Machine learning and radiomics for segmentation and classification of adnexal masses on ultrasound.


Journal

NPJ precision oncology
ISSN: 2397-768X
Titre abrégé: NPJ Precis Oncol
Pays: England
ID NLM: 101708166

Informations de publication

Date de publication:
20 Feb 2024
Historique:
received: 23 05 2023
accepted: 30 01 2024
medline: 21 2 2024
pubmed: 21 2 2024
entrez: 20 2 2024
Statut: epublish

Résumé

Ultrasound-based models exist to support the classification of adnexal masses but are subjective and rely upon ultrasound expertise. We aimed to develop an end-to-end machine learning (ML) model capable of automating the classification of adnexal masses. In this retrospective study, transvaginal ultrasound scan images with linked diagnoses (ultrasound subjective assessment or histology) were extracted and segmented from Imperial College Healthcare, UK (ICH development dataset; n = 577 masses; 1444 images) and Morgagni-Pierantoni Hospital, Italy (MPH external dataset; n = 184 masses; 476 images). A segmentation and classification model was developed using convolutional neural networks and traditional radiomics features. Dice surface coefficient (DICE) was used to measure segmentation performance and area under the ROC curve (AUC), F1-score and recall for classification performance. The ICH and MPH datasets had a median age of 45 (IQR 35-60) and 48 (IQR 38-57) years old and consisted of 23.1% and 31.5% malignant cases, respectively. The best segmentation model achieved a DICE score of 0.85 ± 0.01, 0.88 ± 0.01 and 0.85 ± 0.01 in the ICH training, ICH validation and MPH test sets. The best classification model achieved a recall of 1.00 and F1-score of 0.88 (AUC:0.93), 0.94 (AUC:0.89) and 0.83 (AUC:0.90) in the ICH training, ICH validation and MPH test sets, respectively. We have developed an end-to-end radiomics-based model capable of adnexal mass segmentation and classification, with a comparable predictive performance (AUC 0.90) to the published performance of expert subjective assessment (gold standard), and current risk models. Further prospective evaluation of the classification performance of this ML model against existing methods is required.

Identifiants

pubmed: 38378773
doi: 10.1038/s41698-024-00527-8
pii: 10.1038/s41698-024-00527-8
doi:

Types de publication

Journal Article

Langues

eng

Pagination

41

Subventions

Organisme : RCUK | MRC | Medical Research Foundation
ID : MR/M015858/1

Informations de copyright

© 2024. The Author(s).

Références

Cancer Research UK. Ovarian Cancer Survival Statistics. https://www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/ovarian-cancer/survival .
Buys, S. S. et al. Effect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) cancer screening randomized controlled trial. JAMA 305, 2295–2303 (2011).
pubmed: 21642681 doi: 10.1001/jama.2011.766
Jacobs, I. J. et al. Ovarian cancer screening and mortality in the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS): a randomised controlled trial. Lancet 387, 945–956 (2016).
pubmed: 26707054 pmcid: 4779792 doi: 10.1016/S0140-6736(15)01224-6
McDonald, J. M. & Modesitt, S. C. The incidental postmenopausal adnexal mass. Clin. Obstet. Gynecol. 49, 506–516 (2006).
pubmed: 16885657 doi: 10.1097/00003081-200609000-00010
Froyman, W. et al. Risk of complications in patients with conservatively managed ovarian tumours (IOTA5): a 2-year interim analysis of a multicentre, prospective, cohort study. Lancet Oncol. 20, 448–458 (2019).
pubmed: 30737137 doi: 10.1016/S1470-2045(18)30837-4
Meys, E. M. J. et al. Subjective assessment versus ultrasound models to diagnose ovarian cancer: a systematic review and meta-analysis. Eur. J. Cancer 58, 17–29 (2016).
pubmed: 26922169 doi: 10.1016/j.ejca.2016.01.007
Jacobs, I. et al. A risk of malignancy index incorporating CA 125, ultrasound and menopausal status for the accurate preoperative diagnosis of ovarian cancer. Br. J. Obstet. Gynaecol. 97, 922–929 (1990).
pubmed: 2223684 doi: 10.1111/j.1471-0528.1990.tb02448.x
Timmerman, D. et al. Simple ultrasound-based rules for the diagnosis of ovarian cancer. Ultrasound Obstet. Gynecol. 31, 681–690 (2008).
pubmed: 18504770 doi: 10.1002/uog.5365
Van Calster, B. et al. Evaluating the risk of ovarian cancer before surgery using the ADNEX model to differentiate between benign, borderline, early and advanced stage invasive, and secondary metastatic tumours: prospective multicentre diagnostic study. BMJ 349, g5920 (2014).
pubmed: 25320247 pmcid: 4198550 doi: 10.1136/bmj.g5920
Andreotti, R. F. et al. Ovarian-adnexal reporting lexicon for ultrasound: a white paper of the ACR ovarian-adnexal reporting and data system committee. J. Am. Coll. Radiol. 15, 1415–1429 (2018).
pubmed: 30149950 doi: 10.1016/j.jacr.2018.07.004
Meys, E. M. J. et al. Estimating risk of malignancy in adnexal masses: external validation of the ADNEX model and comparison with other frequently used ultrasound methods. Ultrasound Obstet. Gynecol. 49, 784–792 (2017).
pubmed: 27514486 pmcid: 5488216 doi: 10.1002/uog.17225
Van Calster, B. et al. Validation of models to diagnose ovarian cancer in patients managed surgically or conservatively: multicentre cohort study. BMJ m2614 https://doi.org/10.1136/bmj.m2614 (2020).
Sayasneh, A. et al. A multicenter prospective external validation of the diagnostic performance of IOTA simple descriptors and rules to characterize ovarian masses. Gynecol. Oncol. 130, 140–146 (2013).
pubmed: 23578539 doi: 10.1016/j.ygyno.2013.04.003
LeCun, Y., Bengio, Y. & Hinton, G. Deep learning. Nature 521, 436–444 (2015).
doi: 10.1038/nature14539 pubmed: 26017442
Lambin, P. et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur. J. Cancer 48, 441–446 (2012).
pubmed: 22257792 pmcid: 4533986 doi: 10.1016/j.ejca.2011.11.036
Nougaret, S. et al. Radiomics and radiogenomics in ovarian cancer: a literature review. Abdom. Radiol. N.Y. 46, 2308–2322 (2021).
doi: 10.1007/s00261-020-02820-z
Xu, H.-L. et al. Artificial intelligence performance in image-based ovarian cancer identification: a systematic review and meta-analysis. eClinicalMedicine 53, 101662 (2022).
pubmed: 36147628 pmcid: 9486055 doi: 10.1016/j.eclinm.2022.101662
Christiansen, F. et al. Ultrasound image analysis using deep neural networks for discriminating between benign and malignant ovarian tumors: comparison with expert subjective assessment. Ultrasound Obstet. Gynecol. 57, 155–163 (2021).
pubmed: 33142359 pmcid: 7839489 doi: 10.1002/uog.23530
Gao, Y. et al. Deep learning-enabled pelvic ultrasound images for accurate diagnosis of ovarian cancer in China: a retrospective, multicentre, diagnostic study. Lancet Digit. Health 4, e179–e187 (2022).
pubmed: 35216752 doi: 10.1016/S2589-7500(21)00278-8
Guo, X. & Zhao, G. Establishment and verification of logistic regression model for qualitative diagnosis of ovarian cancer based on MRI and ultrasound signs. Comput. Math. Methods Med. 2022, 1–8 (2022).
Wang, H. et al. Application of deep convolutional neural networks for discriminating benign, borderline, and malignant serous ovarian tumors from ultrasound images. Front. Oncol. 11, 770683 (2021).
pubmed: 34988015 pmcid: 8720926 doi: 10.3389/fonc.2021.770683
Acharya, U. R. et al. Ovarian tumor characterization and classification using ultrasound—a new online paradigm. J. Digit. Imaging 26, 544–553 (2013).
pubmed: 23160866 doi: 10.1007/s10278-012-9553-8
Acharya, U. R. et al. GyneScan: an improved online paradigm for screening of ovarian cancer via tissue characterization. Technol. Cancer Res. Treat. 13, 529–539 (2014).
pubmed: 24325128 doi: 10.7785/tcrtexpress.2013.600273
Pathak, H. & Kulkarni, V. Identification of ovarian mass through ultrasound images using machine learning techniques. In Proc. IEEE International Conference on Research in Computational Intelligence and Communication Networks (ICRCICN) 137–140 (IEEE, 2015). https://doi.org/10.1109/ICRCICN.2015.7434224 .
Chiappa, V. et al. The Adoption of Radiomics and machine learning improves the diagnostic processes of women with Ovarian MAsses (the AROMA pilot study). J. Ultrasound 24, 429–437 (2021).
pubmed: 32696414 doi: 10.1007/s40477-020-00503-5
Mol, B. W. J. et al. Distinguishing the benign and malignant adnexal mass: an external validation of prognostic models. Gynecol. Oncol. 80, 162–167 (2001).
pubmed: 11161854 doi: 10.1006/gyno.2000.6052
Li, J. et al. A Deep Learning model system for diagnosis and management of adnexal masses. Cancers 14, 5291 (2022).
pubmed: 36358710 pmcid: 9659123 doi: 10.3390/cancers14215291
Al-karawi, D. et al. An evaluation of the effectiveness of image-based texture features extracted from static B-mode ultrasound images in distinguishing between benign and malignant ovarian masses. Ultrason. Imaging 43, 124–138 (2021).
pubmed: 33629652 doi: 10.1177/0161734621998091
Lu, H. et al. A mathematical-descriptor of tumor-mesoscopic-structure from computed-tomography images annotates prognostic- and molecular-phenotypes of epithelial ovarian cancer. Nat. Commun. 10, 764 (2019).
pubmed: 30770825 pmcid: 6377605 doi: 10.1038/s41467-019-08718-9
Fotopoulou, C. et al. Validation analysis of the novel imaging-based prognostic radiomic signature in patients undergoing primary surgery for advanced high-grade serous ovarian cancer (HGSOC). Br. J. Cancer 126, 1047–1054 (2022).
pubmed: 34923575 doi: 10.1038/s41416-021-01662-w
Qi, L. et al. Diagnosis of ovarian neoplasms using nomogram in combination with ultrasound image-based radiomics signature and clinical factors. Front. Genet. 12, 753948 (2021).
pubmed: 34650603 pmcid: 8505695 doi: 10.3389/fgene.2021.753948
P-331 Differentiating subcentimeter lung metastases in colorectal cancer patients by radiomics and deep learning approaches: a multicenter study—Google Search. https://www.google.com/search?client=firefox-b-d&q=P-331+Differentiating+subcentimeter+lung+metastases+in+colorectal+cancer+patients+by+radiomics+and+deep+learning+approaches%3A+A+multicenter+study .
Chen, Y. et al. Deep learning radiomics of preoperative breast MRI for prediction of axillary lymph node metastasis in breast cancer. J. Digit. Imaging 1–9 https://doi.org/10.1007/s10278-023-00818-9 (2023).
Laqua, F. C. et al. Transfer-learning deep radiomics and hand-crafted radiomics for classifying lymph nodes from contrast-enhanced computed tomography in lung cancer. Cancers 15, 2850 (2023).
pubmed: 37345187 pmcid: 10216416 doi: 10.3390/cancers15102850
Quan, M.-Y. et al. Deep learning radiomics model based on breast ultrasound video to predict HER2 expression status. Front. Endocrinol. 14, 1144812 (2023).
doi: 10.3389/fendo.2023.1144812
Hunter, B. et al. A radiomics-based decision support tool improves lung cancer diagnosis in combination with the Herder score in large lung nodules. eBioMedicine 86, 104344 (2022).
pubmed: 36370635 pmcid: 9664396 doi: 10.1016/j.ebiom.2022.104344
Timmerman, D. et al. Terms, definitions and measurements to describe the sonographic features of adnexal tumors: a consensus opinion from the International Ovarian Tumor Analysis (IOTA) Group. Ultrasound Obstet. Gynecol. 16, 500–505 (2000).
pubmed: 11169340 doi: 10.1046/j.1469-0705.2000.00287.x
Meinhold-Heerlein, I. et al. Statement by the Kommission Ovar of the AGO: the new FIGO and WHO classifications of ovarian, fallopian tube and primary peritoneal cancer. Geburtshilfe Frauenheilkd. 75, 1021–1027 (2015).
pubmed: 26556905 pmcid: 4629993 doi: 10.1055/s-0035-1558079
Fedorov, A. et al. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn. Reson. Imaging 30, 1323–1341 (2012).
pubmed: 22770690 pmcid: 3466397 doi: 10.1016/j.mri.2012.05.001
European Federation of Societies for Ultrasound in Medicine and Biology. Ultraschall Med. Eur. J. Ultrasound 27, 79–95 (2006).
Zwanenburg, A., Leger, S., Vallières, M. & Löck, S. Image biomarker standardisation initiative. arXiv e-prints https://ui.adsabs.harvard.edu/abs/2016arXiv161207003Z https://doi.org/10.48550/arXiv.1612.07003 (2016).
Lambin, P. et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat. Rev. Clin. Oncol. 14, 749–762 (2017).
pubmed: 28975929 doi: 10.1038/nrclinonc.2017.141
Qin, G. & Hotilovac, L. Comparison of non-parametric confidence intervals for the area under the ROC curve of a continuous-scale diagnostic test. Stat. Methods Med. Res. 17, 207–221 (2008).
doi: 10.1177/0962280207087173
Friedman, J., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010).
pubmed: 20808728 pmcid: 2929880 doi: 10.18637/jss.v033.i01
Guyon, I. & Elisseeff, A. An introduction to variable and feature selection. J. Mach. Learn. Res. 3, 1157–1182 (2003).
Cortes, C. & Vapnik, V. Support-vector networks. Mach. Learn. 20, 273–297 (1995).
doi: 10.1007/BF00994018
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300 (1995).
Guyon, I., Weston, J., Barnhill, S. & Vapnik, V. Gene selection for cancer classification using support vector machines. Mach. Learn. 46, 389–422 (2002).
doi: 10.1023/A:1012487302797
Kraskov, A., Stögbauer, H. & Grassberger, P. Estimating mutual information. Phys. Rev. E 69, 066138 (2004).
doi: 10.1103/PhysRevE.69.066138
Kursa, M. B. & Rudnicki, W. R. Feature Selection with the Boruta Package. J. Stat. Soft. 36, 1–13 (2010).
doi: 10.18637/jss.v036.i11
Hastie, T., Tibshirani, R. & Friedman, J. The Elements of Statistical Learning. (Springer, 2009). https://doi.org/10.1007/978-0-387-84858-7 .
Cover, T. & Hart, P. Nearest neighbor pattern classification. IEEE Trans. Inf. Theory 13, 21–27 (1967).
doi: 10.1109/TIT.1967.1053964
Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001).
doi: 10.1023/A:1010933404324
Chen, T. & Guestrin, C. XGBoost: a scalable tree boosting system. 785–794. https://doi.org/10.1145/2939672.2939785 (2016).
The Collinearity Problem in Linear Regression. The Partial Least Squares (PLS) approach to generalized inverses. SIAM J. Sci. Comput. https://epubs.siam.org/doi/10.1137/0905052 .
Pattern Recognition and Neural Networks. https://www.stats.ox.ac.uk/~ripley/PRbook/ .
Domingos, P. & Pazzani, M. On the optimality of the simple Bayesian classifier under zero-one loss. Mach. Learn. 29, 103–130 (1997).
doi: 10.1023/A:1007413511361

Auteurs

Jennifer F Barcroft (JF)

Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.

Kristofer Linton-Reid (K)

Department of Surgery and Cancer, Imperial College London, London, UK.

Chiara Landolfo (C)

Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.

Maya Al-Memar (M)

Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.

Nina Parker (N)

Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.

Chris Kyriacou (C)

Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.

Maria Munaretto (M)

Department of Obstetrics and Gynaecology, Ospedale Morgagni-Pierantoni, Forli, Italy.

Martina Fantauzzi (M)

Department of Medicine and Surgery, University of Milan-Bicocca, Milan, Italy.

Nina Cooper (N)

Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.

Joseph Yazbek (J)

Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.

Nishat Bharwani (N)

Department of Radiology, Imperial College Healthcare NHS Trust, London, UK.

Sa Ra Lee (SR)

Department of Obstetrics and Gynaecology, Asan Medical Center, Seoul, South Korea.

Ju Hee Kim (JH)

Department of Obstetrics and Gynaecology, Asan Medical Center, Seoul, South Korea.

Dirk Timmerman (D)

Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
Department of Obstetrics and Gynecology, University Hospitals Leuven, Leuven, Belgium.
Department of Development and Regeneration, KU Leuven, Leuven, Belgium.

Joram Posma (J)

Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.

Luca Savelli (L)

Department of Obstetrics and Gynaecology, Ospedale Morgagni-Pierantoni, Forli, Italy.

Srdjan Saso (S)

Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.
Department of Surgery and Cancer, Imperial College London, London, UK.

Eric O Aboagye (EO)

Department of Surgery and Cancer, Imperial College London, London, UK. eric.aboagye@imperial.ac.uk.

Tom Bourne (T)

Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
Department of Obstetrics and Gynaecology, Imperial College Healthcare NHS Trust, London, UK.
Department of Development and Regeneration, KU Leuven, Leuven, Belgium.

Classifications MeSH