Abstract
Purpose
More than 80% of patients with ovarian epithelial cancer (OEC) show complete remission after initial treatment but eventually experience recurrence of the disease. This study aimed to develop a radiomics signature to identify a new prognostic indicator based on preoperative ultrasound imaging.
Methods
A total of 111 patients with OEC who underwent transvaginal ultrasound before surgery were included. Of these, 76 were divided into the training cohort and 35 into the test cohort. We defined the region of interest (ROI) of the tumor by manually drawing the tumor contour on the ultrasound image of the lesion. The radiomics features were extracted from ultrasound images. The radiomics score (Rad-Score) was constructed using the least absolute shrinkage and selection operator (LASSO) analysis and Cox regression. Combined with the ultrasound radiomics features, significant clinical variables were also used to establish predictive models for 5-year progression-free survival (PFS) prediction. The efficiency of the model was evaluated using the area under the curve (AUC). Kaplan–Meier analysis was used to evaluate the association between the Rad-Score and PFS.
Results
The combined model was superior to the clinical and Rad-Score models in estimating 5-year PFS and achieved an AUC of 0.868 (95%CI 0.766–0.971) in the training cohort. The Rad-Score was negatively correlated with prognosis in the training and test cohorts.
Conclusions
The combined model that incorporated both clinical parameters and ultrasound radiomics features achieved a good prognosis in patients with OEC, which might aid clinical decision-making.
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Abbreviations
- AUC:
-
Area under the curve
- CI:
-
Confidence interval
- CT:
-
Computed tomography
- GLCM:
-
Gray-level co-occurrence matrix
- GLRLM:
-
Gray-level run-length matrix
- GLSZM:
-
Gray-level size zone matrix
- LASSO:
-
Least absolute shrinkage and selection operator
- MRI:
-
Magnetic resonance imaging
- OC:
-
Ovarian cancer
- OEC:
-
Ovarian epithelial cancer
- PFS:
-
Progression-free survival
- Rad-Score:
-
Radiomics score
- ROC:
-
Receiver-operating characteristic
- ROI:
-
Region of interest
- TC:
-
Serum total cholesterol
- WBC:
-
White blood cells
References
R.L. Siegel, K.D. Miller, A. Jemal, Cancer statistics, 2019, CA Cancer J Clin 69(1) (2019) 7-34.
W. Chen, R. Zheng, P.D. Baade, S. Zhang, H. Zeng, F. Bray, A. Jemal, X.Q. Yu, J. He, Cancer statistics in China, 2015, CA Cancer J Clin 66(2) (2016) 115-32.
L.A. Torre, B. Trabert, C.E. DeSantis, K.D. Miller, G. Samimi, C.D. Runowicz, M.M. Gaudet, A. Jemal, R.L. Siegel, Ovarian cancer statistics, 2018, CA Cancer J Clin 68(4) (2018) 284-296.
S.A. Cannistra, Cancer of the ovary, N Engl J Med 351(24) (2004) 2519-29.
D.D. Bowtell, S. Bohm, A.A. Ahmed, P.J. Aspuria, R.C. Bast, Jr., V. Beral, J.S. Berek, M.J. Birrer, S. Blagden, M.A. Bookman, J.D. Brenton, K.B. Chiappinelli, F.C. Martins, G. Coukos, R. Drapkin, R. Edmondson, C. Fotopoulou, H. Gabra, J. Galon, C. Gourley, V. Heong, D.G. Huntsman, M. Iwanicki, B.Y. Karlan, A. Kaye, E. Lengyel, D.A. Levine, K.H. Lu, I.A. McNeish, U. Menon, S.A. Narod, B.H. Nelson, K.P. Nephew, P. Pharoah, D.J. Powell, Jr., P. Ramos, I.L. Romero, C.L. Scott, A.K. Sood, E.A. Stronach, F.R. Balkwill, Rethinking ovarian cancer II: reducing mortality from high-grade serous ovarian cancer, Nat Rev Cancer 15(11) (2015) 668-79.
R.E. Bristow, R.S. Tomacruz, D.K. Armstrong, E.L. Trimble, F.J. Montz, Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis, J Clin Oncol 20(5) (2002) 1248-59.
D.S. Chi, C.C. Franklin, D.A. Levine, F. Akselrod, P. Sabbatini, W.R. Jarnagin, R. DeMatteo, E.A. Poynor, N.R. Abu-Rustum, R.R. Barakat, Improved optimal cytoreduction rates for stages IIIC and IV epithelial ovarian, fallopian tube, and primary peritoneal cancer: a change in surgical approach, Gynecol Oncol 94(3) (2004) 650-4.
P. Wimberger, M. Wehling, N. Lehmann, R. Kimmig, B. Schmalfeldt, A. Burges, P. Harter, J. Pfisterer, A. du Bois, Influence of residual tumor on outcome in ovarian cancer patients with FIGO stage IV disease: an exploratory analysis of the AGO-OVAR (Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group), Ann Surg Oncol 17(6) (2010) 1642-8.
H.J. Aerts, E.R. Velazquez, R.T. Leijenaar, C. Parmar, P. Grossmann, S. Carvalho, J. Bussink, R. Monshouwer, B. Haibe-Kains, D. Rietveld, F. Hoebers, M.M. Rietbergen, C.R. Leemans, A. Dekker, J. Quackenbush, R.J. Gillies, P. Lambin, Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach, Nat Commun 5 (2014) 4006.
H.J. Aerts, The Potential of Radiomic-Based Phenotyping in Precision Medicine: A Review, JAMA Oncol 2(12) (2016) 1636-1642.
M. Kirienko, L. Cozzi, L. Antunovic, L. Lozza, A. Fogliata, E. Voulaz, A. Rossi, A. Chiti, M. Sollini, Prediction of disease-free survival by the PET/CT radiomic signature in non-small cell lung cancer patients undergoing surgery, Eur J Nucl Med Mol Imaging 45(2) (2018) 207-217.
S. Rizzo, F. Botta, S. Raimondi, D. Origgi, V. Buscarino, A. Colarieti, F. Tomao, G. Aletti, V. Zanagnolo, M. Del Grande, N. Colombo, M. Bellomi, Radiomics of high-grade serous ovarian cancer: association between quantitative CT features, residual tumour and disease progression within 12 months, Eur Radiol 28(11) (2018) 4849-4859.
W. Wei, Z. Liu, Y. Rong, B. Zhou, Y. Bai, W. Wei, S. Wang, M. Wang, Y. Guo, J. Tian, A Computed Tomography-Based Radiomic Prognostic Marker of Advanced High-Grade Serous Ovarian Cancer Recurrence: A Multicenter Study, Front Oncol 9 (2019) 255.
S. Wang, Z. Liu, Y. Rong, B. Zhou, Y. Bai, W. Wei, W. Wei, M. Wang, Y. Guo, J. Tian, Deep learning provides a new computed tomography-based prognostic biomarker for recurrence prediction in high-grade serous ovarian cancer, Radiother Oncol 132 (2019) 171-177.
H. Lu, M. Arshad, A. Thornton, G. Avesani, P. Cunnea, E. Curry, F. Kanavati, J. Liang, K. Nixon, S.T. Williams, M.A. Hassan, D.D.L. Bowtell, H. Gabra, C. Fotopoulou, A. Rockall, E.O. Aboagye, A mathematical-descriptor of tumor-mesoscopic-structure from computed-tomography images annotates prognostic- and molecular-phenotypes of epithelial ovarian cancer, Nat Commun 10(1) (2019) 764.
H. Zhang, Y. Mao, X. Chen, G. Wu, X. Liu, P. Zhang, Y. Bai, P. Lu, W. Yao, Y. Wang, J. Yu, G. Zhang, Magnetic resonance imaging radiomics in categorizing ovarian masses and predicting clinical outcome: a preliminary study, Eur Radiol 29(7) (2019) 3358-3371.
M.A. Pascual, B. Graupera, L. Hereter, A. Rotili, I. Rodriguez, J.L. Alcazar, Intra- and interobserver variability of 2D and 3D transvaginal sonography in the diagnosis of benign versus malignant adnexal masses, J Clin Ultrasound 39(6) (2011) 316-21.
X. Jin, Y. Ai, J. Zhang, H. Zhu, J. Jin, Y. Teng, B. Chen, C. Xie, Noninvasive prediction of lymph node status for patients with early-stage cervical cancer based on radiomics features from ultrasound images, Eur Radiol 30(7) (2020) 4117-4124.
V.Y. Park, K. Han, E. Lee, E.K. Kim, H.J. Moon, J.H. Yoon, J.Y. Kwak, Association Between Radiomics Signature and Disease-Free Survival in Conventional Papillary Thyroid Carcinoma, Sci Rep 9(1) (2019) 4501.
H.T. Hu, Z. Wang, X.W. Huang, S.L. Chen, X. Zheng, S.M. Ruan, X.Y. Xie, M.D. Lu, J. Yu, J. Tian, P. Liang, W. Wang, M. Kuang, Ultrasound-based radiomics score: a potential biomarker for the prediction of microvascular invasion in hepatocellular carcinoma, Eur Radiol 29(6) (2019) 2890-2901.
D. DiCenzo, K. Quiaoit, K. Fatima, D. Bhardwaj, L. Sannachi, M. Gangeh, A. Sadeghi-Naini, A. Dasgupta, M.C. Kolios, M. Trudeau, S. Gandhi, A. Eisen, F. Wright, N. Look Hong, A. Sahgal, G. Stanisz, C. Brezden, R. Dinniwell, W.T. Tran, W. Yang, B. Curpen, G.J. Czarnota, Quantitative ultrasound radiomics in predicting response to neoadjuvant chemotherapy in patients with locally advanced breast cancer: Results from multi-institutional study, Cancer Med 9(16) (2020) 5798–5806. https://doi.org/10.1002/cam4.3255
V. Chiappa, G. Bogani, M. Interlenghi, C. Salvatore, F. Bertolina, G. Sarpietro, M. Signorelli, I. Castiglioni, F. Raspagliesi, The Adoption of Radiomics and machine learning improves the diagnostic processes of women with Ovarian MAsses (the AROMA pilot study), J Ultrasound (2020). https://doi.org/10.1007/s40477-020-00503-5.
A.J.A.P. Fattaneh, G.o.T.o.t. Breast, F.G. Organs, World Health Organization Classification of Tumours, 30(3) (2003) 274–276.
Q. Chen, D. Zhu, J. Liu, M. Zhang, H. Xu, Y. Xiang, C. Zhan, Y. Zhang, S. Huang, Y. Yang, Clinical-radiomics Nomogram for Risk Estimation of Early Hematoma Expansion after Acute Intracerebral Hemorrhage, Acad Radiol 28(3) (2021) 307–317. https://doi.org/10.1016/j.acra.2020.02.021
A. Meier, H. Veeraraghavan, S. Nougaret, Y. Lakhman, R. Sosa, R.A. Soslow, E.J. Sutton, H. Hricak, E. Sala, H.A. Vargas, Association between CT-texture-derived tumor heterogeneity, outcomes, and BRCA mutation status in patients with high-grade serous ovarian cancer, Abdom Radiol (NY) 44(6) (2019) 2040–2047.
D.Q. Zhu, Q. Chen, Y.L. Xiang, C.Y. Zhan, M.Y. Zhang, C. Chen, Q.C. Zhuge, W.J. Chen, X.M. Yang, Y.J. Yang, Predicting intraventricular hemorrhage growth with a machine learning-based, radiomics-clinical model, Aging (Albany NY) 13(9) (2021) 12833–12848. https://doi.org/10.18632/aging.202954.
A. Lindgren, M. Anttila, O. Arponen, S. Rautiainen, M. Kononen, R. Vanninen, H. Sallinen, Prognostic value of preoperative dynamic contrast-enhanced magnetic resonance imaging in epithelial ovarian cancer, Eur J Radiol 115 (2019) 66-73.
F. Zeppernick, I. Meinhold-Heerlein, The new FIGO staging system for ovarian, fallopian tube, and primary peritoneal cancer, Arch Gynecol Obstet 290(5) (2014) 839-42.
N. Komura, S. Mabuchi, K. Shimura, M. Kawano, Y. Matsumoto, T. Kimura, Significance of Pretreatment C-Reactive Protein, Albumin, and C-Reactive Protein to Albumin Ratio in Predicting Poor Prognosis in Epithelial Ovarian Cancer Patients, Nutr Cancer (2020). https://doi.org/10.1080/01635581.2020.1798479
L.N. Ge, F. Wang, Prognostic significance of preoperative serum albumin in epithelial ovarian cancer patients: a systematic review and dose-response meta-analysis of observational studies, Cancer Manag Res 10 (2018) 815-825.
B.R. Corr, M. Moroney, J. Sheeder, S.G. Eckhardt, B. Sawyer, K. Behbakht, J.R. Diamond, Survival and clinical outcomes of patients with ovarian cancer who were treated on phase 1 clinical trials, Cancer 126(19) (2020) 4289-4293.
M.P. Czub, A.M. Boulton, E.J. Rastelli, N.R. Tasker, T.S. Maskrey, I.K. Blanco, K.E. McQueeney, J.H. Bushweller, W. Minor, P. Wipf, E.R. Sharlow, J.S. Lazo, Structure of the Complex of an Iminopyridinedione Protein Tyrosine Phosphatase 4A3 Phosphatase Inhibitor with Human Serum Albumin, Mol Pharmacol 98(6) (2020) 648-657.
Z. Feng, H. Wen, X. Ju, R. Bi, X. Chen, W. Yang, X. Wu, The preoperative prognostic nutritional index is a predictive and prognostic factor of high-grade serous ovarian cancer, BMC Cancer 18(1) (2018) 883.
W. Chen, S. Zhong, B. Shan, S. Zhou, X. Wu, H. Yang, S. Ye, Serum D-dimer, albumin and systemic inflammatory response markers in ovarian clear cell carcinoma and their prognostic implications, J Ovarian Res 13(1) (2020) 89.
A. Mantovani, P. Allavena, A. Sica, F.J.N. Balkwill, Cancer-related inflammation, 454(7203) (2008) 436-44.
B. Laky, M. Janda, G. Cleghorn, A. Obermair, Comparison of different nutritional assessments and body-composition measurements in detecting malnutrition among gynecologic cancer patients, Am J Clin Nutr 87(6) (2008) 1678-1685. https://doi.org/10.1093/ajcn/87.6.1678.
Y.T. Peng, C.Y. Zhou, P. Lin, D.Y. Wen, X.D. Wang, X.Z. Zhong, D.H. Pan, Q. Que, X. Li, L. Chen, Y. He, H. Yang, Preoperative Ultrasound Radiomics Signatures for Noninvasive Evaluation of Biological Characteristics of Intrahepatic Cholangiocarcinoma, Acad Radiol 27(6) (2020) 785-797.
Y. Dong, Q.M. Wang, Q. Li, L.Y. Li, Q. Zhang, Z. Yao, M. Dai, J. Yu, W.P. Wang, Preoperative Prediction of Microvascular Invasion of Hepatocellular Carcinoma: Radiomics Algorithm Based on Ultrasound Original Radio Frequency Signals, Front Oncol 9 (2019) 1203.
M.R. Kwon, J.H. Shin, H. Park, H. Cho, E. Kim, S.Y. Hahn, Radiomics Based on Thyroid Ultrasound Can Predict Distant Metastasis of Follicular Thyroid Carcinoma, J Clin Med 9(7) (2020). https://doi.org/10.3390/jcm9072156
T. Liu, X. Ge, J. Yu, Y. Guo, Y. Wang, W. Wang, L. Cui, Comparison of the application of B-mode and strain elastography ultrasound in the estimation of lymph node metastasis of papillary thyroid carcinoma based on a radiomics approach, Int J Comput Assist Radiol Surg 13(10) (2018) 1617-1627.
B. Tran, J.E. Dancey, S. Kamel-Reid, J.D. McPherson, P.L. Bedard, A.M. Brown, T. Zhang, P. Shaw, N. Onetto, L. Stein, T.J. Hudson, B.G. Neel, L.L. Siu, Cancer genomics: technology, discovery, and translation, J Clin Oncol 30(6) (2012) 647-60.
R.M. Haralick, K. Shanmugam, I.H. Dinstein, Textural Features for Image Classification, IEEE Trans Syst Man Cybern SMC-3(6) (1973) 610–621. https://doi.org/10.1109/tsmc.1973.4309314.
P. Lambin, E. Rios-Velazquez, R. Leijenaar, S. Carvalho, R.G. van Stiphout, P. Granton, C.M. Zegers, R. Gillies, R. Boellard, A. Dekker, H.J. Aerts, Radiomics: extracting more information from medical images using advanced feature analysis, Eur J Cancer 48(4) (2012) 441-6.
Funding
This study has received funding by the Project of China Natural Science Foundation (Grant Number 81803781) and Project of Zhejiang Provincial Natural Science Foundation (Grant Number LQ18H280007).
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FY made substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data; or the creation of new software used in the work; FL drafted the work or revised it critically for important intellectual content. LL agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. FL and LL contributed equally to this work, they are the co-corresponding author.
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Yao, F., Ding, J., Hu, Z. et al. Ultrasound-based radiomics score: a potential biomarker for the prediction of progression-free survival in ovarian epithelial cancer. Abdom Radiol 46, 4936–4945 (2021). https://doi.org/10.1007/s00261-021-03163-z
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DOI: https://doi.org/10.1007/s00261-021-03163-z