoto,et al.  In vitro experimental study of the relationship between the apparent diffusion coefficient and changes in cellularity and cell morphology. , 2009, Oncology reports.

[17]  B. Efron Estimating the Error Rate of a Prediction Rule: Improvement on Cross-Validation , 1983 .

[18]  S. Sener,et al.  Neoadjuvant therapy for breast cancer , 2010, Journal of surgical oncology.

[19]  Ming-Ting Wu,et al.  Monitoring breast cancer response to neoadjuvant systemic chemotherapy using parametric contrast-enhanced MRI: a pilot study. , 2007, Academic radiology.

[20]  S. Gautam,et al.  Identification of residual breast carcinoma following neoadjuvant chemotherapy: diffusion-weighted imaging--comparison with contrast-enhanced MR imaging and pathologic findings. , 2010, Radiology.

[21]  Yoshiaki Sota,et al.  Prediction of pathological complete response to neoadjuvant chemotherapy by magnetic resonance imaging in breast cancer patients. , 2015, Breast.

[22]  Andreas Makris,et al.  Use of dynamic contrast-enhanced MR imaging to predict survival in patients with primary breast cancer undergoing neoadjuvant chemotherapy. , 2011, Radiology.

[23]  Anthony Rhodes,et al.  American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. , 2010, Archives of pathology & laboratory medicine.

[24]  Xia Li,et al.  DCE‐MRI analysis methods for predicting the response of breast cancer to neoadjuvant chemotherapy: Pilot study findings , 2014, Magnetic resonance in medicine.

[25]  Lorenzo Bonomo,et al.  Diffusion‐weighted Imaging in Evaluating the Response to Neoadjuvant Breast Cancer Treatment , 2011, The breast journal.

[26]  L. Turnbull,et al.  Prognostic value of pre-treatment DCE-MRI parameters in predicting disease free and overall survival for breast cancer patients undergoing neoadjuvant chemotherapy. , 2009, European journal of radiology.

[27]  U. Sharma,et al.  Longitudinal study of the assessment by MRI and diffusion‐weighted imaging of tumor response in patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy , 2009, NMR in biomedicine.

[28]  Claude B. Sirlin,et al.  Automated registration of sequential breath-hold dynamic contrast-enhanced MR images: a comparison of three techniques. , 2011, Magnetic resonance imaging.

[29]  E. Öztürk,et al.  Diffusion Weighted MR Imaging of Breast and Correlation of Prognostic Factors in Breast Cancer. , 2016, Balkan medical journal.

[30]  Jie Chen,et al.  Can diffusion-weighted MR imaging and contrast-enhanced MR imaging precisely evaluate and predict pathological response to neoadjuvant chemotherapy in patients with breast cancer? , 2012, Breast Cancer Research and Treatment.

[31]  Woo Kyung Moon,et al.  Comparison of diffusion-weighted MR imaging and FDG PET/CT to predict pathological complete response to neoadjuvant chemotherapy in patients with breast cancer , 2011, European Radiology.

[32]  Naranamangalam R Jagannathan,et al.  Role of apparent diffusion coefficient values for the differentiation of viable and necrotic areas of breast cancer and its potential utility to guide voxel positioning for MRS in the absence of dynamic contrast-enhanced MRI data. , 2012, Magnetic resonance imaging.

[33]  Lars J. Grimm,et al.  Can breast cancer molecular subtype help to select patients for preoperative MR imaging? , 2015, Radiology.

[34]  Ruijiang Li,et al.  Intratumor partitioning and texture analysis of dynamic contrast‐enhanced (DCE)‐MRI identifies relevant tumor subregions to predict pathological response of breast cancer to neoadjuvant chemotherapy , 2016, Journal of magnetic resonance imaging : JMRI.

[35]  Carmel Hayes,et al.  Prediction of clinicopathologic response of breast cancer to primary chemotherapy at contrast-enhanced MR imaging: initial clinical results. , 2006, Radiology.

[36]  L. Breiman,et al.  Submodel selection and evaluation in regression. The X-random case , 1992 .

[37]  Charles R. Meyer,et al.  Demonstration of accuracy and clinical versatility of mutual information for automatic multimodality image fusion using affine and thin-plate spline warped geometric deformations , 1997, Medical Image Anal..

[38]  Shigeru Nawano,et al.  Diffusion-weighted imaging of breast cancer with the sensitivity encoding technique: analysis of the apparent diffusion coefficient value. , 2004, Magnetic resonance in medical sciences : MRMS : an official journal of Japan Society of Magnetic Resonance in Medicine.

[39]  Min-Ying Su,et al.  Breast Cancer Patients Undergoing Neoadjuvant AC-Chemotherapy , 2008 .

[40]  Mingxiang Wu,et al.  Association Between Imaging Characteristics and Different Molecular Subtypes of Breast Cancer. , 2017, Academic radiology.

[41]  Christian A. Rees,et al.  Molecular portraits of human breast tumours , 2000, Nature.

[42]  Olav Haraldseth,et al.  Measurement of cell density and necrotic fraction in human melanoma xenografts by diffusion weighted magnetic resonance imaging , 2000, Magnetic resonance in medicine.

[43]  John M S Bartlett,et al.  Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. , 2013, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[44]  Thomas E Yankeelov,et al.  The role of magnetic resonance imaging biomarkers in clinical trials of treatment response in cancer. , 2011, Seminars in oncology.

[45]  R. Kauppinen,et al.  Monitoring thymidine kinase and ganciclovir-induced changes in rat malignant glioma in vivo by nuclear magnetic resonance imaging. , 1998, Cancer gene therapy.

[46]  Benoit M Dawant,et al.  Validation of an algorithm for the nonrigid registration of longitudinal breast MR images using realistic phantoms. , 2010, Medical physics.

[47]  S. Rodenhuis,et al.  Neoadjuvant chemotherapy adaptation and serial MRI response monitoring in ER-positive HER2-negative breast cancer , 2013, British Journal of Cancer.

[48]  N Houssami,et al.  Early prediction of pathologic response to neoadjuvant therapy in breast cancer: systematic review of the accuracy of MRI. , 2012, Breast.

[49]  Xia Li,et al.  Research and applications: Machine learning for predicting the response of breast cancer to neoadjuvant chemotherapy , 2013, J. Am. Medical Informatics Assoc..

[50]  Gianluca Franceschini,et al.  Effect of breast cancer phenotype on diagnostic performance of MRI in the prediction to response to neoadjuvant treatment. , 2014, European journal of radiology.

[51]  Thomas E Yankeelov,et al.  Multiparametric Magnetic Resonance Imaging for Predicting Pathological Response After the First Cycle of Neoadjuvant Chemotherapy in Breast Cancer , 2015, Investigative radiology.

[52]  Benoit M Dawant,et al.  A nonrigid registration algorithm for longitudinal breast MR images and the analysis of breast tumor response. , 2009, Magnetic resonance imaging.

[53]  P J Drew,et al.  Evaluation of response to neoadjuvant chemoradiotherapy for locally advanced breast cancer with dynamic contrast-enhanced MRI of the breast. , 2001, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[54]  Erika Cule,et al.  Ridge Regression in Prediction Problems: Automatic Choice of the Ridge Parameter , 2013, Genetic epidemiology.