Skip to main content
Top
Published in: Insights into Imaging 1/2023

Open Access 01-12-2023 | Kidney Cancer | Original Article

A multi-model based on radiogenomics and deep learning techniques associated with histological grade and survival in clear cell renal cell carcinoma

Authors: Shihui Wang, Chao Zhu, Yidong Jin, Hongqing Yu, Lili Wu, Aijuan Zhang, Beibei Wang, Jian Zhai

Published in: Insights into Imaging | Issue 1/2023

Login to get access

Abstract

Objectives

This study aims to evaluate the efficacy of multi-model incorporated by radiomics, deep learning, and transcriptomics features for predicting pathological grade and survival in patients with clear cell renal cell carcinoma (ccRCC).

Methods

In this study, data were collected from 177 ccRCC patients, including radiomics features, deep learning (DL) features, and RNA sequencing data. Diagnostic models were then created using these data through least absolute shrinkage and selection operator (LASSO) analysis. Additionally, a multi-model was developed by combining radiomics, DL, and transcriptomics features. The prognostic performance of the multi-model was evaluated based on progression-free survival (PFS) and overall survival (OS) outcomes, assessed using Harrell’s concordance index (C-index). Furthermore, we conducted an analysis to investigate the relationship between the multi-model and immune cell infiltration.

Results

The multi-model demonstrated favorable performance in discriminating pathological grade, with area under the ROC curve (AUC) values of 0.946 (95% CI: 0.912–0.980) and 0.864 (95% CI: 0.734–0.994) in the training and testing cohorts, respectively. Additionally, it exhibited statistically significant prognostic performance for predicting PFS and OS. Furthermore, the high-grade group displayed a higher abundance of immune cells compared to the low-grade group.

Conclusions

The multi-model incorporated radiomics, DL, and transcriptomics features demonstrated promising performance in predicting pathological grade and prognosis in patients with ccRCC.

Critical relevance statement

We developed a multi-model to predict the grade and survival in clear cell renal cell carcinoma and explored the molecular biological significance of the multi-model of different histological grades.

Key points

1. The multi-model achieved an AUC of 0.864 for assessing pathological grade.
2. The multi-model exhibited an association with survival in ccRCC patients.
3. The high-grade group demonstrated a greater abundance of immune cells.

Graphical Abstract

Appendix
Available only for authorised users
Literature
2.
go back to reference Dagher J, Delahunt B, Rioux-Leclercq N et al (2017) Clear cell renal cell carcinoma: validation of World Health Organization/International Society of Urological Pathology grading. Histopathology 71:918–925CrossRefPubMed Dagher J, Delahunt B, Rioux-Leclercq N et al (2017) Clear cell renal cell carcinoma: validation of World Health Organization/International Society of Urological Pathology grading. Histopathology 71:918–925CrossRefPubMed
3.
go back to reference El Khoury LY, Fu S, Hlady RA et al (2021) 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 13:12CrossRefPubMedPubMedCentral El Khoury LY, Fu S, Hlady RA et al (2021) 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 13:12CrossRefPubMedPubMedCentral
4.
go back to reference Delahunt B, Eble JN, Egevad L, Samaratunga H (2019) Grading of renal cell carcinoma. Histopathology 74:4–17CrossRefPubMed Delahunt B, Eble JN, Egevad L, Samaratunga H (2019) Grading of renal cell carcinoma. Histopathology 74:4–17CrossRefPubMed
5.
go back to reference Kim H, Inomoto C, Uchida T et al (2018) Verification of the International Society of Urological Pathology recommendations in Japanese patients with clear cell renal cell carcinoma. Int J Oncol 52:1139–1148PubMedPubMedCentral Kim H, Inomoto C, Uchida T et al (2018) Verification of the International Society of Urological Pathology recommendations in Japanese patients with clear cell renal cell carcinoma. Int J Oncol 52:1139–1148PubMedPubMedCentral
6.
go back to reference Halverson SJ, Kunju LP, Bhalla R et al (2013) Accuracy of determining small renal mass management with risk stratified biopsies: confirmation by final pathology. J Urol 189:441–446CrossRefPubMed Halverson SJ, Kunju LP, Bhalla R et al (2013) Accuracy of determining small renal mass management with risk stratified biopsies: confirmation by final pathology. J Urol 189:441–446CrossRefPubMed
7.
go back to reference Zhou H, Mao H, Dong D et al (2020) Development and external validation of radiomics approach for nuclear grading in clear cell renal cell carcinoma. Ann Surg Oncol 27:4057–4065CrossRefPubMed Zhou H, Mao H, Dong D et al (2020) Development and external validation of radiomics approach for nuclear grading in clear cell renal cell carcinoma. Ann Surg Oncol 27:4057–4065CrossRefPubMed
8.
go back to reference Dwivedi DK, Xi Y, Kapur P et al (2021) Magnetic resonance imaging radiomics analyses for prediction of high-grade histology and necrosis in clear cell renal cell carcinoma: preliminary experience. Clin Genitourin Cancer 19:12-21.e11CrossRefPubMed Dwivedi DK, Xi Y, Kapur P et al (2021) Magnetic resonance imaging radiomics analyses for prediction of high-grade histology and necrosis in clear cell renal cell carcinoma: preliminary experience. Clin Genitourin Cancer 19:12-21.e11CrossRefPubMed
9.
go back to reference Wan F, Zhu Y, Han C et al (2017) Identification and validation of an eight-gene expression signature for predicting high Fuhrman grade renal cell carcinoma. Int J Cancer 140:1199–1208CrossRefPubMed Wan F, Zhu Y, Han C et al (2017) Identification and validation of an eight-gene expression signature for predicting high Fuhrman grade renal cell carcinoma. Int J Cancer 140:1199–1208CrossRefPubMed
10.
go back to reference Cui E, Li Z, Ma C et al (2020) Predicting the ISUP grade of clear cell renal cell carcinoma with multiparametric MR and multiphase CT radiomics. Eur Radiol 30:2912–2921CrossRefPubMed Cui E, Li Z, Ma C et al (2020) Predicting the ISUP grade of clear cell renal cell carcinoma with multiparametric MR and multiphase CT radiomics. Eur Radiol 30:2912–2921CrossRefPubMed
11.
go back to reference Zhao Y, Wu C, Li W et al (2021) 2-[(18)F]FDG PET/CT parameters associated with WHO/ISUP grade in clear cell renal cell carcinoma. Eur J Nucl Med Mol Imaging 48:570–579CrossRefPubMed Zhao Y, Wu C, Li W et al (2021) 2-[(18)F]FDG PET/CT parameters associated with WHO/ISUP grade in clear cell renal cell carcinoma. Eur J Nucl Med Mol Imaging 48:570–579CrossRefPubMed
12.
go back to reference Demirjian NL, Varghese BA, Cen SY et al (2022) CT-based radiomics stratification of tumor grade and TNM stage of clear cell renal cell carcinoma. Eur Radiol 32:2552–2563CrossRefPubMed Demirjian NL, Varghese BA, Cen SY et al (2022) CT-based radiomics stratification of tumor grade and TNM stage of clear cell renal cell carcinoma. Eur Radiol 32:2552–2563CrossRefPubMed
13.
go back to reference Hussain MA, Hamarneh G, Garbi R (2021) Learnable image histograms-based deep radiomics for renal cell carcinoma grading and staging. Comput Med Imaging Graph 90:101924CrossRefPubMed Hussain MA, Hamarneh G, Garbi R (2021) Learnable image histograms-based deep radiomics for renal cell carcinoma grading and staging. Comput Med Imaging Graph 90:101924CrossRefPubMed
14.
go back to reference Lin P, Wen DY, Chen L et al (2020) A radiogenomics signature for predicting the clinical outcome of bladder urothelial carcinoma. Eur Radiol 30:547–557CrossRefPubMed Lin P, Wen DY, Chen L et al (2020) A radiogenomics signature for predicting the clinical outcome of bladder urothelial carcinoma. Eur Radiol 30:547–557CrossRefPubMed
15.
go back to reference Clark K, Vendt B, Smith K et al (2013) The Cancer Imaging Archive (TCIA): maintaining and operating a public information repository. J Digit Imaging 26:1045–1057CrossRefPubMedPubMedCentral Clark K, Vendt B, Smith K et al (2013) The Cancer Imaging Archive (TCIA): maintaining and operating a public information repository. J Digit Imaging 26:1045–1057CrossRefPubMedPubMedCentral
16.
go back to reference Cancer Genome Atlas Research Network (2013) Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499(7456):43–49CrossRef Cancer Genome Atlas Research Network (2013) Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499(7456):43–49CrossRef
17.
go back to reference Zheng Z, Chen Z, Xie Y, Zhong Q, Xie W (2021) Development and validation of a CT-based nomogram for preoperative prediction of clear cell renal cell carcinoma grades. Eur Radiol 31:6078–6086CrossRefPubMed Zheng Z, Chen Z, Xie Y, Zhong Q, Xie W (2021) Development and validation of a CT-based nomogram for preoperative prediction of clear cell renal cell carcinoma grades. Eur Radiol 31:6078–6086CrossRefPubMed
18.
go back to reference Millet I, Curros F, Serre I, Taourel P, Thuret R (2012) Can renal biopsy accurately predict histological subtype and Fuhrman grade of renal cell carcinoma? J Urol 188:1690–1694CrossRefPubMed Millet I, Curros F, Serre I, Taourel P, Thuret R (2012) Can renal biopsy accurately predict histological subtype and Fuhrman grade of renal cell carcinoma? J Urol 188:1690–1694CrossRefPubMed
19.
go back to reference Parker WP, Cheville JC, Frank I et al (2017) Application of the Stage, Size, Grade, and Necrosis (SSIGN) score for clear cell renal cell carcinoma in contemporary patients. Eur Urol 71:665–673CrossRefPubMed Parker WP, Cheville JC, Frank I et al (2017) Application of the Stage, Size, Grade, and Necrosis (SSIGN) score for clear cell renal cell carcinoma in contemporary patients. Eur Urol 71:665–673CrossRefPubMed
20.
go back to reference Zigeuner R, Hutterer G, Chromecki T et al (2010) External validation of the Mayo Clinic stage, size, grade, and necrosis (SSIGN) score for clear-cell renal cell carcinoma in a single European centre applying routine pathology. Eur Urol 57:102–109CrossRefPubMed Zigeuner R, Hutterer G, Chromecki T et al (2010) External validation of the Mayo Clinic stage, size, grade, and necrosis (SSIGN) score for clear-cell renal cell carcinoma in a single European centre applying routine pathology. Eur Urol 57:102–109CrossRefPubMed
21.
go back to reference Xu L, Yang C, Zhang F et al (2022) Deep learning using CT Images to grade clear cell renal cell carcinoma: development and validation of a prediction model. Cancers (Basel) 14(11):2574CrossRefPubMed Xu L, Yang C, Zhang F et al (2022) Deep learning using CT Images to grade clear cell renal cell carcinoma: development and validation of a prediction model. Cancers (Basel) 14(11):2574CrossRefPubMed
22.
go back to reference Feng Z, Lou S, Zhang L et al (2019) New preoperative nomogram using the centrality index to predict high nuclear grade clear cell renal carcinoma. Cancer Manag Res 11:10921–10928CrossRefPubMedPubMedCentral Feng Z, Lou S, Zhang L et al (2019) New preoperative nomogram using the centrality index to predict high nuclear grade clear cell renal carcinoma. Cancer Manag Res 11:10921–10928CrossRefPubMedPubMedCentral
23.
go back to reference Adams LC, Jurmeister P, Ralla B et al (2019) Assessment of the extracellular volume fraction for the grading of clear cell renal cell carcinoma: first results and histopathological findings. Eur Radiol 29:5832–5843CrossRefPubMed Adams LC, Jurmeister P, Ralla B et al (2019) Assessment of the extracellular volume fraction for the grading of clear cell renal cell carcinoma: first results and histopathological findings. Eur Radiol 29:5832–5843CrossRefPubMed
24.
go back to reference Zeng H, Chen L, Wang M, Luo Y, Huang Y, Ma X (2021) Integrative radiogenomics analysis for predicting molecular features and survival in clear cell renal cell carcinoma. Aging (Albany NY) 13:9960–9975CrossRefPubMed Zeng H, Chen L, Wang M, Luo Y, Huang Y, Ma X (2021) Integrative radiogenomics analysis for predicting molecular features and survival in clear cell renal cell carcinoma. Aging (Albany NY) 13:9960–9975CrossRefPubMed
25.
go back to reference Khodabakhshi Z, Amini M, Mostafaei S et al (2021) Overall survival prediction in renal cell carcinoma patients using computed tomography radiomic and clinical information. J Digit Imaging 34:1086–1098CrossRefPubMedPubMedCentral Khodabakhshi Z, Amini M, Mostafaei S et al (2021) Overall survival prediction in renal cell carcinoma patients using computed tomography radiomic and clinical information. J Digit Imaging 34:1086–1098CrossRefPubMedPubMedCentral
26.
go back to reference Na X, Duan HO, Messing EM et al (2003) Identification of the RNA polymerase II subunit hsRPB7 as a novel target of the von Hippel-Lindau protein. EMBO J 22:4249–4259CrossRefPubMedPubMedCentral Na X, Duan HO, Messing EM et al (2003) Identification of the RNA polymerase II subunit hsRPB7 as a novel target of the von Hippel-Lindau protein. EMBO J 22:4249–4259CrossRefPubMedPubMedCentral
27.
go back to reference Şenbabaoğlu Y, Gejman RS, Winer AG et al (2016) Tumor immune microenvironment characterization in clear cell renal cell carcinoma identifies prognostic and immunotherapeutically relevant messenger RNA signatures. Genome Biol 17:231CrossRefPubMedPubMedCentral Şenbabaoğlu Y, Gejman RS, Winer AG et al (2016) Tumor immune microenvironment characterization in clear cell renal cell carcinoma identifies prognostic and immunotherapeutically relevant messenger RNA signatures. Genome Biol 17:231CrossRefPubMedPubMedCentral
28.
go back to reference Ferrall-Fairbanks MC, Chakiryan NH, Chobrutskiy BI et al (2022) Quantification of T- and B-cell immune receptor distribution diversity characterizes immune cell infiltration and lymphocyte heterogeneity in clear cell renal cell carcinoma. Cancer Res 82:929–942CrossRefPubMedPubMedCentral Ferrall-Fairbanks MC, Chakiryan NH, Chobrutskiy BI et al (2022) Quantification of T- and B-cell immune receptor distribution diversity characterizes immune cell infiltration and lymphocyte heterogeneity in clear cell renal cell carcinoma. Cancer Res 82:929–942CrossRefPubMedPubMedCentral
Metadata
Title
A multi-model based on radiogenomics and deep learning techniques associated with histological grade and survival in clear cell renal cell carcinoma
Authors
Shihui Wang
Chao Zhu
Yidong Jin
Hongqing Yu
Lili Wu
Aijuan Zhang
Beibei Wang
Jian Zhai
Publication date
01-12-2023
Publisher
Springer Vienna
Published in
Insights into Imaging / Issue 1/2023
Electronic ISSN: 1869-4101
DOI
https://doi.org/10.1186/s13244-023-01557-9

Other articles of this Issue 1/2023

Insights into Imaging 1/2023 Go to the issue