Early prediction of neoadjuvant chemotherapy response by exploiting a transfer learning approach on breast DCE-MRIs.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
08 07 2021
Historique:
received: 06 05 2021
accepted: 28 06 2021
entrez: 9 7 2021
pubmed: 10 7 2021
medline: 9 11 2021
Statut: epublish

Résumé

The dynamic contrast-enhanced MR imaging plays a crucial role in evaluating the effectiveness of neoadjuvant chemotherapy (NAC) even since its early stage through the prediction of the final pathological complete response (pCR). In this study, we proposed a transfer learning approach to predict if a patient achieved pCR (pCR) or did not (non-pCR) by exploiting, separately or in combination, pre-treatment and early-treatment exams from I-SPY1 TRIAL public database. First, low-level features, i.e., related to local structure of the image, were automatically extracted by a pre-trained convolutional neural network (CNN) overcoming manual feature extraction. Next, an optimal set of most stable features was detected and then used to design an SVM classifier. A first subset of patients, called fine-tuning dataset (30 pCR; 78 non-pCR), was used to perform the optimal choice of features. A second subset not involved in the feature selection process was employed as an independent test (7 pCR; 19 non-pCR) to validate the model. By combining the optimal features extracted from both pre-treatment and early-treatment exams with some clinical features, i.e., ER, PgR, HER2 and molecular subtype, an accuracy of 91.4% and 92.3%, and an AUC value of 0.93 and 0.90, were returned on the fine-tuning dataset and the independent test, respectively. Overall, the low-level CNN features have an important role in the early evaluation of the NAC efficacy by predicting pCR. The proposed model represents a first effort towards the development of a clinical support tool for an early prediction of pCR to NAC.

Identifiants

pubmed: 34238968
doi: 10.1038/s41598-021-93592-z
pii: 10.1038/s41598-021-93592-z
pmc: PMC8266861
doi:

Substances chimiques

Receptors, Estrogen 0
Receptors, Progesterone 0
ERBB2 protein, human EC 2.7.10.1
Receptor, ErbB-2 EC 2.7.10.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

14123

Références

Eun, N. L. et al. Texture analysis with 3.0-T MRI for association of response to neoadjuvant chemotherapy in breast cancer. Radiology 294, 31–41 (2020).
pubmed: 31769740 doi: 10.1148/radiol.2019182718
Cain, H. et al. Neoadjuvant therapy in early breast cancer: treatment considerations and common debates in practice. Clin. Oncol. 29, 642–652 (2017).
doi: 10.1016/j.clon.2017.06.003
Rustin, G. J. S. et al. Re: New guidelines to evaluate the response to treatment in solid tumors (Ovarian Cancer) [2]. J. Natl. Cancer Inst. 96, 487–488 (2004).
pubmed: 15026475 doi: 10.1093/jnci/djh081
Eisenhauer, E. A. et al. New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1.1). Eur. J. Cancer 45, 228–247 (2009).
pubmed: 19097774 doi: 10.1016/j.ejca.2008.10.026
Caudle, A. S. et al. Impact of progression during neoadjuvant chemotherapy on surgical management of breast cancer. Ann. Surg. Oncol. 18, 932–938 (2011).
pubmed: 21061075 pmcid: 4347926 doi: 10.1245/s10434-010-1390-8
Cho, J. H. et al. Oncologic safety of breast-conserving surgery compared to mastectomy in patients receiving neoadjuvant chemotherapy for locally advanced breast cancer. J. Surg. Oncol. 108, 531–536 (2013).
pubmed: 24115142 doi: 10.1002/jso.23439
Hylton, N. M. et al. Locally advanced breast cancer: MR imaging for prediction of response to neoadjuvant chemotherapy - Results from ACRIN 6657/I-SPY TRIAL. Radiology 263, 663–672 (2012).
pubmed: 22623692 pmcid: 3359517 doi: 10.1148/radiol.12110748
Loo, C. E. et al. Magnetic resonance imaging response monitoring of breast cancer during neoadjuvant chemotherapy: Relevance of Breast Cancer Subtype. J. Clin. Oncol. 29, 660–666 (2011).
pubmed: 21220595 doi: 10.1200/JCO.2010.31.1258
Marinovich, M. L. et al. Early prediction of pathologic response to neoadjuvant therapy in breast cancer: Systematic review of the accuracy of MRI. Breast 21, 669–677 (2012).
pubmed: 22863284 doi: 10.1016/j.breast.2012.07.006
Scheel, J. R. et al. MRI, clinical examination, and mammography for preoperative assessment of residual disease and pathologic complete response after neoadjuvant chemotherapy for breast cancer: ACRIN 6657 trial. Am. J. Roentgenol. 210, 1376–1385 (2018).
doi: 10.2214/AJR.17.18323
Su, M. Y. L. Breast cancer: Early prediction of response to neoadjuvant chemotherapy using parametric response maps for MR imaging: Cho N, im S-A, Park I-A, et al (Seoul Natl Univ College of Medicine, Republic of Korea) Radiology 272:385–396, 2014. Breast Dis. 26, 134–137 (2015).
Li, X. et al. Multiparametric magnetic resonance imaging for predicting pathological response after the first cycle of neoadjuvant chemotherapy in breast cancer. Invest. Radiol. 50, 195–204 (2015).
pubmed: 25360603 pmcid: 4471951 doi: 10.1097/RLI.0000000000000100
Fangberget, A. et al. Neoadjuvant chemotherapy in breast cancer-response evaluation and prediction of response to treatment using dynamic contrast-enhanced and diffusion-weighted MR imaging. Eur. Radiol. 21, 1188–1199 (2011).
pubmed: 21127880 doi: 10.1007/s00330-010-2020-3
Sharma, U., Danishad, K. K. A., Seenu, V. & Jagannathan, N. R. Longitudinal study of the assessment by MRI and diffusion-weighted imaging of tumor response in patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy. NMR Biomed. 22, 104–113 (2009).
pubmed: 18384182 doi: 10.1002/nbm.1245
Beresford, M. J. et al. Inter- and intraobserver variability in the evaluation of dynamic breast cancer MRI. J. Magn. Reson. Imaging 24, 1316–1325 (2006).
pubmed: 17058203 doi: 10.1002/jmri.20768
Bellotti, R. et al. The MAGIC-5 project: Medical applications on a grid infrastructure connection. IEEE Nucl. Sci. Symp. Conf. Rec. 3, 1902–1906 (2004).
Losurdo, L. et al. Radiomics analysis on contrast-enhanced spectral mammography images for breast cancer diagnosis: A pilot study. Entropy 21, 1110 (2019).
pmcid: 7514454 doi: 10.3390/e21111110
Fanizzi, A. et al. Ensemble discretewavelet transform and gray-level co-occurrence matrix for microcalcification cluster classification in digital mammography. Appl. Sci. 9, 1–14 (2019).
doi: 10.3390/app9245388
Fanizzi, A. et al. Hough transform for clustered microcalcifications detection in full-field digital mammograms. Appl. Digit. Image Process. XL 10396, 1039616 (2017).
Braman, N. M. et al. Intratumoral and peritumoral radiomics for the pretreatment prediction of pathological complete response to neoadjuvant chemotherapy based on breast DCE-MRI. Breast Cancer Res. 19, 1–14 (2017).
Jahani, N. et al. Prediction of treatment response to neoadjuvant chemotherapy for breast cancer via early changes in tumor heterogeneity captured by DCE-MRI registration. Sci. Rep. 9, 1–12 (2019).
doi: 10.1038/s41598-019-48465-x
Tahmassebi, A. et al. Impact of machine learning with multiparametric magnetic resonance imaging of the breast for early prediction of response to neoadjuvant chemotherapy and survival outcomes in breast cancer patients. Invest. Radiol. 54, 110–117 (2019).
pubmed: 30358693 pmcid: 6310100 doi: 10.1097/RLI.0000000000000518
Lo Gullo, R., Eskreis-Winkler, S., Morris, E. A. & Pinker, K. Machine learning with multiparametric magnetic resonance imaging of the breast for early prediction of response to neoadjuvant chemotherapy. Breast 49, 115–122 (2020).
pubmed: 31786416 doi: 10.1016/j.breast.2019.11.009
Arasu, V. A. et al. Population-based assessment of the association between magnetic resonance imaging background parenchymal enhancement and future primary breast cancer risk. J. Clin. Oncol. 37, 954–963 (2019).
pubmed: 30625040 pmcid: 6494266 doi: 10.1200/JCO.18.00378
Forgia, D. La et al. Response predictivity to neoadjuvant therapies in breast cancer: A qualitative analysis of background parenchymal enhancement in DCE-MRI, Journal of Personalized Medicine, 11, 256 (2021).
LeCun, Y., Bengio, Y. & Hinton, G. Deep learning. Nature 521, 436–444 (2015).
pubmed: 26017442 doi: 10.1038/nature14539
Panigrahi, S., Nanda, A. & Swarnkar, T. A survey on transfer learning. IEEE Trans. Knowl. Data Eng. 22, 1345–1359 (2009).
Wang, Z. et al. Breast cancer detection using extreme learning machine based on feature fusion with CNN deep features. IEEE Access 7, 105146–105158 (2019).
doi: 10.1109/ACCESS.2019.2892795
Yu, S. D., Liu, L. L., Wang, Z. Y., Dai, G. Z. & Xie, Y. Q. Transferring deep neural networks for the differentiation of mammographic breast lesions. Sci. China Technol. Sci. 62, 441–447 (2019).
doi: 10.1007/s11431-017-9317-3
Huynh, B. Q., Antropova, N. & Giger, M. L. Comparison of breast DCE-MRI contrast time points for predicting response to neoadjuvant chemotherapy using deep convolutional neural network features with transfer learning. Med. Imaging 2017 Comput. Diagnosis 10134, 101340U (2017).
Ha, R. et al. Prior to initiation of chemotherapy, can we predict breast tumor response? Deep learning convolutional neural networks approach using a breast MRI tumor dataset. J. Digit. Imaging 32, 693–701 (2019).
pubmed: 30361936 doi: 10.1007/s10278-018-0144-1
Liu, M. Z. et al. A novel CNN algorithm for pathological complete response prediction using an I-SPY TRIAL breast MRI database. Magn. Reson. Imaging 73, 148–151 (2020).
pubmed: 32889091 pmcid: 8111786 doi: 10.1016/j.mri.2020.08.021
Ravichandran, K., Braman, N., Janowczyk, A. & Madabhushi, A. A deep learning classifier for prediction of pathological complete response to neoadjuvant chemotherapy from baseline breast DCE-MRI. 11 (2018). https://doi.org/10.1117/12.2294056
El Adoui, M., Drisis, S. & Benjelloun, M. Multi-input deep learning architecture for predicting breast tumor response to chemotherapy using quantitative MR images. Int. J. Comput. Assist. Radiol. Surg. 15, 1491–1500 (2020).
pubmed: 32556920 doi: 10.1007/s11548-020-02209-9
Newitt, D. & Hylton, N. Multi-center breast DCE-MRI data and segmentations from patients in the I-SPY 1/ACRIN 6657 trials. Cancer Imaging Arch. 10, 7 (2016).
Hylton, N. M. et al. Neoadjuvant chemotherapy for breast cancer: Functional tumor volume by MR imaging predicts recurrencefree survival-results from the ACRIN 6657/CALGB 150007 I-SPY 1 TRIAL. Radiology 279, 44–55 (2016).
pubmed: 26624971 doi: 10.1148/radiol.2015150013
Clark, K. et al. The cancer imaging archive (TCIA): Maintaining and operating a public information repository. J. Digit. Imaging 26, 1045–1057 (2013).
pubmed: 23884657 pmcid: 3824915 doi: 10.1007/s10278-013-9622-7
Russakovsky, O. et al. ImageNet Large Scale Visual Recognition Challenge. Int. J. Comput. Vis. 115, 211–252 (2015).
doi: 10.1007/s11263-015-0816-y
Ding, Y. et al. Does dose-dense neoadjuvant chemotherapy have clinically significant prognostic value in breast cancer?: A meta-analysis of 3,724 patients. PLoS ONE 15, 1–12 (2020).
doi: 10.1371/journal.pone.0234058
Korde, L. A. et al. Neoadjuvant chemotherapy, endocrine therapy, and targeted therapy for breast cancer: ASCO guideline. J. Clin. Oncol. https://doi.org/10.1200/jco.20.03399 (2021).
doi: 10.1200/jco.20.03399 pubmed: 34324367 pmcid: 8274745
Burges, C. J. A Tutorial on Support Vector Machines for Pattern Recognition. Data Min. Knowl. Discov. 2, 121–167 (1998).
doi: 10.1023/A:1009715923555
Casti, P. et al. Calibration of vision-based measurement of pain intensity with multiple expert observers. IEEE Trans. Instrum. Meas. 68, 2442–2450 (2019).
doi: 10.1109/TIM.2019.2909603
Mencattini, A. et al. Discovering the hidden messages within cell trajectories using a deep learning approach for in vitro evaluation of cancer drug treatments. Sci. Rep. 10, 1–11 (2020).
doi: 10.1038/s41598-020-64246-3
Salakhutdinov, R., Tenenbaum, J. B. & Torralba, A. Learning with Hierarchical-Deep Models. IEEE Trans. Pattern Anal. Mach. Intell. 35, 1958–1971 (2013).
pubmed: 23787346 doi: 10.1109/TPAMI.2012.269
Zheng, L., Zhao, Y., Wang, S., Wang, J. & Tian, Q. Good Practice in CNN Feature Transfer. arXiv Prepr. arXiv:1604.00133 . (2016).
Mann, H. B. & Whitney, D. R. On a test of whether one of two random variables is stochastically larger larger than the other. Ann. Math. Stat. 18, 50–60 (1947).
doi: 10.1214/aoms/1177730491
Nogueira, S., Sechidis, K. & Brown, G. On the stability of feature selection algorithms. J. Mach. Learn. Res. 18, 1–54 (2018).
Kalousis, A., Prados, J. & Hilario, M. Stability of feature selection algorithms: A study on high-dimensional spaces. Knowl. Inf. Syst. 12, 95–116 (2007).
doi: 10.1007/s10115-006-0040-8
Youden, W. J. Index for rating diagnostic tests. Cancer 3, 32–35 (1950).
doi: 10.1002/1097-0142(1950)3:1<32::AID-CNCR2820030106>3.0.CO;2-3 pubmed: 15405679

Auteurs

Maria Colomba Comes (MC)

Struttura Semplice Dipartimentale di Fisica Sanitaria, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Annarita Fanizzi (A)

Struttura Semplice Dipartimentale di Fisica Sanitaria, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy. a.fanizzi@oncologico.bari.it.

Samantha Bove (S)

Dipartimento di Matematica, Università Degli Studi di Bari, 70121, Bari, Italy.

Vittorio Didonna (V)

Struttura Semplice Dipartimentale di Fisica Sanitaria, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Sergio Diotaiuti (S)

Struttura Semplice Dipartimentale di Chirurgia, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Daniele La Forgia (D)

Struttura Semplice Dipartimentale di Radiologia Senologica, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Agnese Latorre (A)

Unità Operativa Complessa di Oncologia Medica, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Eugenio Martinelli (E)

Interdisciplinary Center for Advanced Studies on Lab-on-Chip and Organ-on-Chip Applications (ICLOC), University of Rome Tor Vergata, 00133, Rome, Italy.
Dipartimento di Ingegneria Elettronica, Università di Roma Tor Vergata, Via del politecnico 1, 00133, Rome, Italy.

Arianna Mencattini (A)

Interdisciplinary Center for Advanced Studies on Lab-on-Chip and Organ-on-Chip Applications (ICLOC), University of Rome Tor Vergata, 00133, Rome, Italy.
Dipartimento di Ingegneria Elettronica, Università di Roma Tor Vergata, Via del politecnico 1, 00133, Rome, Italy.

Annalisa Nardone (A)

Unita Opertiva Complessa di Radioterapia, IRCCS Istituto Tumori "Giovanni Paolo II", 70124, Bari, Italy.

Angelo Virgilio Paradiso (AV)

Oncologia Sperimentale e Biobanca, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Cosmo Maurizio Ressa (CM)

Unità Operativa Complessa di Chirurgica Plastica e Ricostruttiva, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Pasquale Tamborra (P)

Struttura Semplice Dipartimentale di Fisica Sanitaria, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Vito Lorusso (V)

Unità Operativa Complessa di Oncologia Medica, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Raffaella Massafra (R)

Struttura Semplice Dipartimentale di Fisica Sanitaria, I.R.C.C.S. Istituto Tumori "Giovanni Paolo II", Viale Orazio Flacco 65, 70124, Bari, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH