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Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging 8/2022

28.03.2022 | Original Article

The radiomics-based tumor heterogeneity adds incremental value to the existing prognostic models for predicting outcome in localized clear cell renal cell carcinoma: a multicenter study

verfasst von: Guangjie Yang, Pei Nie, Lei Yan, Mingxin Zhang, Yangyang Wang, Lianzi Zhao, Mingyao Li, Fei Xie, Haizhu Xie, Xianjun Li, Fawei Xiang, Nan Wang, Nan Cheng, Xia Zhao, Ning Wang, Yicong Wang, Chengcheng Chen, Canhua Yun, Jingjing Cui, Shaofeng Duan, Ran Zhang, Dapeng Hao, Ximing Wang, Zhenguang Wang, Haitao Niu

Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging | Ausgabe 8/2022

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Abstract

Purpose

Tumor heterogeneity, which is associated with poor outcomes, has not been exhibited in the University of California, Los Angeles, Integrated Staging System (UISS), and the Stage, Size, Grade and Necrosis (SSIGN) scores. Radiomics allows an in-depth characterization of heterogeneity across the tumor, but its incremental value to the existing prognostic models for clear cell renal cell carcinoma (ccRCC) outcome is unknown. The purpose of this study was to evaluate the association between the radiomics-based tumor heterogeneity and postoperative risk of recurrence in localized ccRCC, and to assess its incremental value to UISS and SSIGN.

Methods

A multicenter 866 ccRCC patients derived from 12 Chinese hospitals were studied. The endpoint was recurrence-free survival (RFS). A CT-based radiomics signature (RS) was developed and assessed in the whole cohort and in the subgroups stratified by UISS and SSIGN. Two combined nomograms, the R-UISS (combining RS and UISS) and R-SSIGN (combining RS and SSIGN), were developed. The incremental value of RS to UISS and SSIGN in RFS prediction was evaluated. R statistical software was used for statistics.

Results

Patients with low radiomics scores were 4.44 times more likely to experience recurrence than those with high radiomics scores (P<0.001). Stratified analysis suggested the association is significant among low- and intermediate-risk patients identified by UISS and SSIGN. The R-UISS and R-SSIGN showed better predictive capability than UISS and SSIGN did with higher C-indices (R-UISS vs. UISS, 0.74 vs. 0.64; R-SSIGN vs. SSIGN, 0.78 vs. 0.76) and higher clinical net benefit.

Conclusions

The radiomics-based tumor heterogeneity can predict outcome and add incremental value to the existing prognostic models in localized ccRCC patients. Incorporating radiomics-based tumor heterogeneity in ccRCC prognostic models may provide the opportunity to better surveillance and adjuvant clinical trial design.
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Literatur
1.
Zurück zum Zitat Volpe A, Patard JJ. Prognostic factors in renal cell carcinoma. World J Urol. 2010;28:319–27.CrossRef Volpe A, Patard JJ. Prognostic factors in renal cell carcinoma. World J Urol. 2010;28:319–27.CrossRef
2.
Zurück zum Zitat Stewart SB, Thompson RH, Psutka SP, Cheville JC, Lohse CM, Boorjian SA, et al. Evaluation of the National Comprehensive Cancer Network and American Urological Association renal cell carcinoma surveillance guidelines. J Clin Oncol. 2014;32:4059–65.CrossRef Stewart SB, Thompson RH, Psutka SP, Cheville JC, Lohse CM, Boorjian SA, et al. Evaluation of the National Comprehensive Cancer Network and American Urological Association renal cell carcinoma surveillance guidelines. J Clin Oncol. 2014;32:4059–65.CrossRef
3.
Zurück zum Zitat Zhang J, Fujimoto J, Zhang J, Wedge DC, Song X, Zhang J, et al. Intratumor heterogeneity in localized lung adenocarcinomas delineated by multiregion sequencing. Science. 2014;346:256–9.CrossRef Zhang J, Fujimoto J, Zhang J, Wedge DC, Song X, Zhang J, et al. Intratumor heterogeneity in localized lung adenocarcinomas delineated by multiregion sequencing. Science. 2014;346:256–9.CrossRef
4.
Zurück zum Zitat Rutman AM, Kuo MD. Radiogenomics: creating a link between molecular diagnostics and diagnostic imaging. Eur J Radiol. 2009;70:232–41.CrossRef Rutman AM, Kuo MD. Radiogenomics: creating a link between molecular diagnostics and diagnostic imaging. Eur J Radiol. 2009;70:232–41.CrossRef
5.
Zurück zum Zitat de Leon AD, Kapur P, Pedrosa I. Radiomics in kidney cancer: MR imaging. Magn Reson Imaging Clin N Am. 2019;27:1–13.CrossRef de Leon AD, Kapur P, Pedrosa I. Radiomics in kidney cancer: MR imaging. Magn Reson Imaging Clin N Am. 2019;27:1–13.CrossRef
6.
Zurück zum Zitat Jiang Y, Yuan Q, Lv W, Xi S, Huang W, Sun Z, et al. Radiomic signature of (18)F fluorodeoxyglucose PET/CT for prediction of gastric cancer survival and chemotherapeutic benefits. Theranostics. 2018;8:5915–28.CrossRef Jiang Y, Yuan Q, Lv W, Xi S, Huang W, Sun Z, et al. Radiomic signature of (18)F fluorodeoxyglucose PET/CT for prediction of gastric cancer survival and chemotherapeutic benefits. Theranostics. 2018;8:5915–28.CrossRef
7.
Zurück zum Zitat Li W, Zhang L, Tian C, Song H, Fang M, Hu C, et al. Prognostic value of computed tomography radiomics features in patients with gastric cancer following curative resection. Eur Radiol. 2019;29:3079–89.CrossRef Li W, Zhang L, Tian C, Song H, Fang M, Hu C, et al. Prognostic value of computed tomography radiomics features in patients with gastric cancer following curative resection. Eur Radiol. 2019;29:3079–89.CrossRef
8.
Zurück zum Zitat Huang Y, Liu Z, He L, Chen X, Pan D, Ma Z, et al. Radiomics signature: a potential biomarker for the prediction of disease-free survival in early-stage (I or II) non-small cell lung cancer. Radiology. 2016;281:947–57.CrossRef Huang Y, Liu Z, He L, Chen X, Pan D, Ma Z, et al. Radiomics signature: a potential biomarker for the prediction of disease-free survival in early-stage (I or II) non-small cell lung cancer. Radiology. 2016;281:947–57.CrossRef
9.
Zurück zum Zitat Lin P, Wen DY, Chen L, Li X, Li SH, Yan HB, et al. A radiogenomics signature for predicting the clinical outcome of bladder urothelial carcinoma. Eur Radiol. 2020;30:547–57.CrossRef Lin P, Wen DY, Chen L, Li X, Li SH, Yan HB, et al. A radiogenomics signature for predicting the clinical outcome of bladder urothelial carcinoma. Eur Radiol. 2020;30:547–57.CrossRef
10.
Zurück zum Zitat Park H, Lim Y, Ko ES, Cho HH, Lee JE, Han BK, et al. Radiomics signature on magnetic resonance imaging: association with disease-free survival in patients with invasive breast cancer. Clin Cancer Res. 2018;24:4705–14.CrossRef Park H, Lim Y, Ko ES, Cho HH, Lee JE, Han BK, et al. Radiomics signature on magnetic resonance imaging: association with disease-free survival in patients with invasive breast cancer. Clin Cancer Res. 2018;24:4705–14.CrossRef
11.
Zurück zum Zitat Wu Y, Xu L, Yang P, Lin N, Huang X, Pan W, et al. Survival prediction in high-grade osteosarcoma using radiomics of diagnostic computed tomography. EBioMedicine. 2018;34:27–34.CrossRef Wu Y, Xu L, Yang P, Lin N, Huang X, Pan W, et al. Survival prediction in high-grade osteosarcoma using radiomics of diagnostic computed tomography. EBioMedicine. 2018;34:27–34.CrossRef
12.
Zurück zum Zitat Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): the TRIPOD statement. BMJ. 2015;350:g7594.CrossRef Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): the TRIPOD statement. BMJ. 2015;350:g7594.CrossRef
13.
Zurück zum Zitat Zisman A, Pantuck AJ, Wieder J, Chao DH, Dorey F, Said JW, et al. Risk group assessment and clinical outcome algorithm to predict the natural history of patients with surgically resected renal cell carcinoma. J Clin Oncol. 2002;20:4559–66.CrossRef Zisman A, Pantuck AJ, Wieder J, Chao DH, Dorey F, Said JW, et al. Risk group assessment and clinical outcome algorithm to predict the natural history of patients with surgically resected renal cell carcinoma. J Clin Oncol. 2002;20:4559–66.CrossRef
14.
Zurück zum Zitat Leibovich BC, Blute ML, Cheville JC, Lohse CM, Frank I, Kwon ED, et al. Prediction of progression after radical nephrectomy for patients with clear cell renal cell carcinoma: a stratification tool for prospective clinical trials. Cancer. 2003;97:1663–71.CrossRef Leibovich BC, Blute ML, Cheville JC, Lohse CM, Frank I, Kwon ED, et al. Prediction of progression after radical nephrectomy for patients with clear cell renal cell carcinoma: a stratification tool for prospective clinical trials. Cancer. 2003;97:1663–71.CrossRef
15.
Zurück zum Zitat Nie P, Yang G, Wang N, Yan L, Miao W, Duan Y, Wang Y, Gong A, Zhao Y, Wu J, Zhang C, Wang M, Cui J, Yu M, Li D, Sun Y, Wang Y, Wang Z. Additional value of metabolic parameters to PET/CT-based radiomics nomogram in predicting lymphovascular invasion and outcome in lung adenocarcinoma. Eur J Nucl Med Mol Imaging. 2021:48217–30. Nie P, Yang G, Wang N, Yan L, Miao W, Duan Y, Wang Y, Gong A, Zhao Y, Wu J, Zhang C, Wang M, Cui J, Yu M, Li D, Sun Y, Wang Y, Wang Z. Additional value of metabolic parameters to PET/CT-based radiomics nomogram in predicting lymphovascular invasion and outcome in lung adenocarcinoma. Eur J Nucl Med Mol Imaging. 2021:48217–30.
16.
Zurück zum Zitat Nie P, Yang G, Wang Z, Yan L, Miao W, Hao D, Wu J, Zhao Y, Gong A, Cui J, Jia Y, Niu H. A CT-based radiomics nomogram for differentiation of renal angiomyolipoma without visible fat from homogeneous clear cell renal cell carcinoma. Eur Radiol. 2020;30:1274–84.CrossRef Nie P, Yang G, Wang Z, Yan L, Miao W, Hao D, Wu J, Zhao Y, Gong A, Cui J, Jia Y, Niu H. A CT-based radiomics nomogram for differentiation of renal angiomyolipoma without visible fat from homogeneous clear cell renal cell carcinoma. Eur Radiol. 2020;30:1274–84.CrossRef
17.
Zurück zum Zitat Correa AF, Jegede O, Haas NB, Flaherty KT, Pins MR, Messing EM, et al. Predicting renal cancer recurrence: defining limitations of existing prognostic models with prospective trial-based validation. J Clin Oncol. 2019;37:2062–71.CrossRef Correa AF, Jegede O, Haas NB, Flaherty KT, Pins MR, Messing EM, et al. Predicting renal cancer recurrence: defining limitations of existing prognostic models with prospective trial-based validation. J Clin Oncol. 2019;37:2062–71.CrossRef
18.
Zurück zum Zitat Ficarra V, Novara G, Galfano A, Brunelli M, Cavalleri S, Martignoni G, et al. The ‘Stage, Size, Grade and Necrosis’ score is more accurate than the University of California Los Angeles Integrated Staging System for predicting cancer-specific survival in patients with clear cell renal cell carcinoma. BJU Int. 2009;103:165–70.CrossRef Ficarra V, Novara G, Galfano A, Brunelli M, Cavalleri S, Martignoni G, et al. The ‘Stage, Size, Grade and Necrosis’ score is more accurate than the University of California Los Angeles Integrated Staging System for predicting cancer-specific survival in patients with clear cell renal cell carcinoma. BJU Int. 2009;103:165–70.CrossRef
19.
Zurück zum Zitat Parker WP, Cheville JC, Frank I, Zaid HB, Lohse CM, Boorjian SA, et al. Application of the Stage, Size, Grade, and Necrosis (SSIGN) score for clear cell renal cell carcinoma in contemporary patients. Eur Urol. 2017;71:665–73.CrossRef Parker WP, Cheville JC, Frank I, Zaid HB, Lohse CM, Boorjian SA, et al. Application of the Stage, Size, Grade, and Necrosis (SSIGN) score for clear cell renal cell carcinoma in contemporary patients. Eur Urol. 2017;71:665–73.CrossRef
20.
Zurück zum Zitat Ohsugi H, Yoshida T, Ohe C, Ikeda J, Sugi M, Kinoshita H, et al. The SSPN score, a novel scoring system incorporating PBRM1 expression, predicts postoperative recurrence for patients with non-metastatic clear cell renal cell carcinoma. Ann Surg Oncol. 2021;28:2359–66.CrossRef Ohsugi H, Yoshida T, Ohe C, Ikeda J, Sugi M, Kinoshita H, et al. The SSPN score, a novel scoring system incorporating PBRM1 expression, predicts postoperative recurrence for patients with non-metastatic clear cell renal cell carcinoma. Ann Surg Oncol. 2021;28:2359–66.CrossRef
21.
Zurück zum Zitat El Khoury LY, Fu S, Hlady RA, Wagner RT, Wang L, Eckel-Passow JE, et al. Identification of DNA methylation signatures associated with poor outcome in lower-risk Stage, Size, Grade and Necrosis (SSIGN) score clear cell renal cell cancer. Clin Epigenetics. 2021;13:12.CrossRef El Khoury LY, Fu S, Hlady RA, Wagner RT, Wang L, Eckel-Passow JE, et al. Identification of DNA methylation signatures associated with poor outcome in lower-risk Stage, Size, Grade and Necrosis (SSIGN) score clear cell renal cell cancer. Clin Epigenetics. 2021;13:12.CrossRef
22.
Zurück zum Zitat Sun R, Limkin EJ, Vakalopoulou M, Dercle L, Champiat S, Han SR, et al. 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. 2018;19:1180–91.CrossRef Sun R, Limkin EJ, Vakalopoulou M, Dercle L, Champiat S, Han SR, et al. 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. 2018;19:1180–91.CrossRef
23.
Zurück zum Zitat Mulé S, Thiefin G, Costentin C, Durot C, Rahmouni A, Luciani A, et al. Advanced hepatocellular carcinoma: pretreatment contrast-enhanced CT texture parameters as predictive biomarkers of survival in patients treated with sorafenib. Radiology. 2018;288:445–55.CrossRef Mulé S, Thiefin G, Costentin C, Durot C, Rahmouni A, Luciani A, et al. Advanced hepatocellular carcinoma: pretreatment contrast-enhanced CT texture parameters as predictive biomarkers of survival in patients treated with sorafenib. Radiology. 2018;288:445–55.CrossRef
24.
Zurück zum Zitat Ganeshan B, Skogen K, Pressney I, Coutroubis D, Miles K. Tumour heterogeneity in oesophageal cancer assessed by CT texture analysis: preliminary evidence of an association with tumour metabolism, stage, and survival. Clin Radiol. 2012;67:157–64.CrossRef Ganeshan B, Skogen K, Pressney I, Coutroubis D, Miles K. Tumour heterogeneity in oesophageal cancer assessed by CT texture analysis: preliminary evidence of an association with tumour metabolism, stage, and survival. Clin Radiol. 2012;67:157–64.CrossRef
25.
Zurück zum Zitat Kim JH, Ko ES, Lim Y, Lee KS, Han BK, Ko EY, et al. Breast cancer heterogeneity: MR imaging texture analysis and survival outcomes. Radiology. 2017;282:665–75.CrossRef Kim JH, Ko ES, Lim Y, Lee KS, Han BK, Ko EY, et al. Breast cancer heterogeneity: MR imaging texture analysis and survival outcomes. Radiology. 2017;282:665–75.CrossRef
26.
Zurück zum Zitat Moon SH, Kim J, Joung JG, Cha H, Park WY, Ahn JS, et al. Correlations between metabolic texture features, genetic heterogeneity, and mutation burden in patients with lung cancer. Eur J Nucl Med Mol Imaging. 2019;46:446–54.CrossRef Moon SH, Kim J, Joung JG, Cha H, Park WY, Ahn JS, et al. Correlations between metabolic texture features, genetic heterogeneity, and mutation burden in patients with lung cancer. Eur J Nucl Med Mol Imaging. 2019;46:446–54.CrossRef
27.
Zurück zum Zitat Lubner MG, Stabo N, Abel EJ, Del Rio AM, Pickhardt PJ. CT textural analysis of large primary renal cell carcinomas: pretreatment tumor heterogeneity correlates with histologic findings and clinical outcomes. AJR Am J Roentgenol. 2016;207:96–105.CrossRef Lubner MG, Stabo N, Abel EJ, Del Rio AM, Pickhardt PJ. CT textural analysis of large primary renal cell carcinomas: pretreatment tumor heterogeneity correlates with histologic findings and clinical outcomes. AJR Am J Roentgenol. 2016;207:96–105.CrossRef
28.
Zurück zum Zitat Yan L, Yang G, Cui J, Miao W, Wang Y, Zhao Y, et al. Radiomics analysis of contrast-enhanced CT predicts survival in clear cell renal cell carcinoma. Front Oncol. 2021;11:671420.CrossRef Yan L, Yang G, Cui J, Miao W, Wang Y, Zhao Y, et al. Radiomics analysis of contrast-enhanced CT predicts survival in clear cell renal cell carcinoma. Front Oncol. 2021;11:671420.CrossRef
29.
Zurück zum Zitat Ganeshan B, Goh V, Mandeville HC, Ng QS, Hoskin PJ, Miles KA. Non-small cell lung cancer: histopathologic correlates for texture parameters at CT. Radiology. 2013;266:326–36.CrossRef Ganeshan B, Goh V, Mandeville HC, Ng QS, Hoskin PJ, Miles KA. Non-small cell lung cancer: histopathologic correlates for texture parameters at CT. Radiology. 2013;266:326–36.CrossRef
30.
Zurück zum Zitat Segal E, Sirlin CB, Ooi C, Adler AS, Gollub J, Chen X, et al. Decoding global gene expression programs in liver cancer by noninvasive imaging. Nat Biotechnol. 2007;25:675–80.CrossRef Segal E, Sirlin CB, Ooi C, Adler AS, Gollub J, Chen X, et al. Decoding global gene expression programs in liver cancer by noninvasive imaging. Nat Biotechnol. 2007;25:675–80.CrossRef
31.
Zurück zum Zitat Park JE, Kim D, Kim HS, Park SY, Kim JY, Cho SJ, et al. Quality of science and reporting of radiomics in oncologic studies: room for improvement according to radiomics quality score and TRIPOD statement. Eur Radiol. 2020;30:523–36.CrossRef Park JE, Kim D, Kim HS, Park SY, Kim JY, Cho SJ, et al. Quality of science and reporting of radiomics in oncologic studies: room for improvement according to radiomics quality score and TRIPOD statement. Eur Radiol. 2020;30:523–36.CrossRef
32.
Zurück zum Zitat Ficarra V, Martignoni G, Lohse C, Novara G, Pea M, Cavalleri S, et al. External validation of the Mayo Clinic Stage, Size, Grade and Necrosis (SSIGN) score to predict cancer specific survival using a European series of conventional renal cell carcinoma. J Urol. 2006;175:1235–9.CrossRef Ficarra V, Martignoni G, Lohse C, Novara G, Pea M, Cavalleri S, et al. External validation of the Mayo Clinic Stage, Size, Grade and Necrosis (SSIGN) score to predict cancer specific survival using a European series of conventional renal cell carcinoma. J Urol. 2006;175:1235–9.CrossRef
Metadaten
Titel
The radiomics-based tumor heterogeneity adds incremental value to the existing prognostic models for predicting outcome in localized clear cell renal cell carcinoma: a multicenter study
verfasst von
Guangjie Yang
Pei Nie
Lei Yan
Mingxin Zhang
Yangyang Wang
Lianzi Zhao
Mingyao Li
Fei Xie
Haizhu Xie
Xianjun Li
Fawei Xiang
Nan Wang
Nan Cheng
Xia Zhao
Ning Wang
Yicong Wang
Chengcheng Chen
Canhua Yun
Jingjing Cui
Shaofeng Duan
Ran Zhang
Dapeng Hao
Ximing Wang
Zhenguang Wang
Haitao Niu
Publikationsdatum
28.03.2022
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nuclear Medicine and Molecular Imaging / Ausgabe 8/2022
Print ISSN: 1619-7070
Elektronische ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-022-05773-1

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