Original article
Testosterone-deficiency as a risk factor for hip fracture in elderly men
Déficit de testosterona como factor de riesgo de fractura de cadera en hombres de edad avanzada
J. Torremadé-Barredaa,
, J. Rodríguez-Tolràa, I. Román-Romerab, A. Padró-Miquelc, J. Rius-Morenod, E. Franco-Mirandaa
Corresponding author
a Servicio de Urología, Hospital Universitario de Bellvitge, Barcelona, Spain
b Servicio de Medicina Preventiva, Hospital Universitario de Bellvitge, Barcelona, Spain
c Servicio de Bioquímica Clínica, Hospital Universitario de Bellvitge, Barcelona, Spain
d Servicio de Traumatología, Hospital Universitario de Bellvitge, Barcelona, Spain
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"apellidos" => "Franco-Miranda" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:4 [ 0 => array:3 [ "entidad" => "Servicio de Urología, Hospital Universitario de Bellvitge, Barcelona, Spain" "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Servicio de Medicina Preventiva, Hospital Universitario de Bellvitge, Barcelona, Spain" "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Servicio de Bioquímica Clínica, Hospital Universitario de Bellvitge, Barcelona, Spain" "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Servicio de Traumatología, Hospital Universitario de Bellvitge, Barcelona, Spain" "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Déficit de testosterona como factor de riesgo de fractura de cadera en hombres de edad avanzada" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1636 "Ancho" => 2029 "Tamanyo" => 141806 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Selection of the study sample.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Progressive loss of bone mineral density weakens bones and increases the likelihood of fractures. These fractures increase with age and lead to significant morbidity and mortality in the population, being higher in men than in women.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Multiple studies have demonstrated that androgens play a crucial role in maintaining bone mineral density. We know the loss of bone mass after castration or androgen deprivation therapy in prostate cancer.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> Also, androgen replacement therapy is associated to an increased bone mineral density in the spine and hip.<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> However, to date, there is little published evidence linking the effect of testosterone therapy and the risk of osteoporotic fractures.<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4,5</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">The aim of this study was to relate the levels of androgens and the risk of osteoporotic hip fracture in men.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Materials and methods</span><p id="par0020" class="elsevierStylePara elsevierViewall">We conducted a case–control study in the period between February 2010 and January 2011, where the study population were the individuals belonging to the <span class="elsevierStyleItalic">Costa Ponent-Metropolitana Sud</span> health area, whose referral hospital is the <span class="elsevierStyleItalic">Hospital Universitario de Bellvitge</span>. We defined case as any man diagnosed with hip fracture confirmed after radiological study in the Emergency Department at that time interval. The controls were male subjects of the same reference population who underwent a routine blood test in this period of time, without a diagnosis of hip fracture.</p><p id="par0025" class="elsevierStylePara elsevierViewall">The exclusion criteria that were applied to both groups were: (a) previous diagnosis of osteoporosis; (b) high-energy fractures; (c) androgen deprivation in prostate cancer patients; (d) diagnosis of hypogonadism; (e) treatment with corticosteroids; and (f) metastatic bone disease (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">Altogether there were 54 cases and 54 controls, whose data were paired according to their age (pairing range of 2 years).</p><p id="par0035" class="elsevierStylePara elsevierViewall">All the study subjects underwent a thorough medical history to identify the possible causes of secondary osteoporosis, a physical examination and a general blood analysis and a specific hormone one, made during the first 48<span class="elsevierStyleHsp" style=""></span>h after admission, between 7 and 9<span class="elsevierStyleHsp" style=""></span>am.</p><p id="par0040" class="elsevierStylePara elsevierViewall">The variables selected were age, concomitant disease (diabetes mellitus, hypertension, dyslipidemia, ischemic heart disease, and other diseases), type of fracture according to its anatomic classification (subcapital, transcervical, basicervical, pertrochanteric, persubtrochanteric, and subtrochanteric), and the variables result of the analysis (hemoglobin, hematocrit, mean corpuscular speed, creatinine, cholesterol, triglycerides, albumin, total testosterone, sex hormone binding globulin, and total estradiol). Furthermore, we subsequently calculated free testosterone (FT) and bioavailable testosterone (BioT) according to the formulas proposed by Vermeulen et al.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> and accepted by the main scientific societies.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">The statistical analysis was carried out in different phases. First we carried out the descriptive analysis of the variables, according to their category. The quantitative variables were defined, according to their normality (Kolmogorov–Smirnov test), using measures of central tendency (mean or median) and of dispersion (standard deviation or interquartile range). The qualitative variables were described by means of frequencies and proportions. Then, we proceeded to perform the bivariate analysis. For the quantitative variables with normal distribution, we used the Student's “<span class="elsevierStyleItalic">t</span>” test, and for those who did not have a normal distribution, the Mann–Whitney U test. In the case of qualitative variables, we used the Chi square test, or Fischer's exact test when the conditions were not met for the first one (the frequency of some of the expected data was lower than 5). The variables with a <span class="elsevierStyleItalic">p</span> value lower than 0.05 were introduced in the multivariate analysis, where we used a binary logistic regression model, obtaining the adjusted ORs with the 95% CI. The statistical program used was SPSS version 17.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall">68 male patients with a diagnosis of hip fracture, of which one died in the first 24<span class="elsevierStyleHsp" style=""></span>h of admission and 4 were transferred to other hospitals (5 losses in total), were admitted to the Emergency Department of our hospital. Of the 63 remaining patients, 9 patients were excluded according to the criteria described above. The main reasons for exclusion were treatment with androgen deprivation in prostate cancer patients (4 patients) and high-energy fractures (3 patients). We excluded one patient with metastatic bone disease and another patient treated with corticosteroids.</p><p id="par0055" class="elsevierStylePara elsevierViewall">We recruited 54 men with hip fracture, with a median age of 81 years (range: 41–93). The radiological findings confirmed the presence of subcapital fracture (38.9%) and pertrochanteric fracture (38.9%). Other less common fractures were persubtrochanteric (11.1%), basicervical (5.6%), subtrochanteric (3.7%), and transcervical (1.9%). The median age of the controls was 80.5 years (range: 43–95). The clinical characteristics of the patients are summarized in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">The prevalence of cardiovascular risk factors was high in the 2 groups, with hypertension being the most frequent history in both groups. Hypertension and dyslipidemia had higher prevalence in the control group (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.05), finding no statistically significant differences in the other cardiovascular risk factors studied.</p><p id="par0065" class="elsevierStylePara elsevierViewall">The hormone determinations in both groups were compared (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>). The hip fracture patients had testosterone levels lower than controls (8.74<span class="elsevierStyleHsp" style=""></span>nmol/l vs. 11.16<span class="elsevierStyleHsp" style=""></span>nmol/l; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.116). In contrast, estradiol levels were higher in the patients with hip fracture (184<span class="elsevierStyleHsp" style=""></span>pmol/l vs. 164.92<span class="elsevierStyleHsp" style=""></span>pmol/l; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.095). Despite significant differences in the bivariate study, by introducing the testosterone and estradiol variables in the multivariate analysis, we only obtained a correlation trend, without being statistically significant.</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">It is confirmed that the free testosterone levels are independently associated with being a case in the multivariate analysis. We can see that the free testosterone of the cases was 155.1<span class="elsevierStyleHsp" style=""></span>pmol/l and 204.4<span class="elsevierStyleHsp" style=""></span>pmol/l (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.020) in controls. Also, the bioavailable testosterone was significantly lower in the cases than in the controls (2.69<span class="elsevierStyleHsp" style=""></span>nmol/l vs. 3.89<span class="elsevierStyleHsp" style=""></span>nmol/l; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.002) after the multivariate analysis, being the best predictor fracture model with an adjusted OR of 1.58. The comparison of the levels of sex steroids between the 2 groups is presented in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0075" class="elsevierStylePara elsevierViewall">Bone mineralization is the product of the equilibrium between bone formation by osteoblasts and resorption mediated by osteoclasts. Only if these phases are properly attached, the bone mass remains stable. When resorption predominates over formation, bone is lost, the fragility and fracture risk increases. Multiple factors have been identified that lead to this imbalance, sex steroids being one of them.</p><p id="par0080" class="elsevierStylePara elsevierViewall">Human adrenergic receptors belong to the family of nuclear receptors and they were cloned for the first time in 1988.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> Subsequently, Kasperk et al. described the effect of androgens on osteoblastic cells, increasing their activity.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> Several hypotheses have been postulated about the action of androgens on osteoclasts through other intermediaries such as IL-6, PGE2, and PTH.<a class="elsevierStyleCrossRefs" href="#bib0050"><span class="elsevierStyleSup">10–12</span></a></p><p id="par0085" class="elsevierStylePara elsevierViewall">Estrogen receptors are also present in osteoblasts and osteoclasts.<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> Estrogens stimulate the creation of periosteum in males, requiring threshold values necessary for proper bone integrity.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">Therefore, the action of androgens on bone will occur directly on androgenic receptors, and indirectly on estrogen receptors after aromatization to estradiol.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">Low testosterone levels have been associated to hip fractures in multiple studies. Jackson in 1992 was among the first authors to correlate hip fractures in elderly patients with gonadal deficiency, concluding that early identification would be necessary in this group of patients as well as treating androgen deficiency.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> Despite these findings, it was not until a decade later that new studies were published in the same line. Amin et al. analyzed the risk of hip fracture with the estradiol and testosterone levels in the Framingham study (1981–1999), aiming that the low estradiol levels increased the risk of hip fracture, and even more when the low estradiol levels were associated to low testosterone levels.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> But as we see in our study, the correlation between estradiol and osteoporotic fracture is not as consistent. Leifke et al. observe that low levels of total and free testosterone are a predictor of hip fracture, but they are not so for estradiol.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> The low free testosterone levels are not only associated to hip fractures, but they have also been related to symptomatic vertebral fractures.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Mellstrom et al. also confirmed this hypothesis, identifying free testosterone as an independent predictor of fracture in osteoporotic hip, femur, arm, and spine fractures.<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a></p><p id="par0100" class="elsevierStylePara elsevierViewall">Our study confirms the previously postulated results, although there are some methodological limitations in its preparation. The advanced age of both groups leads the control sample to present a higher prevalence of dyslipidemia and hypertension than the cases, as it corresponds to patients undergoing some kind of routine health control by their general practitioner or specialist. Also, performing the analytical determination of the cases occurred in the first 48<span class="elsevierStyleHsp" style=""></span>h, depending on the availability of the laboratory. Although the mean life of albumin is 21 days,<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> albumin levels were lower in the cases, due to the simple fact of staying on absolute diet without protein intake waiting for definitive surgery. This led to the free testosterone levels not to be so different due to the compensatory effect of low albumin in the cases.</p><p id="par0105" class="elsevierStylePara elsevierViewall">In conclusion, the patients with hip fractures have significantly lower levels of calculated and bioavailable free testosterone in our study population. These findings suggest that the levels of free and bioavailable testosterone are independent predictors of osteoporotic hip fracture in elderly patients. Further studies will be designed to determine whether androgen replacement therapy in these patients could provide some benefit in the prevention of osteoporotic fractures.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Conflict of interest</span><p id="par0110" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflict of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:2 [ "identificador" => "xres227338" "titulo" => array:5 [ 0 => "Abstract" 1 => "Objetives" 2 => "Materials and methods" 3 => "Results" 4 => "Conclusions" ] ] 1 => array:2 [ "identificador" => "xpalclavsec212225" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "xres227339" "titulo" => array:5 [ 0 => "Resumen" 1 => "Objetivos" 2 => "Material y métodos" 3 => "Resultados" 4 => "Conclusiones" ] ] 3 => array:2 [ "identificador" => "xpalclavsec212226" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Materials and methods" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Conflict of interest" ] 9 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2012-05-01" "fechaAceptado" => "2012-06-30" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec212225" "palabras" => array:4 [ 0 => "Hypogonadism" 1 => "Testosterone" 2 => "Osteoporosis" 3 => "Hip fractures" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec212226" "palabras" => array:4 [ 0 => "Hipogonadismo" 1 => "Testosterona" 2 => "Osteoporosis" 3 => "Fracturas de cadera" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span class="elsevierStyleSectionTitle" id="sect0010">Objetives</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Progressive loss of bone mineral density weakens the bones and increases the probability of osteoporotic fractures. It is well known that sex steroids play a role in the maintenance of bone density. This fact makes us think there might be a correlation between sex steroid levels and osteoporotic hip fractures.</p> <span class="elsevierStyleSectionTitle" id="sect0015">Materials and methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A case–control study was performed. The cases were 54 men who suffered from hip fracture. They were compared with 54 age-matched male control subjects. Levels of total testosterone, sex hormone binding globuline, albumin and estradiol were measured in all subjects in order to calculate free testosterone and bio-testosterone levels.</p> <span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Men who suffered from hip fracture had lower serum total testosterone (8.74<span class="elsevierStyleHsp" style=""></span>nmol/l vs. 11.16<span class="elsevierStyleHsp" style=""></span>nmol/l; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.116) and lower free testostenone (155.1<span class="elsevierStyleHsp" style=""></span>pmol/l vs. 204.4<span class="elsevierStyleHsp" style=""></span>pmol/l; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.02) than control subjects. Bio-testosterone levels were lower in patients with hip fracture (2.69<span class="elsevierStyleHsp" style=""></span>nmol/l vs. 3.89<span class="elsevierStyleHsp" style=""></span>nmol/l; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.002), being the latter the best fracture predictor (OR: 1.58).</p> <span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">In our study population, men with hip fractures had significantly lower levels of calculated free testosterone and bio-testosterone. These findings suggest that free testosterone and bio-testosterone levels are independent predictors for osteoporotic hip fracture in elderly men.</p>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span class="elsevierStyleSectionTitle" id="sect0035">Objetivos</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">La pérdida progresiva de la densidad mineral ósea debilita los huesos y aumenta la probabilidad de fracturas osteoporóticas. Es conocida la acción de los andrógenos en el mantenimiento de la densidad mineral ósea. Este hecho nos hace pensar que podría existir una relación entre los niveles de esteroides sexuales y la fracturas osteoporóticas de cadera.</p> <span class="elsevierStyleSectionTitle" id="sect0040">Material y métodos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se realiza un estudio caso-control, donde los casos correspondieron a 54 varones con fractura de cadera que se aparearon por edad con 54 controles varones. A todos los pacientes se les determinó niveles de testosterona total, globulina transportadora de hormonas sexuales, albúmina y estradiol para el cálculo de la testosterona libre y la testosterona biodisponible.</p> <span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Los pacientes con fractura de cadera presentaron unos niveles de testosterona inferiores a los controles (8,74 n/mol/L frente a 11,16<span class="elsevierStyleHsp" style=""></span>nmol/L; p<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0,116) al igual que de testosterona libre (155,1<span class="elsevierStyleHsp" style=""></span>pmol/L frente a 204,4<span class="elsevierStyleHsp" style=""></span>pmol/L; p<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0,02). Los niveles de testosterona biodisponible fueron inferiores en pacientes con fractura de cadera (2,69<span class="elsevierStyleHsp" style=""></span>nmol/L frente a 3,89<span class="elsevierStyleHsp" style=""></span>nmol/L; p<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0,002) siendo esta última el mejor predictor para fractura (OR: 1,58).</p> <span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Los pacientes con fractura de cadera presentan unos niveles significativamente inferiores de testosterona libre calculada y biodisponible en nuestra población a estudio. Estos hallazgos sugieren que los niveles de testosterona libre y biodisponible son predictores independientes de fractura de cadera osteoporótica en pacientes de edad avanzada.</p>" ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Torremadé-Barreda J, et al. Déficit de testosterona como factor de riesgo de fractura de cadera en hombres de edad avanzada. Actas Urol Esp. 2013;37:142–6.</p>" ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1636 "Ancho" => 2029 "Tamanyo" => 141806 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Selection of the study sample.</p>" ] ] 1 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "leyenda" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">The values correspond to the prevalence of the risk factor studied expressed in number of cases and the percentage over the total. The significance in the multivariate study is expressed in the last column, a value of <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>><span class="elsevierStyleHsp" style=""></span>0.05 being not significant (NS).</p>" "tablatextoimagen" => array:1 [ 0 => array:2 [ "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"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</td><td 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" style="border-bottom: 2px solid black">Cases<span class="elsevierStyleItalic">n</span> (%) \t\t\t\t\t\t\n \t\t\t\t</td><td 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" style="border-bottom: 2px solid black">Controls<span class="elsevierStyleItalic">n</span> (%) \t\t\t\t\t\t\n \t\t\t\t</td><td 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" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span> value \t\t\t\t\t\t\n \t\t\t\t</td></tr></thead><tbody title="tbody"><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">Diabetes \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">16 (26.6) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18 (33.3) \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">NS \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">Hypertension \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">29 (53.7) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">43 (79.6) \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">0.001 \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">Dyslipidemia \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">11 (20.4) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">23 (42.6) \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">0.013 \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">Ischemic heart disease \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">11 (20.4) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">7 (13) \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">NS \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">Non-ischemic heart disease \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8 (14.8) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">15 (27.8) \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">NS \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">Stroke \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">7 (13) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">5 (9.3) \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">NS \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">Benign prostatic hyperplasia \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4 (7.4) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8 (14.8) \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">NS \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">Chronic renal failure \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">11 (20.4) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">15 (27.8) \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">NS \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">Peripheral arterial vasculopathy \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3 (5.6) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4 (7.4) \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">NS \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab338925.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Main characteristics of cases and controls.</p>" ] ] 2 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "leyenda" => "<p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">The values correspond to the mean<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>standard deviation and the statistical significance in the multivariate analysis.</p>" "tablatextoimagen" => array:1 [ 0 => array:2 [ "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"><td class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</td><td 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" style="border-bottom: 2px solid black">Cases \t\t\t\t\t\t\n \t\t\t\t</td><td 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" style="border-bottom: 2px solid black">Controls \t\t\t\t\t\t\n \t\t\t\t</td><td 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" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span> value \t\t\t\t\t\t\n \t\t\t\t</td></tr></thead><tbody title="tbody"><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">Total testosterone (nmol/l) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8.74<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>4.71 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">11.16<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>5.85 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.116 \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">SHBG (nmol/l) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">49.53<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>19.83 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">44.52<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>19.88 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.265 \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">Albumin (g/l) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">30.67<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>3.83 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">34.75<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>6.06 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.000 \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">Estradiol (pmol/l) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">184.06<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>51.95 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">164.92<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>69.81 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.095 \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">Free testosterone (pmol/l) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">155.1<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>98.6 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">204.4<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>105 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.020 \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">Bioavailable testosterone (nmol/l) \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2.69<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>1.67 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3.89<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>2.01 \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="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.002 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab338926.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Comparison of sex steroid levels between the 2 groups.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2018 February | 12 | 0 | 12 |
| 2018 January | 5 | 3 | 8 |
| 2017 December | 18 | 0 | 18 |
| 2017 November | 7 | 1 | 8 |
| 2017 October | 24 | 2 | 26 |
| 2017 September | 6 | 2 | 8 |
| 2017 August | 19 | 0 | 19 |
| 2017 July | 10 | 2 | 12 |
| 2017 June | 17 | 1 | 18 |
| 2017 May | 16 | 1 | 17 |
| 2017 April | 8 | 2 | 10 |
| 2017 March | 15 | 2 | 17 |
| 2017 February | 16 | 0 | 16 |
| 2017 January | 11 | 0 | 11 |
| 2016 December | 22 | 3 | 25 |
| 2016 November | 24 | 5 | 29 |
| 2016 October | 28 | 11 | 39 |
| 2016 September | 31 | 3 | 34 |
| 2016 August | 25 | 2 | 27 |
| 2016 July | 16 | 1 | 17 |
| 2016 June | 17 | 14 | 31 |
| 2016 May | 14 | 6 | 20 |
| 2016 April | 29 | 4 | 33 |
| 2016 March | 23 | 7 | 30 |
| 2016 February | 24 | 13 | 37 |
| 2016 January | 23 | 8 | 31 |
| 2015 December | 15 | 10 | 25 |
| 2015 November | 13 | 2 | 15 |
| 2015 October | 18 | 8 | 26 |
| 2015 September | 16 | 2 | 18 |
| 2015 August | 14 | 6 | 20 |
| 2015 July | 8 | 3 | 11 |
| 2015 June | 5 | 1 | 6 |
| 2015 May | 8 | 5 | 13 |
| 2015 April | 14 | 10 | 24 |
| 2015 March | 19 | 8 | 27 |
| 2014 August | 1 | 1 | 2 |
| 2014 July | 2 | 0 | 2 |
| 2014 June | 1 | 0 | 1 |
| 2014 May | 3 | 1 | 4 |
| 2014 January | 2 | 2 | 4 |
| 2013 December | 18 | 4 | 22 |
| 2013 November | 14 | 6 | 20 |
| 2013 October | 15 | 7 | 22 |
| 2013 September | 7 | 2 | 9 |
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