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Published in: European Radiology 10/2021

01-10-2021 | Magnetic Resonance Imaging | Oncology

Noninvasive prediction of residual disease for advanced high-grade serous ovarian carcinoma by MRI-based radiomic-clinical nomogram

Authors: Haiming Li, Rui Zhang, Ruimin Li, Wei Xia, Xiaojun Chen, Jiayi Zhang, Songqi Cai, Yong’ai Li, Shuhui Zhao, Jinwei Qiang, Weijun Peng, Yajia Gu, Xin Gao

Published in: European Radiology | Issue 10/2021

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Abstract

Objectives

To develop a preoperative MRI-based radiomic-clinical nomogram for prediction of residual disease (RD) in patients with advanced high-grade serous ovarian carcinoma (HGSOC).

Methods

In total, 217 patients with advanced HGSOC were enrolled from January 2014 to June 2019 and randomly divided into a training set (n = 160) and a validation set (n = 57). Finally, 841 radiomic features were extracted from each tumor on T2-weighted imaging (T2WI) and contrast-enhanced T1-weighted imaging (CE-T1WI) sequence, respectively. We used two fusion methods, the maximal volume of interest (MV) and the maximal feature value (MF), to fuse the radiomic features of bilateral tumors, so that patients with bilateral tumors have the same kind of radiomic features as patients with unilateral tumors. The radiomic signatures were constructed by using mRMR method and LASSO classifier. Multivariable logistic regression analysis was used to develop a radiomic-clinical nomogram incorporating radiomic signature and conventional clinico-radiological features. The performance of the nomogram was evaluated on the validation set.

Results

In total, 342 tumors from 217 patients were analyzed in this study. The MF-based radiomic signature showed significantly better prediction performance than the MV-based radiomic signature (AUC = 0.744 vs. 0.650, p = 0.047). By incorporating clinico-radiological features and MF-based radiomic signature, radiomic-clinical nomogram showed favorable prediction ability with an AUC of 0.803 in the validation set, which was significantly higher than that of clinico-radiological signature and MF-based radiomic signature (AUC = 0.623, 0.744, respectively).

Conclusions

The proposed MRI-based radiomic-clinical nomogram provides a promising way to noninvasively predict the RD status.

Key Points

• MRI-based radiomic-clinical nomogram is feasible to noninvasively predict residual disease in patients with advanced HGSOC.
• The radiomic signature based on MF showed significantly better prediction performance than that based on MV.
• The radiomic-clinical nomogram showed a favorable prediction ability with an AUC of 0.803.
Appendix
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Literature
1.
go back to reference Wentzensen N, Poole EM, Trabert B et al (2016) Ovarian cancer risk factors by histologic subtype: An analysis from the Ovarian Cancer Cohort Consortium. J Clin Oncol 34:2888–2898PubMedPubMedCentralCrossRef Wentzensen N, Poole EM, Trabert B et al (2016) Ovarian cancer risk factors by histologic subtype: An analysis from the Ovarian Cancer Cohort Consortium. J Clin Oncol 34:2888–2898PubMedPubMedCentralCrossRef
2.
go back to reference Cybulska P, Stewart JM, Sayad A et al (2018) A genomically characterized collection of high-grade serous ovarian cancer xenografts for preclinical testing. Am J Pathol 188:1120–1131PubMedCrossRef Cybulska P, Stewart JM, Sayad A et al (2018) A genomically characterized collection of high-grade serous ovarian cancer xenografts for preclinical testing. Am J Pathol 188:1120–1131PubMedCrossRef
3.
go back to reference Verhaak RG, Tamayo P, Yang JY et al (2013) Prognostically relevant gene signatures of high-grade serous ovarian carcinoma. J Clin Invest 123:517–525PubMed Verhaak RG, Tamayo P, Yang JY et al (2013) Prognostically relevant gene signatures of high-grade serous ovarian carcinoma. J Clin Invest 123:517–525PubMed
4.
go back to reference Chang SJ, Bristow RE, Ryu HS (2012) Impact of complete cytoreduction leaving no gross residual disease associated with radical cytoreductive surgical procedures on survival in advanced ovarian cancer. Ann Surg Oncol 19:4059–4067PubMedCrossRef Chang SJ, Bristow RE, Ryu HS (2012) Impact of complete cytoreduction leaving no gross residual disease associated with radical cytoreductive surgical procedures on survival in advanced ovarian cancer. Ann Surg Oncol 19:4059–4067PubMedCrossRef
5.
go back to reference du Bois A, Reuss A, Pujade-Lauraine E et al (2009) Role of surgical outcome as prognostic factor in advanced epithelial ovarian cancer: A combined exploratory analysis of 3 prospectively randomized phase 3 multicenter trials: by the Arbeitsgemeinschaft Gynaekologische Onkologie Studiengruppe Ovarialkarzinom (AGO-OVAR) and the Groupe d'Investigateurs Nationaux Poue Ies Etudes des Cancers de I'Ovaire (GINECO). Cancer 115:1234–1244PubMedCrossRef du Bois A, Reuss A, Pujade-Lauraine E et al (2009) Role of surgical outcome as prognostic factor in advanced epithelial ovarian cancer: A combined exploratory analysis of 3 prospectively randomized phase 3 multicenter trials: by the Arbeitsgemeinschaft Gynaekologische Onkologie Studiengruppe Ovarialkarzinom (AGO-OVAR) and the Groupe d'Investigateurs Nationaux Poue Ies Etudes des Cancers de I'Ovaire (GINECO). Cancer 115:1234–1244PubMedCrossRef
6.
go back to reference Fagotti A, Vizzielli G, Fanfani F et al (2015) Introduction of staging laparoscopy in the management of advanced epithelial ovarian, tubal and peritoneal cancer: Impact on prognosis in a single institution experience. Gynecol Oncol 131:341–346CrossRef Fagotti A, Vizzielli G, Fanfani F et al (2015) Introduction of staging laparoscopy in the management of advanced epithelial ovarian, tubal and peritoneal cancer: Impact on prognosis in a single institution experience. Gynecol Oncol 131:341–346CrossRef
7.
go back to reference Kehoe S, Hook J, Nankivell M et al (2015) Primary chemotherapy versus primary surgery for newly diagnosed advanced ovarian cancer (CHORUS): An open-label, randomised, controlled non-inferiority trial. Lancet 386:249–257PubMedCrossRef Kehoe S, Hook J, Nankivell M et al (2015) Primary chemotherapy versus primary surgery for newly diagnosed advanced ovarian cancer (CHORUS): An open-label, randomised, controlled non-inferiority trial. Lancet 386:249–257PubMedCrossRef
8.
go back to reference Vergote I, Tropé CG, Amant F et al (2010) Neoadjuvant chemotherapy or primary surgery in stage IIIc or IV ovarian cancer. N Engl J Med 363:943–953PubMedCrossRef Vergote I, Tropé CG, Amant F et al (2010) Neoadjuvant chemotherapy or primary surgery in stage IIIc or IV ovarian cancer. N Engl J Med 363:943–953PubMedCrossRef
9.
go back to reference Ghirardi V, Moruzzi MC, Bizzarri N et al (2020) Minimal residual disease at primary debulking surgery versus complete tumor resection at interval debulking surgery in advanced epithelial ovarian cancer: A survival analysis. Gynecol Oncol 157:209–213PubMedCrossRef Ghirardi V, Moruzzi MC, Bizzarri N et al (2020) Minimal residual disease at primary debulking surgery versus complete tumor resection at interval debulking surgery in advanced epithelial ovarian cancer: A survival analysis. Gynecol Oncol 157:209–213PubMedCrossRef
10.
go back to reference Fagotti A, Ferrandina G, Fanfani F et al (2006) A laparoscopy-based score to predict surgical outcome in patients with advanced ovarian carcinoma: A pilot study. Ann Surg Oncol 13:1156–1161PubMedCrossRef Fagotti A, Ferrandina G, Fanfani F et al (2006) A laparoscopy-based score to predict surgical outcome in patients with advanced ovarian carcinoma: A pilot study. Ann Surg Oncol 13:1156–1161PubMedCrossRef
11.
go back to reference van de Vrie R, Rutten MJ, Asseler JD et al (2019) Laparoscopy for diagnosing resectability of disease in women with advanced cancer. Cochrane Database Syst Rev 3:CD009786PubMed van de Vrie R, Rutten MJ, Asseler JD et al (2019) Laparoscopy for diagnosing resectability of disease in women with advanced cancer. Cochrane Database Syst Rev 3:CD009786PubMed
12.
go back to reference Suidan RS, Ramirez PT, Sarasohn DM et al (2014) A multicenter prospective trial evaluating the ability of preoperative computed tomography scan and serum CA-125 to predict suboptimal cytoreduction at primary debulking surgery for advanced ovarian, fallopian tube, and peritoneal cancer. Gynecol Oncol 134:455–461PubMedPubMedCentralCrossRef Suidan RS, Ramirez PT, Sarasohn DM et al (2014) A multicenter prospective trial evaluating the ability of preoperative computed tomography scan and serum CA-125 to predict suboptimal cytoreduction at primary debulking surgery for advanced ovarian, fallopian tube, and peritoneal cancer. Gynecol Oncol 134:455–461PubMedPubMedCentralCrossRef
13.
go back to reference Bristow RE, Duska LR, Lambrou NC et al (2000) A model for predicting surgical outcome in patients with advanced ovarian carcinoma using computed tomography. Cancer 89:1532–1540PubMedCrossRef Bristow RE, Duska LR, Lambrou NC et al (2000) A model for predicting surgical outcome in patients with advanced ovarian carcinoma using computed tomography. Cancer 89:1532–1540PubMedCrossRef
14.
go back to reference Dowdy SC, Mullany SA, Brandt KR, Huppert BJ, Cliby WA (2004) The utility of computed tomography scans in predicting suboptimal cytoreductive surgery in women with advanced ovarian cancer. Cancer 101:346–352PubMedCrossRef Dowdy SC, Mullany SA, Brandt KR, Huppert BJ, Cliby WA (2004) The utility of computed tomography scans in predicting suboptimal cytoreductive surgery in women with advanced ovarian cancer. Cancer 101:346–352PubMedCrossRef
15.
go back to reference Axtell AE, Lee MH, Bristow RE et al (2007) Multi-institutional reciprocal validation study of computed tomography predictors of suboptimal primary cytoredcution in patients with advanced ovarian cancer. J Clin Oncol 25:384–389PubMedCrossRef Axtell AE, Lee MH, Bristow RE et al (2007) Multi-institutional reciprocal validation study of computed tomography predictors of suboptimal primary cytoredcution in patients with advanced ovarian cancer. J Clin Oncol 25:384–389PubMedCrossRef
16.
go back to reference Feng Z, Wen H, Jiang Z et al (2018) A triage strategy in advanced ovarian cancer management based on multiple predictive models for R0 resection: A prospective cohort study. J Gynecol Oncol 29:e65PubMedPubMedCentralCrossRef Feng Z, Wen H, Jiang Z et al (2018) A triage strategy in advanced ovarian cancer management based on multiple predictive models for R0 resection: A prospective cohort study. J Gynecol Oncol 29:e65PubMedPubMedCentralCrossRef
17.
go back to reference Lambin P, Leijenaar RTH, Deist TM et al (2017) Radiomics: The bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol 14:749–762PubMedCrossRef Lambin P, Leijenaar RTH, Deist TM et al (2017) Radiomics: The bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol 14:749–762PubMedCrossRef
18.
go back to reference Dong D, Tang L, Li ZY et al (2019) Development and validation of an individualized nomogram to identify occult peritoneal metastasis in patients with advanced gastric cancer. Ann Oncol 30:431–438PubMedPubMedCentralCrossRef Dong D, Tang L, Li ZY et al (2019) Development and validation of an individualized nomogram to identify occult peritoneal metastasis in patients with advanced gastric cancer. Ann Oncol 30:431–438PubMedPubMedCentralCrossRef
19.
go back to reference Liu ZY, Zhang XY, Shi YJ et al (2017) Radiomics analysis for evaluation of pathological complete response to neoadjuvant chemotherapy in locally advanced rectal cancer. Clin Cancer Res 23:7253–7262PubMedCrossRef Liu ZY, Zhang XY, Shi YJ et al (2017) Radiomics analysis for evaluation of pathological complete response to neoadjuvant chemotherapy in locally advanced rectal cancer. Clin Cancer Res 23:7253–7262PubMedCrossRef
20.
go back to reference Peng H, Dong D, Fang MJ et al (2019) Prognostic value of deep learning PET/CT-based radiomics: Potential role for future individual induction chemotherapy in advanced nasopharyngeal carcinoma. Clin Cancer Res 25:4271–4279PubMedCrossRef Peng H, Dong D, Fang MJ et al (2019) Prognostic value of deep learning PET/CT-based radiomics: Potential role for future individual induction chemotherapy in advanced nasopharyngeal carcinoma. Clin Cancer Res 25:4271–4279PubMedCrossRef
21.
go back to reference Nougaret S, Nikolovski I, Paroder V et al (2019) MRI of tumors and tumor mimics in the female pelvis: Anatomic pelvic space-based approach. Radiographics 39:1205–1229PubMedCrossRef Nougaret S, Nikolovski I, Paroder V et al (2019) MRI of tumors and tumor mimics in the female pelvis: Anatomic pelvic space-based approach. Radiographics 39:1205–1229PubMedCrossRef
22.
go back to reference Zhang H, Mao Y, Chen X et al (2019) Magnetic resonance imaging radiomics in categorizing ovarian masses and predicting clinical outcome: A preliminary study. Eur Radiol 29:3358–3371PubMedCrossRef Zhang H, Mao Y, Chen X et al (2019) Magnetic resonance imaging radiomics in categorizing ovarian masses and predicting clinical outcome: A preliminary study. Eur Radiol 29:3358–3371PubMedCrossRef
23.
go back to reference Lee EYP, An H, Perucho JAU et al (2020) Functional tumour burden of peritoneal carcinomatosis derived from DWI could predict incomplete tumour debulking in advanced ovarian carcinoma. Eur Radiol 30:5551–5559PubMedCrossRef Lee EYP, An H, Perucho JAU et al (2020) Functional tumour burden of peritoneal carcinomatosis derived from DWI could predict incomplete tumour debulking in advanced ovarian carcinoma. Eur Radiol 30:5551–5559PubMedCrossRef
24.
go back to reference Mutch DG, Prat J (2014) 2014 FIGO staging for ovarian, fallopian tube and peritoneal cancer. Gynecol Oncol 133:401–404PubMedCrossRef Mutch DG, Prat J (2014) 2014 FIGO staging for ovarian, fallopian tube and peritoneal cancer. Gynecol Oncol 133:401–404PubMedCrossRef
25.
go back to reference Gillies RJ, Kinahan PE, Hricak H (2016) Radiomics: Images are more than pictures, they are data. Radiology 278:563–577PubMedCrossRef Gillies RJ, Kinahan PE, Hricak H (2016) Radiomics: Images are more than pictures, they are data. Radiology 278:563–577PubMedCrossRef
26.
go back to reference Meng X, Xia W, Xie P et al (2019) Preoperative radiomic signature based on multiparametric magnetic resonance imaging for noninvasive evaluation of biological characteristics in rectal cancer. Eur Radiol 29:3200–3209PubMedCrossRef Meng X, Xia W, Xie P et al (2019) Preoperative radiomic signature based on multiparametric magnetic resonance imaging for noninvasive evaluation of biological characteristics in rectal cancer. Eur Radiol 29:3200–3209PubMedCrossRef
27.
go back to reference Huang YQ, Liang CH, He L et al (2016) Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol 34:2157–2164PubMedCrossRef Huang YQ, Liang CH, He L et al (2016) Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol 34:2157–2164PubMedCrossRef
28.
go back to reference Zheng J, Kong J, Wu S et al (2019) Development of a noninvasive tool to preoperatively evaluate the muscular invasiveness of bladder cancer using a radiomics approach. Cancer 125:4388–4398PubMedCrossRef Zheng J, Kong J, Wu S et al (2019) Development of a noninvasive tool to preoperatively evaluate the muscular invasiveness of bladder cancer using a radiomics approach. Cancer 125:4388–4398PubMedCrossRef
29.
go back to reference Sun R, Limkin EJ, Vakalopoulou M et al (2018) A radiomics approach to assess tumour-infiltrating CD8 cells and response to anti-PD-1 or anti-PD-L1 immunotherapy: An imaging biomarker, retrospective multicohort study. Lancet Oncol 19:1180–1191PubMedCrossRef Sun R, Limkin EJ, Vakalopoulou M et al (2018) A radiomics approach to assess tumour-infiltrating CD8 cells and response to anti-PD-1 or anti-PD-L1 immunotherapy: An imaging biomarker, retrospective multicohort study. Lancet Oncol 19:1180–1191PubMedCrossRef
30.
go back to reference Messal HA, Alt S, Ferreira RMM et al (2019) Tissue curvature and apicobasal mechanical tension imbalance instruct cancer morphogenesis. Nature 566:126–130PubMedPubMedCentralCrossRef Messal HA, Alt S, Ferreira RMM et al (2019) Tissue curvature and apicobasal mechanical tension imbalance instruct cancer morphogenesis. Nature 566:126–130PubMedPubMedCentralCrossRef
32.
go back to reference Michielsen K, Dresen R, Vanslembrouck R et al (2017) Diagnostic value of whole body diffusion-weighted MRI compared to computed tomography for pre-operative assessment of patients suspected for ovarian cancer. Eur J Cancer 83:88–98PubMedCrossRef Michielsen K, Dresen R, Vanslembrouck R et al (2017) Diagnostic value of whole body diffusion-weighted MRI compared to computed tomography for pre-operative assessment of patients suspected for ovarian cancer. Eur J Cancer 83:88–98PubMedCrossRef
33.
go back to reference Roze JF, Hoogendam JP, van de Wetering FT et al (2018) Positron emission tomography (PET) and magnetic resonance imaging (MRI) for assessing tumour resectability in advanced epithelial ovarian/fallopian tube/primary peritoneal cancer. Cochrane Database Syst Rev 10:CD012567PubMed Roze JF, Hoogendam JP, van de Wetering FT et al (2018) Positron emission tomography (PET) and magnetic resonance imaging (MRI) for assessing tumour resectability in advanced epithelial ovarian/fallopian tube/primary peritoneal cancer. Cochrane Database Syst Rev 10:CD012567PubMed
34.
go back to reference Wright AA, Bohlke K, Armstrong DK et al (2016) Neoadjuvant chemotherapy for newly diagnosed, advanced ovarian cancer: Society of Gynecologic Oncology and American Society of Clinical Oncology Clinical practice guideline. J Clin Oncol 34:3460–3473PubMedCrossRef Wright AA, Bohlke K, Armstrong DK et al (2016) Neoadjuvant chemotherapy for newly diagnosed, advanced ovarian cancer: Society of Gynecologic Oncology and American Society of Clinical Oncology Clinical practice guideline. J Clin Oncol 34:3460–3473PubMedCrossRef
35.
go back to reference Chang SJ, Hodeib M, Chang J, Bristow RE (2013) Survival impact of complete cytoreduction to no gross residual disease for advanced-stage ovarian cancer: A meta-analysis. Gynecol Oncol 130:493–498PubMedCrossRef Chang SJ, Hodeib M, Chang J, Bristow RE (2013) Survival impact of complete cytoreduction to no gross residual disease for advanced-stage ovarian cancer: A meta-analysis. Gynecol Oncol 130:493–498PubMedCrossRef
36.
go back to reference Varghese BA, Cen SY, Hwang DH, Duddalwar VA (2019) Texture analysis of imaging: What radiologists need to know. AJR Am J Roentgenol 212:520–528PubMedCrossRef Varghese BA, Cen SY, Hwang DH, Duddalwar VA (2019) Texture analysis of imaging: What radiologists need to know. AJR Am J Roentgenol 212:520–528PubMedCrossRef
37.
go back to reference Rizzo S, Botta F, Raimondi S et al (2018) Radiomics of high-grade serous ovarian cancer: Association between quantitative CT features, residual tumour and disease progression within 12 months. Eur Radiol 28:4849–4859PubMedCrossRef Rizzo S, Botta F, Raimondi S et al (2018) Radiomics of high-grade serous ovarian cancer: Association between quantitative CT features, residual tumour and disease progression within 12 months. Eur Radiol 28:4849–4859PubMedCrossRef
38.
go back to reference Lu H, Arshad M, Thornton A et al (2019) A mathematical-descriptor of tumor-mesoscopic-structure from computed-tomography images annotates prognostic- and molecular-phenotypes of epithelial ovarian cancer. Nat Commun 10:764PubMedPubMedCentralCrossRef Lu H, Arshad M, Thornton A et al (2019) A mathematical-descriptor of tumor-mesoscopic-structure from computed-tomography images annotates prognostic- and molecular-phenotypes of epithelial ovarian cancer. Nat Commun 10:764PubMedPubMedCentralCrossRef
39.
go back to reference Kim BR, Kim JH, Ahn SJ et al (2019) CT prediction of resectability and prognosis in patients with pancreatic ductal adenocarcinoma after neoadjuvant treatment using image findings and texture analysis. Eur Radiol 29:362–372PubMedCrossRef Kim BR, Kim JH, Ahn SJ et al (2019) CT prediction of resectability and prognosis in patients with pancreatic ductal adenocarcinoma after neoadjuvant treatment using image findings and texture analysis. Eur Radiol 29:362–372PubMedCrossRef
40.
go back to reference Vargas HA, Veeraraghavan H, Micco M et al (2017) A novel representation of inter-site tumour heterogeneity from pre-treatment computed tomography textures classifies ovarian cancers by clinical outcome. Eur Radiol 27:3991–4001PubMedPubMedCentralCrossRef Vargas HA, Veeraraghavan H, Micco M et al (2017) A novel representation of inter-site tumour heterogeneity from pre-treatment computed tomography textures classifies ovarian cancers by clinical outcome. Eur Radiol 27:3991–4001PubMedPubMedCentralCrossRef
41.
go back to reference Pinto MP, Balmaceda C, Bravo ML et al (2018) Patients inflammatory status and CD4+/CD8+ intraepithelial tumor lymphocyte infiltration are predictors of outcomes in high-grade serous ovarian cancer. Gynecol Oncol 151:10–17PubMedCrossRef Pinto MP, Balmaceda C, Bravo ML et al (2018) Patients inflammatory status and CD4+/CD8+ intraepithelial tumor lymphocyte infiltration are predictors of outcomes in high-grade serous ovarian cancer. Gynecol Oncol 151:10–17PubMedCrossRef
42.
go back to reference Li Y, Jian J, Pickhardt PJ et al (2020) MRI-based machine learning for differentiating borderline from malignant epithelial ovarian tumors: A multicenter study. J Magn Reson Imaging 52:897–904PubMedCrossRef Li Y, Jian J, Pickhardt PJ et al (2020) MRI-based machine learning for differentiating borderline from malignant epithelial ovarian tumors: A multicenter study. J Magn Reson Imaging 52:897–904PubMedCrossRef
43.
go back to reference Nougaret S, Lakhman Y, Gönen M et al (2019) High-grade serous ovarian cancer: Associations between BRCA mutation status, CT imaging phenotypes, and clinical outcomes. Radiology 285:472–481CrossRef Nougaret S, Lakhman Y, Gönen M et al (2019) High-grade serous ovarian cancer: Associations between BRCA mutation status, CT imaging phenotypes, and clinical outcomes. Radiology 285:472–481CrossRef
44.
go back to reference Torres D, Wang C, Kumar A et al (2018) Factors that influence survival in high-grade serous ovarian cancer: A complex relationship between molecular subtype, disease dissemination, and operability. Gynecol Oncol 150:227–232PubMedPubMedCentralCrossRef Torres D, Wang C, Kumar A et al (2018) Factors that influence survival in high-grade serous ovarian cancer: A complex relationship between molecular subtype, disease dissemination, and operability. Gynecol Oncol 150:227–232PubMedPubMedCentralCrossRef
Metadata
Title
Noninvasive prediction of residual disease for advanced high-grade serous ovarian carcinoma by MRI-based radiomic-clinical nomogram
Authors
Haiming Li
Rui Zhang
Ruimin Li
Wei Xia
Xiaojun Chen
Jiayi Zhang
Songqi Cai
Yong’ai Li
Shuhui Zhao
Jinwei Qiang
Weijun Peng
Yajia Gu
Xin Gao
Publication date
01-10-2021
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 10/2021
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-021-07902-0

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