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A new survival model based on ferroptosis-related genes (FRGS) for prognostic prediction in bladder cancer
Nuevo modelo pronóstico de supervivencia del cáncer de vejiga basado en los genes vinculados a la ferroptosis (FRGS)
Yue Yanga,b, Haifeng Hua, Lin Chena, Hanchao Zhanga,b, Jin Yanga,
Corresponding author
yyjakejerry@163.com

Corresponding author.
a Urological Department, The Affiliated Hospital of Chengdu University, Chengdu, Sichuan, China
b Medical College of Soochow University, Suzhou, Jiangsu, China
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Bladder cancer &#40;BLCA&#41;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;2</span></a> is the ninth most common urinary malignancy and it accounts for an estimated 500&#44;000 new cases and 200&#44;000 deaths worldwide&#46; It represents a spectrum of diseases&#44; from noninvasive tumors managed transurethral resection&#44; to aggressive or advanced-stage disease that requires radical cystectomy&#44; immunotherapy&#44; chemotherapy&#44; or multimodal and invasive treatment&#46; However&#44; treatment for BLCA had seen little progress until recently&#44; thus there is a lot to do&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Ferroptosis&#44; a new type of programmed cell death&#44; is different from those of typical cell death processes&#46; It was activated by the accumulation of iron-dependent lipid hydroperoxides and leads to cytological changes to cell death in the end&#46; As the researches of ferroptosis had rapidly increased&#44; present studies<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;4</span></a> have revealed its complex biological function in various human diseases such as degenerative disease&#44; acute kidney injury&#46; In addition&#44; ferroptosis was also demonstrated that it played an important role in suppressing tumor growth and progression&#44;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> thus it could develop a potentially beneficial therapy for cancers&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Several previous studies<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">6&#8211;8</span></a> had already indicated that ferroptosis was correlated with BLCA&#44; but lacked lucubrating&#46; Recently&#44; Jasim<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> reported a development of novel tumor-targeted conjugated polymer nanoparticles &#40;CPNPs&#41; carrying iron for chemodynamic therapy &#40;CDT&#41;&#44; which killed tumor cell through ferroptosis&#44; had an excellent targeting to tumor cells and efficacy&#44; speci&#64257;cally for bladder tumor cells&#46; Therefore&#44; we conducted this study to explore the ferroptosis-related genes&#8217; biological function in BLCA&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Ferroptosis-related gene expression in BLCA</span><p id="par0020" class="elsevierStylePara elsevierViewall">We downloaded the cancer genome atlas &#40;TCGA&#41; dataset &#40;<a href="https://portal.gdc.cancer.gov/">https&#58;&#47;&#47;portal&#46;gdc&#46;cancer&#46;gov&#47;</a>&#41; in January 2020&#44; in which the method of acquisition and application complied with the guidelines and policies&#46; 402 cases of bladder cancer were included &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#44; and raw counts of RNA-sequencing data &#40;level 3&#41; and corresponding clinical information were also obtained&#46; We filtered out 25 ferroptosis-related genes that are derived from Ze-Xian Liu et al&#46;&#39;s<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> systematic analysis of the aberrances and functional implications of ferroptosis in cancer&#46; We explored the expression distribution of ferroptosis-related mRNA&#44; ferroptosis-mRNA&#8217;s relationship&#44; and heat map of ferroptosis-related gene expression in bladder tumor tissues and normal tissues&#46; All the above analysis methods and R package were implemented by R foundation for statistical computing &#40;2020&#41; version 4&#46;0&#46;3 and software packages ggplot2 and pheatmap&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Survival analysis</span><p id="par0025" class="elsevierStylePara elsevierViewall">The KM survival analysis with the log-rank test was also used to compare the survival difference of 25 ferroptosis-related gene expressions in the BLCA from the TCGA dataset&#46; For Kaplan-Meier curves&#44; over-all survival &#40;OS&#41; and disease-specific survival &#40;DSS&#41; were conducted where <span class="elsevierStyleItalic">P</span>-values and hazard ratio &#40;HR&#41; with 95&#37; confidence interval &#40;CI&#41; were generated by log-rank tests and univariate Cox proportional hazards regression&#46; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;05 was considered statistically significant&#46; After screening out the ferroptosis-related gene that significantly affected the survival in BLCA&#44; we defined these genes as &#8220;Target Genes&#8221;&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Prognostic significance of ferroptosis-related gene expression</span><p id="par0030" class="elsevierStylePara elsevierViewall">we performed univariate and multivariate cox regression analysis to identify the proper terms to build the nomogram of &#8220;Target Genes&#8221;&#46; The forest was used to show the <span class="elsevierStyleItalic">P</span>-value&#44; HR&#44; and 95&#37; CI of each variable through the &#8216;forest plot&#39; R package&#46; A nomogram was developed based on the results of multivariate Cox proportional hazards analysis to predict the 1-3-5-year overall survival&#46; The nomogram provided a graphical representation of the factors&#44; which can be used to calculate the risk of survival for an individual patient by the points associated with each risk factor through the &#8216;rms&#8217; R package&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Pathological stage plot and DNA methylation analysis</span><p id="par0035" class="elsevierStylePara elsevierViewall">We further investigate the expression difference in different pathological stages and DNA methylation analysis of &#8220;Target Genes&#8221; by UALCAN web &#40;http&#58;<a href="http://ualcan.path.uab.edu/index.html">http&#58;&#47;&#47;ualcan&#46;path&#46;uab&#46;edu&#47;index&#46;html</a>&#41; and Gene Expression Profiling Interactive Analysis &#40;GEPIA&#41; database &#40;<a href="http://gepia.cancer-pku.cn/">http&#58;&#47;&#47;gepia&#46;cancer-pku&#46;cn&#47;</a>&#41; from the TCGA project&#46; &#8220;Expression&#8221; and &#8220;Methylation&#8221; modules of UALCAN were used to conduct these analyses&#44; with the settings of &#8220;Individual cancer stage&#8221;&#46; Meanwhile&#44; the &#8220;Expression analysis-Box Plots&#8221; of GEPIA was also conducted to ensure the pathological stage plot&#44; and <span class="elsevierStyleItalic">P</span>-value &#60;&#46;05&#44; log2FC &#40;fold change&#41; &#60; 1&#44; and &#8220;Match TCGA tumor&#8221; were set&#46; The box or violin plots are applied with log2 &#91;TPM &#40;Transcripts per million&#41; &#43;1&#93; transformed expression data&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">TMB analysis</span><p id="par0040" class="elsevierStylePara elsevierViewall">We used R software v4&#46;0&#46;3 and &#8216;ggstatsplot&#8217; R packages for statistical analysis to explore the relationship between TMB and &#8220;Target Genes&#8221;&#46; TMB is acquired from the article Vesteinn Thorsson et al&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> in 2019&#46; If not otherwise stated&#44; the rank-sum test detects two sets of data&#44; and a <span class="elsevierStyleItalic">P</span>-value of &#60;&#46;05 is considered statistically significant&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Enrichment analysis</span><p id="par0045" class="elsevierStylePara elsevierViewall">We surfed the STRING website &#40;<a href="https://string-db.org/">https&#58;&#47;&#47;string-db&#46;org&#47;</a>&#41; setting the query of &#8220;Target Genes&#8221;&#44; organism &#40;&#8220;Homo sapiens&#8221;&#41;&#44; the following main parameters&#58; minimum required interaction score &#91;&#8220;Low confidence &#40;0&#46;150&#41;&#8221;&#93;&#44; the meaning of network edges &#40;&#8220;evidence&#8221;&#41;&#44; max number of interactors to show &#40;&#8220;no more than 50 interactors&#8221;&#41; and active interaction sources &#40;&#8220;experiments&#8221;&#41;&#46; Meanwhile&#44; we uploaded the gene lists to DAVID &#40;Database for annotation&#44; visualization&#44; and integrated discovery&#41;&#44; and set them as &#40;&#8220;OFFICIAL&#95;GENE&#95;SYMBOL&#8221;&#41; and species &#40;&#8220;Homo sapiens&#8221;&#41;&#44; and obtained the data of the functional annotation chart&#46; The enriched pathways were finally visualized with the R packages of &#8220;tidyr&#8221; and &#8220;ggplot2&#8221;&#46; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;05 was considered statistically significant&#46; Furthermore&#44; we combined the above data to perform in KEGG &#40;Kyoto encyclopedia of genes and genomes&#41; to find a possible pathway&#46;<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11&#44;13</span></a></p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall">Analyzing multiple data from TCGA&#44; we found that 23 ferroptosis-related genes had a strong correlation among each other in BLCA&#44; and the most were positive correlation&#46; SAT1&#44; SLC1A5&#44; HSPA5&#44; SLC7A11&#44; and CISD1 had larger cluster categories &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A&#41;&#46; As for the expression distribution&#44; eight ferroptosis-related genes&#44; CDKN1A&#44; HSPA5&#44; NFE2L2&#44; MT1G&#44; FANCD2&#44; CISD1&#44; TFRC&#44; NCOA4&#44; had a significantly different expression and heat-map in BLCA and adjacent normal bladder tissues &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#44; C&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Prognostic significance of ferroptosis-related gene expression</span><p id="par0055" class="elsevierStylePara elsevierViewall">According to the expression levels&#44; we divided the BLCA cases into 2 groups&#58; low-expression and high-expression&#46; Kaplan-Meier survival curves performed to draw the association in survival outcomes of BLCA patients&#44; mainly using the datasets of TCGA&#46; We found that the BLCA patients with gradually ascending expression levels of HSPA5 and CISD1 would have a different OS and DFS&#46; Low expression of CISD1 have a better OS &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>A&#41; and DFS &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>C&#41; than the high expression&#44; similarly&#44; a worse outcome of OS &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>B&#41; and DFS &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>D&#41; was showed in the high expression of HSPA5&#46; Therefore&#44; these two genes were regarded as &#8220;Target Genes&#8221;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Building a predictive model</span><p id="par0060" class="elsevierStylePara elsevierViewall">We tried to build predictive model that combined &#8220;Target Genes&#8221; with some vital clinicopathological covariates&#46; Univariate and multivariate analyses were conducted to explore the HR in BLCA&#46; HSPA5 &#40;HR&#8239;&#61;&#8239;1&#46;31&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;014&#41; and CISD1 &#40;HR&#8239;&#61;&#8239;1&#46;33&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;0049&#41; had a significant influence on the univariate analysis &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>A&#41;&#59; and combining with the multivariate analysis&#44; CISD1 was also significantly displayed as a prognostic factor &#40;HR&#8239;&#61;&#8239;1&#46;56 <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;05 <a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>B&#41;&#46; We conducted the nomogram and builded a model to predict the 1-3-5-year OS rates in the discovery group using the Cox regression algorithm&#46; The predictors included CISD1 expression&#44; age of patients&#44; pTMN&#44; satisfying the criteria of <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;05 in risk assessment and the caplets for the 1-3-5-year OS rate were predicted highly compared with an ideal model in the entire cohort &#40;C-index&#58; 0&#46;697&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001 <a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>C&#44;D&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Pathological stages plot and DNA methylation</span><p id="par0065" class="elsevierStylePara elsevierViewall">We further explored the correlation of levels of HSPA5 and CISD1 with different pathological stages&#46; As shown in the figures&#44; HSPA5 had significant differences among stages &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>A&#44; <a class="elsevierStyleCrossRef" href="#fig0020">4</a>B&#41;&#44; and CISD1 was also expressed defferently in normal tissue and stage 1&#47;2 of bladder cancer &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>C&#44; <a class="elsevierStyleCrossRef" href="#fig0020">4</a>D&#41;&#46; Moreover&#44; we demonstrated that higher stages &#40;T3-4&#41; were associated with a higher expression of HSPA5 &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;01 <a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>B&#41;&#46; In addition&#44; DNA methylation was also probed by UALCAN&#44; and the results showed that HSPA5 and CISD1 had a lower methylation rate than normal tissue &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>&#41;&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="fig0025"></elsevierMultimedia></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Enrichment analysis</span><p id="par0070" class="elsevierStylePara elsevierViewall">To gain a further investigation into the molecular mechanism and biological importance of the ferroptosis-related genes in BLCA&#44; we attempted to screen out the HPSA5 expression-correlated genes and pathways by enrichment analyses&#46; Based on the STRING tool&#44; several genes&#58; HSP90B1&#44; ATF6&#44; CANX&#44; CALR&#44; DNAJC10&#44; PDIA3&#44; ERN1&#44; DNAJB11&#44; PDIA4&#44; and P4HB had a strong correlation with HSPA &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>A&#41;&#46; Furthermore&#44; GO enrichment analyses showed that HSPA5 was involved in protein binding and activity&#44; especially in unfolded protein binding&#44; disulfide oxidoreductase activity&#44; Hsp70 protein binding &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>B&#41;&#46; KEGG was also applied for finding the possible pathways&#46; DNA replication&#44; cell cycle&#44; protein export&#44; P53 signaling pathway&#44; and so on were also relevant &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>C&#41;&#46;</p><elsevierMultimedia ident="fig0030"></elsevierMultimedia></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Tumor mutational burden &#40;TMB&#41; analysis</span><p id="par0075" class="elsevierStylePara elsevierViewall">To further explore the role of HSPA5 and CISD1 in the tumorigenesis of BLCA&#44; we conducted a Spearman-Correlation analysis of TMB with HSPA5 and CISD1&#44; notably&#44; we found that HSPA5 had a positive connection with TMB &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;02 Fig&#46; S1&#41;&#46;</p></span></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0135">Discussion</span><p id="par0080" class="elsevierStylePara elsevierViewall">Bladder cancer is a malignant urothelial carcinoma that has a great threat to human health&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> Surgical resection&#44; intravesical infusion therapy&#44; chemotherapy&#44; immunotherapy&#44; and so on were optional treatments&#59; however&#44; the survival of BLCA was not ideal&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> What counts in prolonging the survival time may lie in finding a new method for subsidiarity or therapies&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Ferroptosis<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> has different features and mechanisms from apoptosis and necroptosis&#44; and it widely functions and regulates various diseases&#59; besides&#44; it is also confirmed of a potential function of suppressing tumor growth and killing tumor cells&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> Lately&#44; Zekun Liu reported that the twenty-four ferroptosis regulator genes &#40;FRGs&#41; played critical roles in regulating ferroptosis in tumors&#46; To explore the correlation of FRGs with BLCA&#44; in our present study&#44; we demonstrated that eight ferroptosis-related genes&#44; SAT1&#44; SLC1A5&#44; HSPA5&#44; SLC7A11&#44; and CISD1 had a strong relationship across each other in bladder cancer&#46; To take a further investigation into the expression and the heat-map&#44; we found that CDKN1A&#44; HSPA5&#44; NFE2L2&#44; MT1G&#44; FANCD2&#44; CISD1&#44; TFRC&#44; NCOA4 had different expression distribution in bladder cancer&#46; Notably&#44; different level of HSPA5 and CISD1&#44; would significantly effect the OS and DFS of bladder cancer patients&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Consistent with the previous study&#44; Shanzhu et al&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> demonstrated that HSPA5 regulates ferroptosis cell death through HSPA5-GPX4 pathway in the cancer cells&#46; In Hua Yuan&#8217;s research&#44;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> they showed that CISD1&#44; an iron-containing outer mitochondrial membrane protein&#44; had a novel role in protecting against mitochondrial injury in ferroptosis and could negatively regulate ferroptosis cancer cell death&#46; HSPA5 had a really important role in regulating the homeostasis of mitochondria&#44; which also involved in ferroptosis&#46; Combining with the results&#44; we speculated that HSPA5 and CISD1 had an important role in inhibiting tumor growth and progression&#46; In our study&#44; we found that CISD1 was also significantly displayed as a prognostic factor &#40;HR&#8239;&#61;&#8239;1&#46;56 <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;05&#41; and had an ideal nomogram to predict the 1-year OS &#40;C-index&#58; 0&#46;701&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001&#41;&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">To gain a further investigation&#44; we confirmed that HSPA5 and CISD1 had a lower DNA methylation rate than normal tissue and HSPA5 had a positive connection with TMB &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;02&#41;&#46; In addition&#44; the enrichment analysis and KEGG showed that HSPA5 participated in the DNA replication and P53 signaling pathway&#44; and CISD1 mediated the oxidative phosphorylation and positive regulation of the intrinsic apoptotic signaling pathway&#46; As previous studies<a class="elsevierStyleCrossRefs" href="#bib0100"><span class="elsevierStyleSup">20&#8211;22</span></a> had reported that the above-related signaling pathways and genes affected carcinogenesis and progression&#44; our studies indicated that HSPA5 and CISD1 could contribute to the depression of tumorigenesis in BLCA&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">There were some limitations that we had to admit in this study&#46; Although several databases were used in the analysis&#44; more clinical trials and cell researches were needed to verify the functions of the ferroptosis-related genes&#46; Moreover&#44; we found out that the HSPA5 could participate in p53 signaling pathway which affected BLCA&#44; but the clear tumorigenesis pathways were appealed for exploring&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">In conclusion&#44; our study confirmed that ferroptosis-related genes had a strong correlation with BLCA&#44; notably&#44; HSPA5 and CISD1 may play a role in inducing ferroptosis to suppress bladder tumorigenesis and CISD1 can be a novel prognostic biomarker as well as an effective target for diagnosis and treatment in BLCA&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0140">Ethical approval and consent to participate</span><p id="par0110" class="elsevierStylePara elsevierViewall">This article do not contain any studies with human participants or animals performed by the author&#46;</p></span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0145">Conflict of interest</span><p id="par0115" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflict of interest&#46;</p></span><span id="sec0090" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0150">Author contributions</span><p id="par0120" class="elsevierStylePara elsevierViewall">Methodology&#44; Writing &#8211; original draft&#44; Yue Yang&#46;&#59; Software&#44; Hanchao Zhang&#59; Formal analysis&#44; Haifeng Hu&#59; Data curation&#44; Lin Chen&#59; Writing &#8211; review &#38; editing&#44; Jin Yang&#46;</p></span></span>"
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      "en" => array:3 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Background</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Bladder cancer &#40;BLCA&#41; is a malignant urothelial carcinoma with a high mortality rate&#46; Ferroptosis is a new type of programmed cell death and functions in suppressing tumor growth and progression&#46; However&#44; few studies focus on ferroptosis and BLCA&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Materials and methods</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">We explored the potential oncogenic roles of ferroptosis-related genes in BLCA based on multiple public datasets&#46; We then used univariate and multivariate cox regression to build a new survival model based on ferroptosis-related genes to predict the survival of BLCA&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">We found that 23 ferroptosis-related genes had a strong correlation with each other in BLCA&#46; Eight ferroptosis-related genes&#44; CDKN1A&#44; HSPA5&#44; NFE2L2&#44; MT1G&#44; FANCD2&#44; CISD1&#44; TFRC&#44; NCOA4&#44; had a significantly different expression and heat-map&#46; HSPA5 and CISD1 have a statistically significant difference in OS and DFS&#46; Besides&#44; CISD1 had an ideal nomogram to predict the 1-3-5-year OS &#40;C-index&#58; 0&#46;701&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001&#41;&#46; Furthermore&#44; HSPA5 and CISD1 had a lower DNA methylation rate than normal tissue and HSPA5 had a positive connection with TMB &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;02&#41;&#46; In addition&#44; HSPA5 participated in the DNA replication and P53 signaling pathway&#44; and CISD1 mediated the oxidative phosphorylation and positive regulation of the intrinsic apoptotic signaling pathway&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Ferroptosis-related genes had a strong correlation with BLCA&#44; notably&#44; HSPA5 and CISD1 may play a role in inducing ferroptosis to suppress bladder tumorigenesis and CISD1 can be a novel prognostic biomarker as well as an effective target for diagnosis and treatment in BLCA&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "abst0005"
            "titulo" => "Background"
          ]
          1 => array:2 [
            "identificador" => "abst0010"
            "titulo" => "Materials and methods"
          ]
          2 => array:2 [
            "identificador" => "abst0015"
            "titulo" => "Results"
          ]
          3 => array:2 [
            "identificador" => "abst0020"
            "titulo" => "Conclusion"
          ]
        ]
      ]
      "es" => array:3 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n</span><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">El c&#225;ncer de vejiga &#40;CV&#41; es un carcinoma urotelial maligno con altas tasas de mortalidad&#46; La ferroptosis es un nuevo tipo de muerte celular programada&#44; cuyo funcionamiento impide el crecimiento y la progresi&#243;n tumoral&#46; Sin embargo&#44; existen pocos estudios centrados en la ferroptosis y el CV&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Materiales y m&#233;todos</span><p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Exploramos las posibles funciones oncog&#233;nicas de los genes vinculados a la ferroptosis en el CV bas&#225;ndonos en m&#250;ltiples conjuntos de datos p&#250;blicos&#46; Posteriormente utilizamos la regresi&#243;n de Cox univariante y multivariante para construir un nuevo modelo de supervivencia basado en los genes vinculados a la ferroptosis para predecir la supervivencia en el CV&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Encontramos que 23 genes vinculados a la ferroptosis estaban fuertemente correlacionados entre s&#237; en el CV&#46; Ocho genes vinculados a la ferroptosis&#44; CDKN1A&#44; HSPA5&#44; NFE2L2&#44; MT1G&#44; FANCD2&#44; CISD1&#44; TFRC&#44; NCOA4&#44; ten&#237;an una expresi&#243;n y un mapa de calor significativamente diferentes&#46; HSPA5 y CISD1 mostraron una diferencia estad&#237;sticamente significativa en t&#233;rminos de SG y SLE&#46; Adem&#225;s&#44; CISD1 ten&#237;a un nomograma excelente para predecir la SG a 1-3-5 a&#241;os &#40;&#237;ndice C&#58; 0&#44;701&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#44;001&#41;&#46; Adicionalmente&#44; HSPA5 y CISD1 ten&#237;an una tasa de metilaci&#243;n del ADN inferior a la del tejido normal y HSPA5 ten&#237;a un vinculo positivo con la carga mutacional tumoral &#40;en adelante TMB&#44; por sus siglas en ingl&#233;s&#41; &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#44;02&#41;&#46; Adem&#225;s&#44; se observ&#243; participaci&#243;n del HSPA5 en la replicaci&#243;n del ADN y en la v&#237;a de se&#241;alizaci&#243;n de P53&#44; y mediaci&#243;n del CISD1 en la fosforilaci&#243;n oxidativa y regulaci&#243;n positiva de la v&#237;a intr&#237;nseca de la apoptosis&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusi&#243;n</span><p id="spar0075" class="elsevierStyleSimplePara elsevierViewall">Los genes vinculados a la ferroptosis mostraron una fuerte correlaci&#243;n con el CV&#59; en particular&#44; puede ser relevante el papel de HSPA5 y CISD1 en la inducci&#243;n de la ferroptosis para suprimir la tumorig&#233;nesis vesical y el gen CISD1 puede ser un nuevo biomarcador pron&#243;stico&#44; as&#237; como una diana eficaz para el diagn&#243;stico y tratamiento del CV&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "abst0025"
            "titulo" => "Introducci&#243;n"
          ]
          1 => array:2 [
            "identificador" => "abst0030"
            "titulo" => "Materiales y m&#233;todos"
          ]
          2 => array:2 [
            "identificador" => "abst0035"
            "titulo" => "Resultados"
          ]
          3 => array:2 [
            "identificador" => "abst0040"
            "titulo" => "Conclusi&#243;n"
          ]
        ]
      ]
    ]
    "NotaPie" => array:1 [
      0 => array:2 [
        "etiqueta" => "&#9734;"
        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Yang Y&#44; Hu H&#44; Chen L&#44; Zhang H&#44; Yang J&#46; Nuevo modelo pron&#243;stico de supervivencia del c&#225;ncer de vejiga basado en los genes vinculados a la ferroptosis &#40;FRGS&#41;&#46; Actas Urol Esp&#46; 2022&#59;46&#58;494&#8211;503&#46;</p>"
      ]
    ]
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      0 => array:1 [
        "seccion" => array:1 [
          0 => array:4 [
            "apendice" => "<p id="par0135" class="elsevierStylePara elsevierViewall">The following is Supplementary data to this article&#58;<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>"
            "etiqueta" => "Appendix A"
            "titulo" => "Supplementary data"
            "identificador" => "sec0100"
          ]
        ]
      ]
    ]
    "multimedia" => array:8 [
      0 => array:8 [
        "identificador" => "fig0005"
        "etiqueta" => "Figure 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr1.jpeg"
            "Alto" => 2870
            "Ancho" => 3175
            "Tamanyo" => 1089661
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        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0005"
            "detalle" => "Figure "
            "rol" => "short"
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        "descripcion" => array:1 [
          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Correlation analysis&#58; A&#58; Correlation of 23 ferroptosis-related genes in BLCA&#46; The circle represents the ferroptosis-related mRNA&#44; and the line represents the relationship between genes&#46; The red represents the positive correlation and the blue represents the negative correlation&#46; A thicker line represents a higher correlation between the two genes&#46; B&#58; The expression of ferroptosis-related mRNA in BLCA and normal tissues&#44; where the horizontal axis represents different mRNA&#44; the vertical axis represents the mRNA expression distribution&#44; where different colors represent different groups&#44; and the upper left corner represents the significance p-value test method&#46; Asterisks represent levels of significance&#46; C&#58; Ferroptosis-related gene expression heat map&#44; where different colors represent the expression trend in different samples&#46; &#40;&#42;<span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;05&#44; &#42;&#42;<span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;01&#44; &#42;&#42;&#42;<span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001&#41;&#46;</p>"
        ]
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      1 => array:8 [
        "identificador" => "fig0010"
        "etiqueta" => "Figure 2"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr2.jpeg"
            "Alto" => 3031
            "Ancho" => 2508
            "Tamanyo" => 608932
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        ]
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0010"
            "detalle" => "Figure "
            "rol" => "short"
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Kaplan-Meier survival analysis&#58; Over survival &#40;OS&#41; of CISD1 &#40;A&#41; and HSPA5 &#40;B&#41;&#59; Disease-free survival &#40;DFS&#41; of CISD1 &#40;D&#41; and HSPA5 &#40;E&#41;&#46;</p>"
        ]
      ]
      2 => array:8 [
        "identificador" => "fig0015"
        "etiqueta" => "Figure 3"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr3.jpeg"
            "Alto" => 2560
            "Ancho" => 3175
            "Tamanyo" => 561955
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        ]
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0015"
            "detalle" => "Figure "
            "rol" => "short"
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Predictive model&#58; Univariate &#40;A&#41; and multivariate &#40;B&#41; analyses of HSPA5 and CISD1&#46; C&#58; Nomogram of CISD1 to predict the 1-3-5-year overall survival of BLCA patients&#46; D&#58; Calibration curve for the overall survival nomogram model in the group&#46; A dashed diagonal line represents the ideal nomogram&#46;</p>"
        ]
      ]
      3 => array:8 [
        "identificador" => "fig0020"
        "etiqueta" => "Figure 4"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr4.jpeg"
            "Alto" => 2882
            "Ancho" => 3175
            "Tamanyo" => 457984
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        ]
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0020"
            "detalle" => "Figure "
            "rol" => "short"
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Pathological stages plot&#58; A&#58;Expression of HSPA5 based on the individual cancer stage by UALCAN&#46; B&#58; Pathological stages plot of HSPA5 by GEPIA&#46; C&#58;Expression of CISD1 based on the individual cancer stage by UALCAN&#46; D&#58; Pathological stages plot of CISD1 by GEPIA&#46;</p>"
        ]
      ]
      4 => array:8 [
        "identificador" => "fig0025"
        "etiqueta" => "Figure 5"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr5.jpeg"
            "Alto" => 1161
            "Ancho" => 3175
            "Tamanyo" => 153122
          ]
        ]
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0025"
            "detalle" => "Figure "
            "rol" => "short"
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Promoter methylation level in BLCA&#46; A CISD1&#59; B&#58;HSPA5&#46;</p>"
        ]
      ]
      5 => array:8 [
        "identificador" => "fig0030"
        "etiqueta" => "Figure 6"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr6.jpeg"
            "Alto" => 2391
            "Ancho" => 3175
            "Tamanyo" => 846183
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        ]
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0030"
            "detalle" => "Figure "
            "rol" => "short"
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Enrichment analysis&#58; A&#58; We first obtained the available experimentally determined HSPA5-binding proteins using the STRING tool&#46; B&#58; Molecular function &#40;Gene oncology&#41; of HSPA5&#46; C&#58; Based on the HSPA5-binding and interacted genes&#44; KEGG pathway analysis was performed&#46;</p>"
        ]
      ]
      6 => array:8 [
        "identificador" => "tbl0005"
        "etiqueta" => "Table 1"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0035"
            "detalle" => "Table "
            "rol" => "short"
          ]
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        "tabla" => array:1 [
          "tablatextoimagen" => array:1 [
            0 => array:1 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Character&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Group1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Group2&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">P</span>&#95;value&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">Status&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Alive&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">157&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">157&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Dead&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">149&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">149&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Age&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Mean &#40;SD&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60&#46;1 &#40;11&#46;2&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">61&#46;1 &#40;11&#46;9&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Median &#91;MIN&#44; MAX&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60 &#91;19&#44;90&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">61 &#91;19&#44;90&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;222&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Gender&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">72&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Grade&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">G1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">27&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">62&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">G2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">190&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">300&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">G3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">76&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">119&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">G4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">GX&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">16&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Not Available&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;722&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">New&#95;tumor&#95;event&#95;type&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Metastasis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">18&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Primary&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Recurrence&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">22&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">39&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;421&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Smoking&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Non-smoking&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">59&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">111&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Smoking&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">240&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">381&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;395&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Radiation&#95;therapy&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Non-radiation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">21&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">62&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Radiation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">93&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">121&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;006&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">History&#95;of&#95;neoadjuvant&#95;treatment&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Neoadjuvant&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">No neoadjuvant&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">302&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">492&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#46;656&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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