Prostate cancer: The revolution of the fusion genes | Actas Urológicas Españolas (English Edition)

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with an average age of death of 75 years&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Histologically&#44; PCa is constituted of a heterogeneous mixture of cells&#44; mainly epithelial and stromal&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> This process begins with a dysplasia that starts as a proliferative inflammatory atrophy &#40;PIA&#41;&#44; progressing to prostatic intraepithelial neoplasia &#40;PIN&#41;&#44; and in some cases it leads to a carcinoma&#46; There is evidence to suggest that one of the triggers of tumorogenesis could be a prostate inflammation due to infectious agents or ingestion of carcinogens&#46; In parallel&#44; some cells accumulate genetic alterations that&#44; along with the androgenic signaling&#44; stimulate the growth and proliferation of the tumor&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Clinically&#44; there are two large groups of PCa&#58; prostate tumors able to spread that will end up being lethal&#44; and others that are relatively indolent&#44;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> which&#44; to start with&#44; raise the problem of how to distinguish some tumors from others and the manner of best clinical approach in each case&#46; Currently&#44; serum PSA levels provide highly organ-specific information&#44; but little disease-specific&#46; Thus&#44; both in benign prostatic hyperplasia and prostatitis&#44; serum increases of this biomarker are produced&#44; but many patients with localized PCa also have PSA values that overlap with those of healthy subjects&#44; resulting in a gray area of difficult interpretation of the range between 4 and 10<span class="elsevierStyleHsp" style=""></span>ng&#47;ml&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Moreover&#44; numerous studies suggest that PCa is overdiagnosed in 30&#8211;50&#37; of the cases&#44; that is&#44; not all the patients with an elevated PSA have a prostate tumor&#46; After the diagnosis&#44; the main prognostic factor is the Gleason score&#44; which consists of assigning a grade of 1&#8211;5 in descending differentiation to each of the two main foci of the tumor&#46; The sum of both values is the score&#46; Although this parameter is the gold standard in the clinical management of PCa&#44; it presents certain problems&#58; first&#44; the determination is made on tissue obtained from a prostate biopsy&#44; a surgical procedure that has certain comorbidity&#44; particularly significant in elderly patients&#59; besides&#44; this score suffers from interpretive variation&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">In the prognosis of the disease&#44; the lack of a reliable method capable of determining the time at which the prostate tumor will become hormone-resistant is problematic&#44; because from here on&#44; the patient&#39;s prognosis worsens and bone metastases&#44; for which currently only palliative treatment is available&#44; often occur&#46;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">For all this&#44; it is very important to identify new biomarkers that represent useful tools in the diagnosis and clinical management of PCa&#46; These markers should be determinable by objective&#44; quantitative and mechanism-specific techniques&#44; and as far as possible&#44; they should be accessible by noninvasive methods&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">This review aims to provide an overview of the status of some of these biomarkers&#44; with particular emphasis on TMPRSS2-ETS fusion genes and their possible involvement in the clinical management of patients with PCa&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">New biomarkers in prostate cancer</span><p id="par0040" class="elsevierStylePara elsevierViewall">One approach in the search for biomarkers is to study the expression of genes associated with PCa&#46; Thus&#44; underexpression of the GSTP1 gene &#40;Glutathione S-transferase-PI&#41; &#40;11q13&#41; due to hypermethylation of its promoter region has been described&#46; This gene catalyzes the glutathione-mediated molecular detoxification&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> This alteration is in the vast majority of prostate neoplasias and in 70&#37; of prostate intraepithelial neoplasias &#40;PIN&#41;&#46; Most tumors with this disorder are also associated with hypermethylation of other genes such as <span class="elsevierStyleItalic">p16</span><span class="elsevierStyleSup"><span class="elsevierStyleItalic">INK4A</span></span> &#40;9p21&#41;&#44; <span class="elsevierStyleItalic">p14</span><span class="elsevierStyleSup"><span class="elsevierStyleItalic">ARF</span></span> &#40;9p21&#41; and <span class="elsevierStyleItalic">MGMT</span> &#40;10q26&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">Overexpression of AMACR &#40;5p13&#46;2-q11&#46;1&#41; was also found in 88&#37; of PCa&#46; This gene encodes for alpha-methyl coenzyme A racemase&#44; an enzyme involved in branched chain long fatty acids beta-oxidation&#44;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> which has been proposed as a key factor in the relationship of PCa with certain dietary habits&#46; Given its high expression in PCa&#44; some authors have developed diagnostic urine tests with promising results&#44;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> although the analyzed series are not consistent enough to provide definitive data&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">The expression of other genes has been associated with PCa progression&#46; Thus&#44; the PAR-2 gene &#40;5q13&#46;3&#41;&#44; which encodes for a G protein-coupled receptor activated by specific serine proteases&#44; seems involved in the metastasis<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> and overexpresses in approximately 40&#37; of PCas&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> Other genes have an association with clinical parameters&#44; such as <span class="elsevierStyleItalic">HEPSIN &#40;TMPRSS1&#41;</span> &#40;19q11-q13&#46;2&#41;&#44; which encodes for a transmembrane protein with serine protease activity&#44; and <span class="elsevierStyleItalic">Pim-1</span> &#40;6p21&#46;2&#41;&#44; encoding for a protein with serine-threonine kinase activity&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a><span class="elsevierStyleItalic">SPINK-1</span> &#40;5q32&#41; encodes for a protein that inhibits pancreatic secretion of trypsin and is overexpressed in approximately 10&#37; of PCa cases&#46; Its expression is detectable in urine samples and seems related to the biochemical progression-free interval&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">PTEN</span> &#40;10q23&#46;3&#41; is a tumor suppressor gene that encodes for a protein that dephosphorylates phosphatidylinositol-3-phosphate &#40;PIP3&#41;&#46; The loss of function of this gene is one of the most common genetic abnormalities in various types of cancer&#46; Specifically in PCa&#44; it occurs in approximately 40&#37; of the cases&#46; Deletions of <span class="elsevierStyleItalic">PTEN</span> have been associated with Gleason scores<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>7&#44; as well as with biochemical relapse and nodal metastasis&#46; The deletion of this gene causes a constitutive activation of the PI3K pathway that is key to many cancer processes&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">PCA-3 &#40;DD3&#41;</span> is a gene encoding for a non-coding messenger RNA &#40;mRNA&#41; with a high rate of expression in prostate tumor tissue&#44; and whose biological function is still unclear&#46; There is growing evidence that its determination in urine after prostatic massage is much more specific than PSA levels to detect PCa&#46; Its prognostic ability is at issue&#44; having offered controversial results about it&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> Today it is the only one of these molecular biomarkers for clinical use in some reference centers in the United States and Europe &#40;<a href="http://www.pca3.org/">www&#46;pca3&#46;org</a>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a></p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">The discovery of <span class="elsevierStyleItalic">TMPRSS2-ETS</span> in prostate cancer</span><p id="par0065" class="elsevierStylePara elsevierViewall">The fusion genes are formed when two chromosomes&#44; or two regions of the same&#44; break and change position leading sometimes to a new gene &#40;also called chimeric gene&#41; with a new function&#46; These genes are the result of structural chromosome aberrations &#40;reciprocal translocations&#44; deletions or inversions&#41; that have been described in many types of cancer&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> However&#44; given the size of the human genome and the low percentage of coding DNA&#44; most chromosomal breaks that ultimately result in a balanced translocation would not produce a phenotypic effect because they do not affect coding regions&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Fusion genes have been extensively characterized in lymphomas&#44; leukemias and sarcomas&#44; but only recently have started to be identified and characterized in carcinomas&#44; mainly in PCa although they are also being identified in papillary and follicular thyroid carcinomas&#44; in some kidney and mucoepidermoid carcinomas&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> The delay in the discovery of these genes in carcinomas is probably due to problems in the use of classical cytogenetic techniques in this type of tumors&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p><p id="par0075" class="elsevierStylePara elsevierViewall">In the field of phenotypically significant fusions involved in cancer&#44; we have two great groups&#44; in which overexpression of an oncogene such as COL1A1-PDGF-beta&#44; present in dermatofibrosarcoma <span class="elsevierStyleItalic">protuberans</span>&#44; is produced&#59; and the second group in which there is a chimeric protein that implies a transcription factor&#44; such as EWS-FLI1 in Ewing&#39;s sarcomas&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> While the presence of chimeric genes cannot be observed directly using techniques of high-output analysis &#40;cDNA arrays&#41;&#44; in data sets obtained in these expression experiments&#44; gene rearrangements and copy number alterations can be shown&#44; provided that non-traditional analytical treatments are used for data processing&#46; Student&#39;s <span class="elsevierStyleItalic">t</span>-test&#44; for example&#44; detects genes that constantly overexpress in a certain type of cancer&#44; that is&#44; they have a profile of biomarkers&#44; but it is ineffective when it comes to revealing genes that overexpress in a subset of tumors within a given type of cancer &#40;outliers&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">In 2005&#44; the journal <span class="elsevierStyleItalic">Science</span> published an article by M&#46; Arul Chinnaiyan&#39;s group&#44; from Michigan University&#44; in which a bioinformatic method called COPA &#40;Cancer Outlier Profile Analysis&#41; is implemented&#46; This test seeks to find and reveal genes that overexpress in a subset of cases of a particular cancer &#40;in this case PCa&#41;&#46; With that aim&#44; they analyzed data from 10&#44;486 microarray experiments contained in the Oncomine Database &#40;<a href="http://www.oncomine.org/">http&#58;&#47;&#47;www&#46;oncomine&#46;org&#47;</a>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> In developing this method is the idea that with the evaluation of variance&#44; using the median instead of the mean&#44; the peaks of expression of the genes that only overexpress in a subset of the data will be maintained&#46; This analysis included genes with a known overexpression of a given type of cancer as a confirmation&#44; for example <span class="elsevierStyleItalic">RUNXT1</span> in leukemias&#46; <span class="elsevierStyleItalic">ERG</span> &#40;21q22&#46;3&#41; and <span class="elsevierStyleItalic">ETV1</span> &#40;7p21&#46;2&#41; genes were those with a higher profile of outliers for PCa&#46; Both genes are transcription factors of the ETS family &#40;E26&#41; involved in cell proliferation processes&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">The expression pattern of these transcription factors of the ETS family is mutually exclusive in a subset of PCa cases&#44; a behavior common to other tumors such as Ewing&#39;s sarcoma&#44; in which overexpression of these genes is related to <span class="elsevierStyleItalic">EWS-STD</span> gene fusions&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> From this analogy&#44; Chinnaiyan&#39;s group hypothesized that overexpression of <span class="elsevierStyleItalic">ERG</span> and <span class="elsevierStyleItalic">ETV1</span> may be due to a gene fusion&#46; In order to test the hypothesis&#44; they used the technique of rapid amplification of cDNA ends &#40;RLM-RACE&#41; determining that the <span class="elsevierStyleItalic">TMPRSS2</span> gene was fused in the 5&#8242; position of these <span class="elsevierStyleItalic">ETS</span> family members&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Evidence synthesis</span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Biological implications</span><p id="par0090" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">TMPRSS2</span> is located in the 21q22&#46;3 locus and encodes for a transmembrane receptor of the STP family &#40;type II transmembrane serine protease&#41; with a multimeric structure&#46; This protein comprises a protease domain from S1 family&#44; a LDLRA domain that forms a calcium-binding site&#44; and a third transmembrane domain&#46; TMPRSS2 is regulated by androgens&#44; as it has an androgen response element in the promoter region of its gene&#59; it is found in the seminal fluid proteome and is highly expressed in the prostatic tissue and&#44; to a lesser extent&#44; in the epithelial tissue of the colon&#44; stomach&#44; epididymis and breast&#46; Functionally&#44; by activating this protein&#44; the serine-protease domain is released from the cell surface to the extracellular space and activates PAR-2 &#40;protease-activated receptor&#41;&#44; which&#44; as mentioned above&#44; is a G receptor that plays an important role in PCa metastasis&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> Nevertheless&#44; its significance is unclear&#44; as in TMPRSS2-knockout mouse models it showed a normal phenotype&#44; suggesting that it is a redundant gene&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">For its part&#44; ERG &#40;21q22&#46;2&#41; encodes for a nuclear protein of 363 residues that specifically binds to DNA in regions rich in purine and acts as a transcription factor&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> It consists of 17 exons spanning 300 kilobases and generating&#44; at least&#44; 9 isoforms via alternative splicing&#44; 7 of which code for proteins&#46; This gene is expressed in endothelial tissues&#44; hematopoietic cells&#44; kidney and genitourinary tract&#46; Specifically in PCa&#44; <span class="elsevierStyleItalic">ERG</span> is the most persistently overexpressed gene&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> Among the different <span class="elsevierStyleItalic">ETS</span> family members &#40;which also include <span class="elsevierStyleItalic">ETV4</span>&#44; <span class="elsevierStyleItalic">ETV5</span>&#44; etc&#46;&#41;&#44; many are involved in invasiveness and metastasis processes&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a> This gene family is characterized by the presence in all ETS members of DNA binding domains and several protein binding domains&#46; Particularly&#44; ERG interacts with histone H3 specific methyltransferase &#40;ESET&#41; and may participate in the epigenetic silencing of other genes&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> One hypothesis for the action of this gene in PCa would be that it responds to mitogenic and stress signals transduced through the MAPK pathway by acting on target genes that cause the tumorogenesis process<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0100" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">TMPRSS2</span> and <span class="elsevierStyleItalic">ERG</span> have the same transcriptional orientation&#44; so the fusion of both genes is mainly due to an interstitial deletion in which a region of approximately 3 megabases in the 21q22 locus is lost and&#44; to a lesser extent&#44; to a reciprocal translocation&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> In the deleted cases&#44; the region that is lost on the long arm of chromosome 21 contains 15 genes&#44; of which at least two &#40;<span class="elsevierStyleItalic">ETS2</span> and <span class="elsevierStyleItalic">HMGN1</span>&#41; have been associated with the progression of PCa&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a></p><p id="par0105" class="elsevierStylePara elsevierViewall">Since the initial discovery of two fusions involving the <span class="elsevierStyleItalic">TMPRSS2</span> and <span class="elsevierStyleItalic">ERG</span> genes and two other isoforms of TMPRSS2-ETV1 by Chinnaiyan&#39;s group in 2005&#44;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> many other forms have been described&#46; Currently&#44; there are 20 fusions involving <span class="elsevierStyleItalic">ERG</span> published&#44; other two involving <span class="elsevierStyleItalic">ETV4</span> and another <span class="elsevierStyleItalic">ETV5</span>&#44; all with <span class="elsevierStyleItalic">TMPRSS2</span> in position 5&#8242;&#46; Fusions have also been characterized with other genes in 5&#8242;&#44; such as SLC45A3<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; The latter translocations&#44; although interesting from a biological point of view&#44; have a rather limited clinical potential because of their low incidences &#40;1&#8211;4&#37;&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0110" class="elsevierStylePara elsevierViewall">When it comes to proteins&#44; almost every fusion gene transcripts produces mainly a truncated <span class="elsevierStyleItalic">ERG</span> protein instead of a chimeric protein&#44;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> since the translocated TMPRSS2 region corresponds to the non-coding promoter region of the gene&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">We have evidence that when TMPRSS2-ERG mRNA occurs in the primary tumor&#44; the expression is lost when the androgen signaling of the patient is blocked&#44; recovering it in the hormone-resistant tumor stage&#46; When TMPRSS2 and ERG fuse&#44; a hormone-dependent activation of the transcription factor takes place&#46; Therefore&#44; this deregulation also affects all the target genes of ERG&#44; of which the most frequently co-overexpressed is HDAC-1&#44; which catalyzes the histone deacetylation promoting gene expression&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a></p><p id="par0120" class="elsevierStylePara elsevierViewall">As a whole&#44; ERG overexpression may lead to alterations in the Wnt pathway &#40;responsible for the cell proliferation mechanism&#41;&#44; epigenetic reprogramming and deregulation of cell death pathways&#46; It is worth stressing the role within these pathways of E-cadherin &#40;CDH1&#41;&#44; protein that is considered an important suppressor of metastasis&#46; In PCa&#44; the gene is underexpressed through hypermethylation of its promoter region&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> The involvement of the androgen receptor &#40;AR&#41;&#44; which acts as a master regulator of the progression of the transition from G1-S cell cycle phases by inducing signals that promote G1<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#44; is also very important&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0125" class="elsevierStylePara elsevierViewall">There is also a strong cooperativity between the presence of the fusion gene and the PI3K pathway&#44; which plays a fundamental role in the metabolism of cancer&#46; Firstly&#44; the correlation between the presence of TMPRSS2-ERG&#44; deletions in PTEN&#44; and expression of MYC has been proven&#44; and secondly&#44; transgenic mouse models for the fusion gene develop PIN&#44; but only in the context of a generalized activation of PI3K pathway&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Clinical significance</span><p id="par0130" class="elsevierStylePara elsevierViewall">The discovery of this fusion gene family has several sides of particular interest&#58; one may help to functionally elucidate the hormone-dependent behavior of PCa&#44; and another may be a therapeutic target<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a>&#59; besides&#44; it produces interesting diagnostic and prognostic possibilities&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">While there are many fusions involving TMPRSS2 and other ETS family members&#44; in future&#44; TMPRSS2-ERG alone will be checked&#44; since it is the most prevalent and the most extensively studied chimeric gen&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p><p id="par0145" class="elsevierStylePara elsevierViewall">TMPRSS2-ERG has a frequency of 40&#8211;70&#37; in PCa&#44; which gives an idea of its potential as a biomarker&#46;<a class="elsevierStyleCrossRefs" href="#bib0065"><span class="elsevierStyleSup">13&#44;30</span></a> Although there are many rearrangements involving both genes&#44; most of them involve the TMPRSS2 exon 1 and ERG &#40;T1E4&#41; 4 followed by the fusion of exons TMPRSS2 1 with ERG &#40;T1E2&#41; 2&#44; which&#44; on the whole&#44; represent approximately 80&#37; of these rearrangements&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> The expression of the protein encoded by the isoform T1E4 might promote tumor growth&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">Prostate carcinogenesis is usually a multicenter process in which several pathogenic pathways co-exist with or without the concurrence of the ETS pathway&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> The multifocal PCa is a heterogeneous group of diseases originated in multiple independent clonal expansions&#46; One way to determine the clonality of PCa is to establish the presence and isoform of TMPRSS-ERG in the different foci of the tumor and metastasis&#46; Foci were found in the same prostate with different isoforms of the fusion gene or without having it&#44; and even two isoforms in the same focus&#46; However&#44; the metastasis always shares the status of the fusion gene with its primary tumor&#44; indicating that it is a single clone that evolves from the original location for metastasis&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a></p><p id="par0155" class="elsevierStylePara elsevierViewall">At diagnostic level&#44; the potential of TMPRSS2-ERG detection is undeniable&#44; given its specificity&#46; While the presence of the fusion gene in frozen surgical pieces<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> and in formalin-fixed paraffin embedded &#40;FFPE&#41; pieces<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> is perfectly established&#44; the determination in other less invasive samples such as blood<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> and urine<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> has an obvious interest&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">There is still no consensus on the prognostic implications of TMPRSS2-ERG<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46; This may be due to the heterogeneity of the studied series and the different techniques used in the determination&#58; fluorescent in situ hybridization and RT-PCR mainly&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0165" class="elsevierStylePara elsevierViewall">There is plenty of evidence that seems to point to the fact that PCa with the TMPRSS2-ERG gene&#44; and those that do not contain it&#44; are two distinct groups in the disease&#46; On the one hand&#44; a study of gene expression revealed that tumors with the fusion gene have different transcriptomic profile&#46; Specifically&#44; 87 genes involved in the signaling pathway of estrogen hormones are overexpressed in positive TMPRSS2-ERG tumors with respect to cases that do not carry this gene&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a></p><p id="par0170" class="elsevierStylePara elsevierViewall">Our group studied the clinicopathologic factors using multivariate analysis&#44; stratifying the population according to the presence or absence of the TMPRSS2-ERG gene&#46; The cases with the fusion gene had&#44; as independent prognostic factors&#44; the serum PSA levels at diagnosis&#44; the Gleason score in the prostatectomy piece and the surgical margins&#44; whereas non-rearranged cases showed prognostic value&#58; the cT&#44; the Gleason score and margins&#44;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> which opens the possibility of considering optimized treatments depending on the status of the fusion gene&#46;</p><p id="par0175" class="elsevierStylePara elsevierViewall">The third argument of molecular stratification of PCa is the geographic distribution of genetic abnormalities&#46; The eastern population has a lower incidence of PCa than Westerners&#46; Mao et al&#46; have recently reported that this difference in incidence entails gene differences&#46; While the frequency of TMPRSS2-ERG rearrangement is around 50&#37; of the cases in Westeners&#44; in the Chinese population it would be 2&#46;5&#37;&#44; and the deletions of the PTEN gene with a frequency of about 40&#37; in the western population would only have an incidence of 7&#46;6&#37; in Chinese people&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a></p><p id="par0180" class="elsevierStylePara elsevierViewall">TMPRSS2&#58; ERG is also an interesting therapeutic target&#46; In cell lines containing the rearranged gene&#44; therapy with HDAC inhibitors &#40;trichostatin&#41; drastically reduces tumor growth&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> In addition&#44; these same TMPRSS2-ERG &#43; cases seem to respond well to estrogen receptor &#40;ER&#41; &#945; agonist drugs and ER &#946; agonist ones&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a> Finally&#44; and in clinical trials&#44; the abiraterone acetate&#44; a molecule that blocks androgen signaling inhibiting the cytochrome P17&#44; has obtained promising results in TMPRSS2-ERG cases&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a></p></span></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Conclusions</span><p id="par0185" class="elsevierStylePara elsevierViewall">The high incidence and the connection with the androgenic signaling pathway of TMPRSS2-ERG make it a biomarker with much potential at a diagnostic and prognostic level&#44; but much work is still necessary&#46;<a class="elsevierStyleCrossRefs" href="#bib0065"><span class="elsevierStyleSup">13&#44;18&#44;23&#44;30&#44;35&#8211;40</span></a> Translationally&#44; it is a clear therapeutic target&#46;</p><p id="par0190" class="elsevierStylePara elsevierViewall">Of great interest is also to continue investigating the involvement of the fusion gene in signaling pathways &#40;androgen&#44; PI3K&#44; Wnt&#44; Hedgehog&#41;&#44; which may help to elucidate the still mysterious molecular biology of this type of tumors&#46;</p><p id="par0195" class="elsevierStylePara elsevierViewall">Finally&#44; the detection of this anomaly in a minimally invasive way is promising&#46; In summary&#44; in cancer molecular biology&#44; the field of fusion genes is promising not only at a basic and clinical but also at a translational level as well&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Funding</span><p id="par0200" class="elsevierStylePara elsevierViewall">This work has been funded by the following grants&#58; <span class="elsevierStyleGrantSponsor">FIS PI061619 and PI10&#47;01206</span>&#44; Madrid&#44; Astra Zeneca&#44; Spain and <span class="elsevierStyleGrantSponsor" id="gs0005">ACOMP&#47;2009&#47;176</span> from the <span class="elsevierStyleGrantSponsor" id="gs0010">Generalitat Valenciana</span>&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Conflict of interest</span><p id="par0205" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare&#46;</p></span></span>"
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          "titulo" => "New biomarkers in prostate cancer"
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          "titulo" => "The discovery of TMPRSS2-ETS in prostate cancer"
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          "titulo" => "Evidence synthesis"
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    "fechaRecibido" => "2010-10-26"
    "fechaAceptado" => "2010-11-05"
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            1 => "Prostate cancer"
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            0 => "<span class="elsevierStyleItalic">TMPRSS2-ERG</span>"
            1 => "C&#225;ncer de pr&#243;stata"
            2 => "Pron&#243;stico"
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        "titulo" => "Abstract"
        "resumen" => "<span class="elsevierStyleSectionTitle">Background</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">TMPRSS2-ETS</span> fusion gene rearrangements constitute a very common and specific alteration in prostate cancer cells&#46; These genetic alterations lead the overexpression of <span class="elsevierStyleItalic">ETS</span> genes which encode the E26 family of transcription factors involved in cell proliferation&#46; Of this family&#44; the <span class="elsevierStyleItalic">ERG</span> oncogene is overexpressed in almost 50&#37; of prostate cancer cases&#46;</p> <span class="elsevierStyleSectionTitle">Evidence synthesis</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">TMPRSS2-ERG</span> overexpresses <span class="elsevierStyleItalic">ERG</span> through an androgen-mediated response&#46; Structurally&#44; the rearrangement is due to interstitial deletion and to a lesser extent to reciprocal translocation and plays a key role in cellular metabolism&#46; Almost all fusion gene transcripts produce a truncated ERG protein and the presence of a specific isoform of this gene suggests the clonality of the tumor&#59; hence&#44; metastasis shares the fusion gene status of their primary lesion&#46; Although the prognostic implications of <span class="elsevierStyleItalic">TMPRSS2-ERG</span> have not been fully elucidated&#44; they constitute a field of great diagnostic potential and&#44; therefore&#44; the development of techniques to identify and to analyze the presence and characteristics of this gene in a non-invasive fashion deserves great interest in this area&#46; Currently&#44; there is evidence supporting the hypothesis that the presence of fusion gene differentiates two molecular groups within prostate cancer with a differential behavior making the fusion gene a potential therapeutic target&#46; In this regard&#44; the use of anti-HDAC &#40;trichostatin&#41;&#44; antagonists of estrogen receptor alpha and abiraterone acetate have shown promising results&#46;</p> <span class="elsevierStyleSectionTitle">Conclusions</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">This review describes the great potential offered by the investigation of fusion genes in PC and the need for further studies&#46;</p>"
      ]
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        "resumen" => "<span class="elsevierStyleSectionTitle">Contexto</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Los reordenamientos <span class="elsevierStyleItalic">TMPRSS2-ETS</span> constituyen una alteraci&#243;n espec&#237;fica y frecuente en tumores prost&#225;ticos que conlleva la sobreexpresi&#243;n de los genes <span class="elsevierStyleItalic">ETS</span> que codifican para la familia E26 de factores de transcripci&#243;n&#44; promoviendo la proliferaci&#243;n celular&#46; De entre estos <span class="elsevierStyleItalic">ERG</span> sobreexpresa en casi el 50&#37; de los carcinomas prost&#225;ticos&#46;</p> <span class="elsevierStyleSectionTitle">S&#237;ntesis de evidencia</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">TMPRSS2-ERG</span> sobreexpresa a <span class="elsevierStyleItalic">ERG</span> en respuesta a andr&#243;genos&#46; Estructuralmente este reordenamiento se debe a una deleci&#243;n intersticial y&#44; en menor medida&#44; a una translocaci&#243;n rec&#237;proca&#44; y tiene un papel clave en el metabolismo celular&#46; Casi todos los transcritos del gen de fusi&#243;n producen una prote&#237;na ERG truncada&#44; y la presencia de una determinada isoforma de este gen indica la clonalidad del tumor&#44; de modo que la met&#225;stasis comparte isoforma de <span class="elsevierStyleItalic">TMPRSS2-ERG</span> con su localizaci&#243;n primaria&#46; Aunque las implicaciones pron&#243;sticas de <span class="elsevierStyleItalic">TMPRSS2-ERG</span> no est&#225;n totalmente elucidadas se considera un campo de gran potencial diagn&#243;stico&#44; por lo que el desarrollo de t&#233;cnicas que permitan determinar la presencia y caracter&#237;sticas de este gen de forma no invasiva es muy interesante&#46; La presencia del gen de fusi&#243;n constituye dos grupos moleculares dentro del CaP con un comportamiento evolutivo claramente diferencial&#44; lo que hace que farmacol&#243;gicamente el gen de fusi&#243;n constituya una diana terap&#233;utica potencial&#46; En este sentido&#44; el uso de f&#225;rmacos anti-HDAC &#40;tricostatina&#41;&#44; antagonistas del receptor de estr&#243;genos alfa y acetato de abiraterona han mostrado resultados prometedores&#46;</p> <span class="elsevierStyleSectionTitle">Conclusiones</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Esta revisi&#243;n expone el gran potencial que representa la investigaci&#243;n de los genes de fusi&#243;n en el CaP y la necesidad de profundizar en su estudio&#46;</p>"
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        "nota" => "<p class="elsevierStyleNotepara">Please cite this article as&#58; Fern&#225;ndez-Serra A&#44; et al&#46; C&#225;ncer de pr&#243;stata&#58; la revoluci&#243;n de los genes de fusi&#243;n&#46; Actas Urol Esp&#46; 2011&#59;45&#58;420&#8211;28&#46;</p>"
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Performance of transcription factors of the ETS family on stress reactions mediated through MAPK signal transduction pathway&#46; Adapted from Petrovics et al&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> The red background indicates overexpression of the gene and the blue one&#44; underexpression&#46; ERG highlighted in red&#46;</p>"
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">&#40;A&#41; Isoforms described to date of the TMPRSS2-ERG fusion gene that give an idea of the great instability of this rearrangement&#46; &#40;B&#41; Other minority fusion genes involving different genes &#40;usually hormone-regulated&#41; in 5&#8242; and other transcription factors of the ETS family in position 3&#8242;&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><td class="td" title="\n
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                  \t\t\t\t" style="border-bottom: 2px solid black">Biological characteristcs&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" style="border-bottom: 2px solid black">Method of detection&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" style="border-bottom: 2px solid black">Number of cases&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" style="border-bottom: 2px solid black">Prognostic implication&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" style="border-bottom: 2px solid black">Bibliographical reference&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " rowspan="23" align="left" valign="\n
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                  \t\t\t\t">TMPRSS2-ETS presence</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">RT-PCR&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">111&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Metastasis and death due to PCa&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"><a class="elsevierStyleCrossRef" href="#bib0190">38</a>&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">RT-PCR&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">61&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Early recurrence after radical prostatectomy&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">RT-PCR&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">102&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">Aggressive PCa&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">RT-PCR&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">165&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">Aggressive PCa&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="" valign="\n
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                  \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 after radical prostatectomy&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="" 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" 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">RT-PCR&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">26&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">Aggressive PCa&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" 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="" 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 after radical prostatectomy&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="" 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" 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">RT-PCR&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">55&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">Unrelated to the aggressiveness of PCa&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">Nested RT-PCR&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">32&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">Unrelated to the aggressiveness of PCa&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">RT-PCR&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">63&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">Unrelated to the aggressiveness of PCa&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"><a class="elsevierStyleCrossRef" href="#bib0090">18</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">RT-PCR&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">50&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">Lower Gleason score&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"><a class="elsevierStyleCrossRef" href="#bib0090">18</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">RT-PCR&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">226&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">Classification in two PCa groups with different prognostic characteristics&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"><a class="elsevierStyleCrossRef" href="#bib0150">30</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">FISH&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">96&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">Aggressive PCa&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"><a class="elsevierStyleCrossRef" href="#bib0090">18</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">FISH&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">118 PCa 18 metastases&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">Aggressive PCa&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"><a class="elsevierStyleCrossRef" href="#bib0090">18</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">FISH&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">521 PCa&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">Unrelated to the aggressiveness of PCa&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" 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">40 metastases&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="" 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="" 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" 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">FISH&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">15&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">Unrelated to the aggressiveness of PCa&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"><a class="elsevierStyleCrossRef" href="#bib0090">18</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">FISH&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">196&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">Lower Gleason score&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"><a class="elsevierStyleCrossRef" href="#bib0195">39</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">FISH&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">521 PCa&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">Lower Gleason score&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" 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">40 metastases&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="" 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="" 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" 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">RT-PCR FISH&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">82&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">Unrelated to the aggressiveness of PCa&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"><a class="elsevierStyleCrossRef" href="#bib0065">13</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">RT-PCR&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 Xenotransplantations 7 PCa cell line 49 PCa&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">Greater recurrence-free survival&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"><a class="elsevierStyleCrossRef" href="#bib0200">40</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">FISH&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="" 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="" 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="" 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" 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">TMPRSS2-ERG deletion and with two or more copies of the fusi&#243;n gene&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">FISH&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">445&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">Lower overall survival&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"><a class="elsevierStyleCrossRef" href="#bib0090">18</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><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">Overexpression of ERG&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">RT-PCR&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">114&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">Disease-free survival after radical prostatectomy&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"><a class="elsevierStyleCrossRef" href="#bib0115">23</a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab183650.png"
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        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Prognostic implications of the presence of TMPRSS2-ETS or features related with the gene&#46;</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0005"
          "bibliografiaReferencia" => array:40 [
            0 => array:3 [
              "identificador" => "bib0005"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Situaci&#243;n del c&#225;ncer en Espa&#241;a&#58; incidencia State of cancer in Spain&#58; incidence"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "G&#46; L&#243;pez-Abente"
                            1 => "M&#46; Poll&#225;n"
                            2 => "N&#46; Aragon&#233;s"
                            3 => "B&#46;P&#46; G&#243;mez"
                            4 => "V&#46;H&#46; Barrera"
                            5 => "V&#46; Lope"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "An Sist Sanit Navar"
                        "fecha" => "2004"
                        "volumen" => "27"
                        "paginaInicial" => "165"
                        "paginaFinal" => "173"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/15381948"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0010"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Prostate cancer"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "W&#46;G&#46; Nelson"
                            1 => "A&#46;M&#46; De Marzo"
                            2 => "W&#46;B&#46; Isaacs"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1056/NEJMra021562"
                      "Revista" => array:6 [
                        "tituloSerie" => "N Engl J Med"
                        "fecha" => "2003"
                        "volumen" => "349"
                        "paginaInicial" => "366"
                        "paginaFinal" => "381"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/12878745"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
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