Novel Liquid Biomarkers and Innovative Imaging for Kidney Cancer Diagnosis: What Can Be Implemented in Our Practice Today? A Systematic Review of the Literature

Capitanio, 2019, Epidemiology of renal cell carcinoma, Eur Urol, 75, 74, 10.1016/j.eururo.2018.08.036 Welch, 2019, Epidemiologic signatures in cancer, N Engl J Med, 381, 1378, 10.1056/NEJMsr1905447 Patel, 2019, Clinical stage migration and survival for renal cell carcinoma in the United States, Eur Urol Oncol, 2, 343, 10.1016/j.euo.2018.08.023 Rossi SH, Klatte T, Usher-Smith JA, et al. A decision analysis evaluating screening for kidney cancer using focused renal ultrasound. Eur Urol Focus. In press. https://doi.org/10.1016/j.euf.2019.09.002. Welch, 2018, Regional variation of computed tomographic imaging in the United States and the risk of nephrectomy, JAMA Intern Med, 178, 221, 10.1001/jamainternmed.2017.7508 Kim, 2019, Association of prevalence of benign pathologic findings after partial nephrectomy with preoperative imaging patterns in the United States from 2007 to 2014, JAMA Surg, 154, 225, 10.1001/jamasurg.2018.4602 Campi, 2020, Triggers for delayed intervention in patients with small renal masses undergoing active surveillance: a systematic review, Minerva Urol Nefrol, 72, 389, 10.23736/S0393-2249.20.03870-9 Shah, 2018, The temporal association of robotic surgical diffusion with overtreatment of the small renal mass, J Urol, 200, 981, 10.1016/j.juro.2018.05.081 Ljungberg, 2020 Campbell, 2017, Renal mass and localized renal cancer: AUA guideline, J Urol, 198, 520, 10.1016/j.juro.2017.04.100 Knoll, 2018, Key steps in conducting systematic reviews for underpinning clinical practice guidelines: methodology of the European Association of Urology, Eur Urol, 73, 290, 10.1016/j.eururo.2017.08.016 Liberati, 2009, The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration, J Clin Epidemiol, 62, e1, 10.1016/j.jclinepi.2009.06.006 Altman, 2012, Reporting recommendations for tumor marker prognostic studies (REMARK): explanation and elaboration, BMC Med, 10, 51, 10.1186/1741-7015-10-51 Whiting, 2011, QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies, Ann Intern Med, 155, 529, 10.7326/0003-4819-155-8-201110180-00009 Butz, 2016, Exosomal microRNAs are diagnostic biomarkers and can mediate cell-cell communication in renal cell carcinoma, Eur Urol Focus, 2, 210, 10.1016/j.euf.2015.11.006 Horstmann, 2017, Evaluation of plasmatic kisspetin-10 as a biomarker for malignancy and subtype differentiation in small renal tumours, Urol Int, 98, 177, 10.1159/000452108 Mytsyk, 2018, MicroRNA-15a expression measured in urine samples as a potential biomarker of renal cell carcinoma, Int Urol Nephrol, 50, 851, 10.1007/s11255-018-1841-x Kim, 2019, Prolyl hydroxylase-3 is a novel renal cell carcinoma biomarker, Investig Clin Urol, 60, 425, 10.4111/icu.2019.60.6.425 Kushlinskii, 2019, Kidney injury molecule-1 (KIM-1) in blood plasma of patients with clear-cell carcinoma, Bull Exp Biol Med, 167, 388, 10.1007/s10517-019-04533-w Liu, 2019, Urine metabolomics for renal cell carcinoma (RCC) prediction: tryptophan metabolism as an important pathway in RCC, Front Oncol, 9, 663, 10.3389/fonc.2019.00663 Yu, 2017, Texture analysis as a radiomic marker for differentiating renal tumors, Abdom Radiol, 42, 2470, 10.1007/s00261-017-1144-1 Varghese, 2018, Differentiation of predominantly solid enhancing lipid-poor renal cell masses by use of contrast-enhanced CT: evaluating the role of texture in tumor subtyping, Am J Roentgenol, 211, W288, 10.2214/AJR.18.19551 Li, 2018, Subtype differentiation of small (≤ 4 cm) solid renal mass using volumetric histogram analysis of DWI at 3-T MRI, Am J Roentgenol, 211, 614, 10.2214/AJR.17.19278 Ding, 2019, Differentiating between malignant and benign renal tumors: do IVIM and diffusion kurtosis imaging perform better than DWI?, Eur Radiol, 29, 6930, 10.1007/s00330-019-06240-6 Coy, 2019, Deep learning and radiomics: the utility of Google TensorFlow™ Inception in classifying clear cell renal cell carcinoma and oncocytoma on multiphasic CT, Abdom Radiol, 44, 2009, 10.1007/s00261-019-01929-0 Zabihollahy, 2020, Automated classification of solid renal masses on contrast-enhanced computed tomography images using convolutional neural network with decision fusion, Eur Radiol, 30, 5183, 10.1007/s00330-020-06787-9 Tanaka, 2020, Differentiation of small (≤ 4 cm) renal masses on multiphase contrast-enhanced CT by deep learning, Am J Roentgenol, 214, 605, 10.2214/AJR.19.22074 Sun, 2020, Radiologic-radiomic machine learning models for differentiation of benign and malignant solid renal masses: comparison with expert-level radiologists, Am J Roentgenol, 214, W44, 10.2214/AJR.19.21617 Said, 2020, Characterization of solid renal neoplasms using MRI-based quantitative radiomics features, Abdom Radiol, 45, 2840, 10.1007/s00261-020-02540-4 Fedorko, 2015, Combination of miR-378 and miR-210 serum levels enables sensitive detection of renal cell carcinoma, Int J Mol Sci, 16, 23382, 10.3390/ijms161023382 Wang, 2015, A panel of five serum miRNAs as a potential diagnostic tool for early-stage renal cell carcinoma, Sci Rep, 5, 7610, 10.1038/srep07610 Nuerrula, 2015, Differential expression and clinical significance of serum protein among patients with clear-cell renal cell carcinoma, Cancer Biomarkers, 15, 485, 10.3233/CBM-150490 Iliev, 2016, Expression levels of PIWI-interacting RNA, piR-823, are deregulated in tumor tissue, blood serum and urine of patients with renal cell carcinoma, Anticancer Res, 36, 6419, 10.21873/anticanres.11239 Lu, 2016, Diagnostic and prognostic potential of circulating cell-free genomic and mitochondrial DNA fragments in clear cell renal cell carcinoma patients, Clin Chim Acta, 452, 109, 10.1016/j.cca.2015.11.009 Niedworok, 2016, Validation of the diagnostic and prognostic relevance of serum MMP-7 levels in renal cell cancer by using a novel automated fluorescent immunoassay method, Int Urol Nephrol, 48, 355, 10.1007/s11255-015-1185-8 Wu, 2016, A serum-circulating long noncoding RNA signature can discriminate between patients with clear cell renal cell carcinoma and healthy controls, Oncogenesis, 5, e192, 10.1038/oncsis.2015.48 Orywal, 2016, The diagnostic significance of serum alcohol dehydrogenase isoenzymes and aldehyde dehydrogenase activity in renal cell cancer patients, Exp Mol Pathol, 100, 416, 10.1016/j.yexmp.2016.04.001 Lou, 2017, miR-144-3p as a novel plasma diagnostic biomarker for clear cell renal cell carcinoma, Urol Oncol, 35, 10.1016/j.urolonc.2016.07.012 Chanudet, 2017, Large-scale genome-wide screening of circulating microRNAs in clear cell renal cell carcinoma reveals specific signatures in late-stage disease, Int J Cancer, 141, 1730, 10.1002/ijc.30845 Lee, 2017, Combination of serum histidine and plasma tryptophan as a potential biomarker to detect clear cell renal cell carcinoma, J Transl Med, 15, 72, 10.1186/s12967-017-1178-8 Dong, 2017, Serum level of ANGPTL4 as a potential biomarker in renal cell carcinoma, Urol Oncol, 35, 279, 10.1016/j.urolonc.2016.12.017 Li, 2017, Detection of urinary cell-free miR-210 as a potential tool of liquid biopsy for clear cell renal cell carcinoma, Urol Oncol, 35, 294, 10.1016/j.urolonc.2016.12.007 Fedorko, 2017, Detection of let-7 miRNAs in urine supernatant as potential diagnostic approach in non-metastatic clear-cell renal cell carcinoma, Biochem Med, 27, 411, 10.11613/BM.2017.043 Yang, 2018, Detection of urinary survivin using a magnetic particles-based chemiluminescence immunoassay for the preliminary diagnosis of bladder cancer and renal cell carcinoma combined with LAPTM4B, Oncol Lett, 15, 7923 Gatto, 2018, Plasma glycosaminoglycans as diagnostic and prognostic biomarkers in surgically treated renal cell carcinoma, Eur Urol Oncol, 1, 364, 10.1016/j.euo.2018.04.015 Heinemann, 2018, Serum miR-122-5p and miR-206 expression: non-invasive prognostic biomarkers for renal cell carcinoma, Clin Epigenet, 10, 11, 10.1186/s13148-018-0444-9 Zhang, 2018, MicroRNAs in serum exosomes as potential biomarkers in clear-cell renal cell carcinoma, Eur Urol Focus, 4, 412, 10.1016/j.euf.2016.09.007 Yamamoto, 2018, Increased level and fragmentation of plasma circulating cell-free DNA are diagnostic and prognostic markers for renal cell carcinoma, Oncotarget, 9, 20467, 10.18632/oncotarget.24943 Chen, 2018, miR-224/miR-141 ratio as a novel diagnostic biomarker in renal cell carcinoma, Oncol Lett, 16, 1666 Kim, 2018, Clinical validation of serum endocan (ESM-1) as a potential biomarker in patients with renal cell carcinoma, Oncotarget, 9, 662, 10.18632/oncotarget.23087 Wang, 2019, Circulating miR-200a is a novel molecular biomarker for early-stage renal cell carcinoma, ExRNA, 1, 25, 10.1186/s41544-019-0023-z Song, 2019, Urinary exosome miR-30c-5p as a biomarker of clear cell renal cell carcinoma that inhibits progression by targeting HSPA5, J Cell Mol Med, 23, 6755, 10.1111/jcmm.14553 Nuzzo, 2020, Detection of renal cell carcinoma using plasma and urine cell-free DNA methylomes, Nat Med, 26, 1041, 10.1038/s41591-020-0933-1 Outeiro-Pinho, 2020, MicroRNA-30a-5pme: a novel diagnostic and prognostic biomarker for clear cell renal cell carcinoma in tissue and urine samples, J Exp Clin Cancer Res, 39, 98, 10.1186/s13046-020-01600-3 Huang, 2020, A Three-microRNA panel in serum: serving as a potential diagnostic biomarker for renal cell carcinoma, Pathol Oncol Res, 26, 2425, 10.1007/s12253-020-00842-y Lu, 2015, Differentiation of renal tumor histotypes: usefulness of quantitative analysis of contrast-enhanced ultrasound, Am J Roentgenol, 205, W335, 10.2214/AJR.14.14204 Jhaveri, 2015, Predictive value of chemical-shift MRI in distinguishing clear cell renal cell carcinoma from non-clear cell renal cell carcinoma and minimal-fat angiomyolipoma, Am J Roentgenol, 205, W79, 10.2214/AJR.14.13245 Hodgdon, 2015, Can quantitative CT texture analysis be used to differentiate fat-poor renal angiomyolipoma from renal cell carcinoma on unenhanced CT images?, Radiology, 276, 787, 10.1148/radiol.2015142215 Atri, 2015, Accuracy of contrast-enhanced US for differentiating benign from malignant solid small renal masses, Radiology, 276, 900, 10.1148/radiol.2015140907 Nakajima, 2016, Clinical role of early dynamic FDG-PET/CT for the evaluation of renal cell carcinoma, Eur Radiol, 26, 1852, 10.1007/s00330-015-4026-3 Lubner, 2016, CT textural analysis of large primary renal cell carcinomas: pretreatment tumor heterogeneity correlates with histologic findings and clinical outcomes, Am J Roentgenol, 207, 96, 10.2214/AJR.15.15451 Li, 2016, Quantitative evaluation of contrast-enhanced ultrasound for differentiation of renal cell carcinoma subtypes and angiomyolipoma, Eur J Radiol, 85, 795, 10.1016/j.ejrad.2016.01.009 Kim, 2016, Differentiation of clear cell renal cell carcinoma from other subtypes and fat-poor angiomyolipoma by use of quantitative enhancement measurement during three-phase MDCT, Am J Roentgenol, 206, W21, 10.2214/AJR.15.14666 Gorin, 2016, Prospective evaluation of 99mTc-sestamibi SPECT/CT for the diagnosis of renal oncocytomas and hybrid oncocytic/chromophobe tumors, Eur Urol, 69, 413, 10.1016/j.eururo.2015.08.056 Ding, 2016, Comparison of biexponential and monoexponential model of diffusion-weighted imaging for distinguishing between common renal cell carcinoma and fat poor angiomyolipoma, Korean J Radiol, 17, 853, 10.3348/kjr.2016.17.6.853 Nakajima, 2017, Evaluation of renal cell carcinoma histological subtype and Fuhrman grade using 18F-fluorodeoxyglucose-positron emission tomography/computed tomography, Eur Radiol, 27, 4866, 10.1007/s00330-017-4875-z Canvasser, 2017, Diagnostic accuracy of multiparametric magnetic resonance imaging to identify clear cell renal cell carcinoma in cT1a renal masses, J Urol, 198, 780, 10.1016/j.juro.2017.04.089 Zhu, 2018, Value of intravoxel incoherent motion in assessment of pathological grade of clear cell renal cell carcinoma, Acta Radiol, 59, 121, 10.1177/0284185117716702 Wei, 2018, Analysis of dual energy spectral CT and pathological grading of clear cell renal cell carcinoma (ccRCC), PLoS One, 13, 10.1371/journal.pone.0195699 Shu, 2018, Clear cell renal cell carcinoma: CT-based radiomics features for the prediction of Fuhrman grade, Eur J Radiol, 109, 8, 10.1016/j.ejrad.2018.10.005 Kocak, 2018, Textural differences between renal cell carcinoma subtypes: machine learning-based quantitative computed tomography texture analysis with independent external validation, Eur J Radiol, 107, 149, 10.1016/j.ejrad.2018.08.014 Ding, 2018, CT-based radiomic model predicts high grade of clear cell renal cell carcinoma, Eur J Radiol, 103, 51, 10.1016/j.ejrad.2018.04.013 Dai, 2018, Differentiation of renal cell carcinoma subtypes with different iodine quantification methods using single-phase contrast-enhanced dual-energy CT: areal vs. volumetric analyses, Abdom Radiol, 43, 672, 10.1007/s00261-017-1253-x Shu, 2019, Clear cell renal cell carcinoma: machine learning-based computed tomography radiomics analysis for the prediction of WHO/ISUP grade, Eur J Radiol, 121, 10.1016/j.ejrad.2019.108738 Kocak, 2019, Unenhanced CT texture analysis of clear cell renal cell carcinomas: a machine learning-based study for predicting histopathologic nuclear grade, Am J Roentgenol, 212, W1 Johnson, 2019, Diagnostic performance of prospectively assigned clear cell likelihood scores (ccLS) in small renal masses at multiparametric magnetic resonance imaging, Urol Oncol, 37, 941, 10.1016/j.urolonc.2019.07.023 Feng, 2019, CT texture analysis: a potential tool for predicting the Fuhrman grade of clear-cell renal carcinoma, Cancer Imaging, 19, 6, 10.1186/s40644-019-0195-7 Deng, 2019, CT texture analysis in the differentiation of major renal cell carcinoma subtypes and correlation with Fuhrman grade, Eur Radiol, 29, 6922, 10.1007/s00330-019-06260-2 Cui, 2019, Differentiation of renal angiomyolipoma without visible fat from renal cell carcinoma by machine learning based on whole-tumor computed tomography texture features, Acta Radiol, 60, 1543, 10.1177/0284185119830282 Cai, 2019, Diagnostic performance of ultrasound shear wave elastography in solid small (≤4 cm) renal parenchymal masses, Ultrasound Med Biol, 45, 2328, 10.1016/j.ultrasmedbio.2019.05.010 Zhou, 2020, Development and external validation of radiomics approach for nuclear grading in clear cell renal cell carcinoma, Ann Surg Oncol, 27, 4057, 10.1245/s10434-020-08255-6 Wang, 2020, Differentiation of renal cell carcinoma subtypes through MRI-based radiomics analysis, Eur Radiol, 30, 5738, 10.1007/s00330-020-06896-5 Steinberg RL, Rasmussen RG, Johnson BA, et al. Prospective performance of clear cell likelihood scores (ccLS) in renal masses evaluated with multiparametric magnetic resonance imaging. Eur Radiol. In press. https://doi.org/10.1007/s00330-020-07093-0. Marcon, 2020, Papillary vs clear cell renal cell carcinoma. Differentiation and grading by iodine concentration using DECT-correlation with microvascular density, Eur Radiol, 30, 1, 10.1007/s00330-019-06298-2 Lin, 2020, A CT-based deep learning model for predicting the nuclear grade of clear cell renal cell carcinoma, Eur J Radiol, 129, 10.1016/j.ejrad.2020.109079 Li, 2020, Multiparametric MRI radiomic model for preoperative predicting WHO/ISUP nuclear grade of clear cell renal cell carcinoma, J Magn Reson Imaging, 52, 1557, 10.1002/jmri.27182 Dwivedi DK, Xi Y, Kapur P, et al. Magnetic resonance imaging radiomics analyses for prediction of high-grade histology and necrosis in clear cell renal cell carcinoma: preliminary experience. Clin Genitourin Cancer. In press. https://doi.org/10.1016/j.clgc.2020.05.011. Schaefer, 2010, Diagnostic, prognostic and therapeutic implications of microRNAs in urologic tumors, Nat Rev Urol, 7, 286, 10.1038/nrurol.2010.45 Thery, 2002, Exosomes: composition, biogenesis and function, Nat Rev Immunol, 2, 569, 10.1038/nri855 Ji, 2013, The Kiss-1/Kiss-1R complex as a negative regulator of cell motility and cancer metastasis (review), Int J Mol Med, 32, 747, 10.3892/ijmm.2013.1472 Schödel, 2016, Hypoxia, hypoxia-inducible transcription factors, and renal cancer, Eur Urol, 69, 646, 10.1016/j.eururo.2015.08.007 Tanaka, 2011, Autoantibody against hypoxia-inducible factor prolyl hydroxylase-3 is a potential serological marker for renal cell carcinoma, J Cancer Res Clin Oncol, 137, 789, 10.1007/s00432-010-0940-6 Morrissey, 2011, Sensitivity and specificity of urinary neutrophil gelatinase-associated lipocalin and kidney injury molecule-1 for the diagnosis of renal cell carcinoma, Am J Nephrol, 34, 391, 10.1159/000330851 Zhang, 2014, Urine kidney injury molecule-1: a potential non-invasive biomarker for patients with renal cell carcinoma, Int Urol Nephrol, 46, 379, 10.1007/s11255-013-0522-z Kim, 2011, Urine metabolomic analysis identifies potential biomarkers and pathogenic pathways in kidney cancer, Omics, 15, 293, 10.1089/omi.2010.0094 Monteiro, 2016, Nuclear magnetic resonance metabolomics reveals an excretory metabolic signature of renal cell carcinoma, Sci Rep, 6, 37275, 10.1038/srep37275 Parekh, 2019, Deep learning and radiomics in precision medicine, Expert Rev Precis Med Drug Dev, 4, 59, 10.1080/23808993.2019.1585805 Capitanio U, Pepe G, Incerti E, et al. The role of 18F-FAZA PET/CT in detecting lymph node metastases in renal cell carcinoma patients: a prospective pilot trial. Eur J Nucl Med Mol Imaging. In press. https://doi.org/10.1007/s00259-020-04936-2. Alessandrino, 2019, Radiogenomics in renal cell carcinoma, Abdom Radiol, 44, 1990, 10.1007/s00261-018-1624-y Finelli, 2020, Small renal mass surveillance: histology-specific growth rates in a biopsy-characterized cohort, Eur Urol, 78, 460, 10.1016/j.eururo.2020.06.053