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fluorosis&#44; strontium overload or mixed types have also been described<span class="elsevierStyleSup">3</span>&#46;</p><p class="elsevierStylePara">It is well known that bone mineral density &#40;BMD&#41; is reduced in patients with chronic renal failure and they are at higher fracture risk<span class="elsevierStyleSup">6&#44;7</span>&#46; Uremic patients usually exhibit high plasma intact PTH and high serum concentration of biochemical markers of bone metabolism such as bone specific alkaline phosphatase &#40;bSAP&#41; and collagen breakdown products<span class="elsevierStyleSup">8</span>&#46;<span class="elsevierStyleSup"> </span>Some studies showed low 25OHD3 levels in uremic patients&#44; which is probably implicated in CKD-MBD<span class="elsevierStyleSup">9</span>&#46;</p><p class="elsevierStylePara">Leptin&#44; a hormone produced by fat tissue&#44; decreases appetite and increases basal metabolic rate&#46; Besides that&#44; leptin induces <span class="elsevierStyleItalic">in vitro</span> stem cells differentiation to osteoblasts and reduces osteoclastogenesis&#44; also having an <span class="elsevierStyleItalic">in vivo</span> positive effect on bone mass in mice<span class="elsevierStyleSup">10-13</span>&#46;<span class="elsevierStyleSup"> </span>Intracerebroventricular administration of leptin in wild or ob&#47;ob leptin deficient mice resulted in bone loss<span class="elsevierStyleSup">14</span>&#46;<span class="elsevierStyleSup"> </span>In renal failure serum leptin levels are increased&#44; as leptin is cleared by the kidneys<span class="elsevierStyleSup">15</span>&#46;<span class="elsevierStyleSup"> </span>In ESRD patients&#44; in particular&#44; the blood purification modality appears to affect leptin concentrations<span class="elsevierStyleSup">16</span>&#46;<span class="elsevierStyleSup"> </span>This fact might contribute to the development of CKD-MBD<span class="elsevierStyleSup">17-19</span>&#46;</p><p class="elsevierStylePara">The aim of current study is to investigate&#44; the bone mass density and the bone metabolism in hemodialysed patients as estimated by serum markers of bone metabolism &#40;bSAP and NTx&#41; and to correlate with serum Ca&#44; P&#44; PTH&#44; 25OHD3 and leptin&#46;</p><p class="elsevierStylePara">&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">SUBJECTS AND METHODS&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Patients</span></p><p class="elsevierStylePara">Thirty seven patients&#44; 18 postmenopausal female and 19 male&#44; on maintenance HD were included in the present study after their informed consent&#46; The study was performed during the period April-May&#46; Females were 43-73 years old&#44; mean age 56&#46;7 years and were on HD for 6-222 months with mean HD duration 68&#46;1 months&#46; Males were 41-79 years old&#44; mean age 58 years and were on HD for 24-207 months with mean HD duration 67&#46;1 months&#46; All the patients were treated by conventional HD 4-5 hours&#44; three times a week&#46; None of the patients had a past history of parathyroidectomy or renal transplantation&#44; of fracture or radiographic evidence of vertebral&#44; rib or hip fracture&#46; At the moment of the evaluation none of the patients&#44; in particular the postmenopausal women&#44; was receiving or had received previous to the study&#44; oestrogen or raloxifene&#44; calcitonin&#44; bisphosphonates&#44; PTH or corticosteroids&#46; Thirteen patients received an active vitamin D derivative &#40;one alpha&#41; orally&#46; None of the patients received vitamin K or aluminum hydroxide&#46; There was no clinical or biological evidence for other bone disease such as osteomalacia or Paget&#8217;s disease&#46; All patients were measured for BMD at lumbar spine and at femoral neck and for body weight and height and their body mass index &#40;BMI&#41; was calculated&#46; &#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Biochemistry</span></p><p class="elsevierStylePara">Pre-midweek dialysis blood sampling was collected in the morning from the arteriovenus fistula after a 12h fast&#46; The serum obtained after centrifugation was stored in aliquots at -20 <span class="elsevierStyleSup">o</span>C until assayed&#44; with measurements made immediately after thawing&#46; Serum calcium&#44; phosphorus&#44; total protein&#44; albumin&#44; urea&#44; creatinine&#44; magnesium and total alkaline phosphatase were determined routinely using an automatic analyzer&#46; Serum bSAP was measured by ELISA &#40;Metra BAP EIA&#44; sensitivity 0&#46;7 U&#47;l&#44; intra-assay variation 5&#46;8&#37;&#44; inter-assay variation 5&#46;2&#37;&#41; and serum NTx was also measured by ELISA &#40;Wampole Laboratories&#44; USA&#44; intra-assay variation 4&#46;6&#37;&#44; inter-assay variation 6&#46;9&#37;&#41;&#46; Serum bioactive PTH and 25OHD3 were measured by chemiluminescence&#8217;s assay &#40;Nichols advantage&#44; functional sensitivity &#8804;4 ng&#47;ml&#44; CV 20&#37; for bioactive PTH and functional sensitivity &#8804;7 ng&#47;ml&#44; CV 20&#37; for 25OHD3&#41;&#46; Serum leptin was measured by RIA &#40;Linco Research&#44; sensitivity 0&#46;5 ng&#47;ml&#44; intra-assay variation 4&#46;6&#37;&#44; inter-assay variation 5&#37;&#41;&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Bone mineral density</span></p><p class="elsevierStylePara">Bone mineral density &#40;BMD&#41; of the lumbar spine&#44; total hip&#44; femoral neck and trochanter were measured using Lunar DPX-L densitometer &#40;Lunar&#44; Madison&#44; Wis&#44; USA&#41;&#46; All BMD measurements were performed by the same experienced operator&#46; The densitometer was calibrated everyday with a standard phantom specimen&#46; BMD results were obtained in absolute values &#40;g&#47;cm<span class="elsevierStyleSup">2</span>&#41;&#44; in T score and in Z score&#46; T score is the number of standard deviations from the mean of a healthy young adult population &#40;20-40 years old&#41; and is used to determine osteoporosis or osteopenia&#46; Zscore is the number of standard deviations from the mean of a healthy age- and gender-matched normal population&#44; which allows the comparison of BMD between patients of different age and gender&#46; Osteoporosis was defined as a BMD T score at any site less than -2&#44;5 and osteopenia as a BMD Tscore between -1 and &#8211;2&#44;5&#46; The reference values were obtained from an Italian normal population&#44; similar to Greek normal population&#44; provided by Lunar&#46;&#160; &#160;&#160;&#160;&#160;&#160;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Statistical analysis</span></p><p class="elsevierStylePara">All results are shown as means &#177; SD&#44; unless otherwise indicated&#46; Correlations between variables were assessed using simple linear regression and p &#60;0&#46;05 was accepted as statistically significant&#46; Comparison of categorical variables was performed using chi-square analyses&#46;</p><p class="elsevierStylePara">&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">RESULTS</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Demographic and biochemical data</span></p><p class="elsevierStylePara">Table 1 depicts the demographic data for the 18 female patients and table 2 for the 19 male patients&#46; Table 3 depicts the biochemical data for all 37 patients&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Bone densinometric data</span></p><p class="elsevierStylePara">The prevalence of osteoporosis &#40;T score &#60;-2&#46;5&#41; at lumbar spine and femoral neck was 14&#46;3&#37; and 21&#46;4&#37; respectively&#46; The prevalence of osteopenia &#40;T score between &#8211;1 and &#8211;2&#46;5&#41; at the same sites was 32&#46;1&#37; and 50&#37; respectively&#46; Lumbar spine Z score&#160;&#40;m &#177; SD&#41; was -0&#46;09 &#177; 1&#46;69 and femoral neck Z- score was &#8211;0&#46;76 &#177; 1&#46;14&#46; &#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Bone markers&#44; PTH&#44; 25OHD3 and leptin</span></p><p class="elsevierStylePara">Serum levels of bone markers &#40;NTx and bSAP&#41; were very high &#40;table 3&#41;&#46; Serum PTH and phosphorus levels were also high as expected&#46; Serum 25OHD3 levels were low and the prevalence of vitamin D deficiency was 89&#46;2&#37; among patients&#46; Only 4 patients had normal 25OHD3 levels&#46; Serum leptin was increased particularly in women &#40;table 3&#41;&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Correlation of BMD with PTH&#44; leptin&#44; duration of hemodialysis&#44; body weight and BMI</span></p><p class="elsevierStylePara">Lumbar spine and femoral neck Z-score correlated significantly in a negative manner with serum PTH &#40;p &#60;0&#46;025&#41; &#40;figure 1&#44; figure 2&#41;&#46; Lumbar spine and femoral neck Z-score was not related with serum leptin or with the duration of hemodialysis&#46; We found that 10&#37; of lumbar spine Z-score and 22&#46;9&#37; of femoral neck Z-score variability is due to serum PTH levels&#46; No correlation was found between body weight or BMI and Z-score at any site&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Correlation of PTH with bone markers&#44; 25OHD3 and leptin</span>&#160;</p><p class="elsevierStylePara">Serum PTH correlated significantly in a positive manner with serum NTx and bSAP &#40;R &#61; 0&#46;715&#59; p &#60;0&#46;001 and R &#61; 0&#46;690&#59; p &#60;0&#46;001 respectively&#41; &#40;figure 3&#44; figure 4&#41;&#46; We found that 50&#37; of serum NTx and bSAP variability is due to PTH levels&#46; No correlation was found between serum PTH and 25OHD3 or leptin levels&#46; &#160;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Correlation of 25OHD3 with bone markers and leptin</span></p><p class="elsevierStylePara">No correlation was found between 25OHD3&#44; bone markers &#40;NTx and bSAP&#41; or leptin levels&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Correlation of leptin with bone markers&#44; BMI&#44; body weight&#44; age and duration of hemodialysis</span></p><p class="elsevierStylePara">Serum leptin was not correlated with bone markers &#40;NTx and bSAP&#41;&#46; As expected&#44; serum leptin levels were positively correlated with BMI &#40;R &#61; 0&#46;697&#59; p &#60;0&#46;001&#41; and with body weight &#40;R &#61; 0&#46;577&#59; p &#60;0&#46;001&#41; &#40;figure 5&#44; figure 6&#41;&#46; We also found that 48&#46;5&#37; of serum leptin variability is due to BMI&#46; Leptin levels had no correlation with age or hemodialysis duration&#46; Serum leptin had a positive correlation with serum creatinine &#40;R &#61; 0&#46;419&#59; p &#61; 0&#46;012&#41;&#46;</p><p class="elsevierStylePara">&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">DISCUSSION </span></p><p class="elsevierStylePara">The data on the effect of hemodialysis in end stage renal disease patients on bone density are limited&#46; To date most of the work has been focused on predialysis&#44; HD and kidney transplanted patients and scarce information is available for patients on peritoneal dialysis&#44; haemofiltration and haemodialfiltration<span class="elsevierStyleSup">20-23</span>&#46; The prevalence of osteoporosis in hemodialysed patients is quite variable and depends on several factors including the method used for BMD measurement&#44; the skeletal site and patients&#8217; characteristics&#46; Nonetheless&#44; most of the studies showed reduced BMD in HD patients&#44; which appears to be more pronounced than in peritoneal dialysis patients<span class="elsevierStyleSup">24</span>&#46; The prevalence of osteoporosis in HD patients has been estimated to be 13-29&#37; at lumbar spine<span class="elsevierStyleSup">4&#44;5&#44;24</span> and 16-19&#37; at femoral neck<span class="elsevierStyleSup">4</span>&#46; Our findings are in accordance with these studies&#46; Additionally&#44; we found a high prevalence of osteopenia particularly at femoral neck&#46; In CKD-MBD bone loss is site specific and in patients with uremic hyperparathyroidism&#44; PTH has a preferential effect on cortical bone<span class="elsevierStyleSup">25&#44;26</span>&#46;<span class="elsevierStyleSup"> </span></p><p class="elsevierStylePara">&#160;It has been reported that serum NTx is significantly higher in HD patients than in healthy individuals<span class="elsevierStyleSup">27</span> and appears to be the most reliable and useful bone resorption marker in renal osteodystrophy<span class="elsevierStyleSup">28</span>&#46; In the present study we found extremely high levels of serum NTx and a significant positive correlation between serum NTx and PTH which is in line with previous published results<span class="elsevierStyleSup">27&#44;28</span>&#46;</p><p class="elsevierStylePara">The clearance of bSAP is not performed by the kidney and serum bSAP concentration is therefore not affected by renal function&#46; In our study a number of patients exhibited slightly increased serum bSAP&#46; The significant positive correlation between serum bSAP and NTx with PTH probably suggests that the increased bone turnover is due to secondary hyperparathyroidism&#46;</p><p class="elsevierStylePara">Plasma 25OHD3 levels are often abnormally low in normal population&#44; particularly in the elderly<span class="elsevierStyleSup">29</span> and in unselected medical inpatients<span class="elsevierStyleSup">30</span>&#44; as well as in HD patients<span class="elsevierStyleSup">31</span>&#46; In our cohort of patients there was also a high prevalence of vitamin D deficiency&#46; Ghazali A et al in their study found that low plasma 25OHD3 appears to be a major risk factor for hyperparathyroidism and Looser&#8217;s zones independent of calcitriol levels<span class="elsevierStyleSup">9</span>&#46; Interestingly&#44; and in contrast&#44; we found no correlation between 25OHD3 and PTH or bone markers&#46;</p><p class="elsevierStylePara">Leptin&#44; an adipocyte-derived hormone&#44; is cleared by the kidney&#44; and thus&#44; plasma leptin levels are elevated in HD patients<span class="elsevierStyleSup">17</span>&#46; We also found increased serum leptin levels in our HD patients&#44; particularly in women&#44; which is in accordance with previous studies&#46; It has been reported that there is a link between leptin and bone metabolism in vitro and in vivo experiments<span class="elsevierStyleSup">10-12</span>&#46; Furthermore some studies in humans have shown a positive relationship between leptin and bone parameters<span class="elsevierStyleSup">32-34</span>&#44; while others have not<span class="elsevierStyleSup">35-37</span>&#46;<span class="elsevierStyleSup"> </span>In our study simple regression analysis showed no correlation between serum leptin and Z-score at lumbar spine and femoral neck&#46; Similarly&#44; no correlation was found between leptin and bone markers &#40;NTx and bSAP&#41;&#46; Serum leptin showed a significant positive correlation only with BMI and body weight as expected&#46;</p><p class="elsevierStylePara">In conclusion the prevalence of osteoporosis&#47;osteopenia is increased in HD patients and bone mineral density appears to correlate with high serum levels of bioactive PTH but not with 25OH vitamin D or high serum leptin&#46; Interestingly&#44; the duration of hemodialysis does not appear to affect bone density&#46; The impact of leptin on bone metabolism in HD patients remains to be elucidated with further studies&#46;</p><p class="elsevierStylePara">&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Conflict of interest</span></p><p class="elsevierStylePara">The authors declare they have no potential conflicts of interest related to the contents of this article&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15578&#95;en&#95;t1&#95;109163&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15578_en_t1_109163.jpg" alt="Demographic data in 18 female patients"></img></a></p><p class="elsevierStylePara">Table 1&#46; Demographic data in 18 female patients</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15579&#95;en&#95;t2109163&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15579_en_t2109163.jpg" alt="Demographic data in 19 male patients"></img></a></p><p class="elsevierStylePara">Table 2&#46; Demographic data in 19 male patients</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15580&#95;en&#95;t310916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15580_en_t310916.jpg" alt="Biochemical data in all patients"></img></a></p><p class="elsevierStylePara">Table 3&#46; Biochemical data in all patients</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15581&#95;en&#95;f110916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15581_en_f110916.jpg" alt="Lumbar spine Z score vs PTH&#46;"></img></a></p><p class="elsevierStylePara">Figure 1&#46; Lumbar spine Z score vs PTH&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15582&#95;en&#95;f210916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15582_en_f210916.jpg" alt="Femoral neck Z score vs PTH&#46;"></img></a></p><p class="elsevierStylePara">Figure 2&#46; Femoral neck Z score vs PTH&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15583&#95;en&#95;f310916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15583_en_f310916.jpg" alt="PTH vs NTx&#46;"></img></a></p><p class="elsevierStylePara">Figure 3&#46; PTH vs NTx&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15584&#95;en&#95;f410916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15584_en_f410916.jpg" alt="PTH vs bSAP&#46;"></img></a></p><p class="elsevierStylePara">Figure 4&#46; PTH vs bSAP&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15585&#95;en&#95;f510916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15585_en_f510916.jpg" alt="Leptin vs BMI&#46;"></img></a></p><p class="elsevierStylePara">Figure 5&#46; Leptin vs BMI&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15586&#95;en&#95;f610916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15586_en_f610916.jpg" alt="Leptin vs Body Weight&#46;"></img></a></p><p class="elsevierStylePara">Figure 6&#46; Leptin vs Body Weight&#46;</p>"
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        "resumen" => "<p class="elsevierStylePara"><span class="elsevierStyleBold">Antecedentes&#58; </span>Los trastornos del metabolismo &#243;seo en pacientes en hemodi&#225;lisis &#40;HD&#41; implican varios factores humorales&#44; de los cuales la funci&#243;n central recae sobre la hormona paratiroidea&#46; Cuando hay insuficiencia renal normalmente se detectan niveles elevados de leptina y su relaci&#243;n con el metabolismo &#243;seo est&#225; a&#250;n por esclarecer&#46; Investigamos la densidad mineral &#243;sea &#40;DMO&#41; y el metabolismo &#243;seo en relaci&#243;n con la hormona paratiroidea s&#233;rica&#44; el 25&#40;OH&#41;D3 y la leptina en pacientes en HD&#46; <span class="elsevierStyleBold">M&#233;todos&#58; </span>Medimos la fosfatasa alcalina &#243;sea &#40;FAO&#41;&#44; el telop&#233;ptido N&#44; la hormona paratiroidea&#44; el 25&#40;OH&#41;D3 y la leptina en 37 pacientes en HD&#46; Asimismo&#44; evaluamos el IMC y la DMO en la columna lumbar &#40;CL&#41; y en el cuello femoral &#40;CF&#41; mediante DXA&#46; Las evaluaciones estad&#237;sticas se basaron en an&#225;lisis de regresi&#243;n simples&#46; Entrecruzamiento del telop&#233;ptido N del col&#225;geno &#243;seo tipo I&#46; <span class="elsevierStyleBold">Resultados&#58;</span> 1&#41; De nuestros pacientes&#44; el 32&#44;1&#37; presentaba osteopenia en CL y 50&#37; en CF y el 14&#44;3&#37; y el 21&#44;4&#37; osteoporosis&#44; respectivamente&#46; El puntaje Z en CL o CF no estaba relacionado con la duraci&#243;n de la HD&#46; 2&#41; Los marcadores &#243;seos&#44; la hormona paratiroidea&#44; y los niveles de f&#243;sforo y leptina se vieron incrementados&#46; 3&#41; El 25&#40;OH&#41;D3 era bajo y no estaba relacionado con el telop&#233;ptido N&#44; la FAO o la hormona paratiroidea&#46; 4&#41; La hormona paratiroidea estaba correlacionada con los marcadores &#243;seos y con el puntaje Z en CL y CF&#46; 5&#41; La leptina no presentaba correlaci&#243;n con los marcadores &#243;seos o con el puntaje Z &#40;con excepci&#243;n del IMC&#41;&#46; <span class="elsevierStyleBold">Conclusiones&#58; </span>En nuestros pacientes en hemodi&#225;lisis&#44; los marcadores del metabolismo &#243;seo se vieron incrementados en relaci&#243;n con los niveles elevados de hormona paratiroidea s&#233;rica&#46; La elevada leptina s&#233;rica observada no estaba asociada al metabolismo &#243;seo&#46; Adem&#225;s&#44; la duraci&#243;n de la hemodi&#225;lisis no pareci&#243; afectar a la densidad &#243;sea&#46;<br /><br /></p>"
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        "resumen" => "<p class="elsevierStylePara"><span class="elsevierStyleBold">Background&#58;</span> Bone metabolism disorders in hemodialysed patients &#40;HD&#41; involve several humoral factors&#44; of which PTH plays the central role&#46; Leptin is usually found increased in renal failure and its link with bone metabolism&#160; has not been elucidated&#46; We investigated the BMD and bone metabolism&#160; in association with serum&#160; PTH&#44; 25OHD3 and leptin in HD patients&#46; <span class="elsevierStyleBold">Methods&#58; </span>We measured bone alkaline phosphatase &#40;bSAP&#41;&#44; cross linked N telopeptide of type 1 collagen &#40;NTx&#41;&#44; PTH&#44; 25OHD3 and leptin in 37 HD patients&#46; We also evaluated BMI and BMD in lumbar spine &#40;LS&#41; and in femoral neck &#40;FN&#41; by DXA&#46; Statistical evaluations were based on simple regression analysis&#46; <span class="elsevierStyleBold">Results&#58; </span>1&#41; Osteopenia was found in 32&#44;1&#37; in LS and 50&#37; in FN and osteoporosis in 14&#46;3&#37; and 21&#46;4&#37; of our patients&#44; respectively&#46; LS or FN Z score was not related&#160; to HD duration&#46; 2&#41; Bone markers&#44; PTH&#44; phosphorus and leptin levels were increased&#46; 3&#41; 25OHD3 was low and was not related to NTx&#44; bSAP or PTH&#46; 4&#41; PTH correlated with bone markers and Z score in LS and FN&#46; 5&#41; Leptin had no correlation with bone markers or Z score &#40;except BMI&#41;&#46; <span class="elsevierStyleBold">Conclusions&#58; </span>In our hemodialysed patients bone metabolism markers were increased in relation with high serum&#160; PTH levels&#46; The observed high serum leptin was not associated with bone metabolism&#46; Additionally the duration of hemodialysis did not appear to affect bone density&#46;<span class="elsevierStyleBold"></span></p>"
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Bone mineral density and bone metabolism in hemodialysis patients. Correlation with PTH, 25OHD3 and leptin
Densidad mineral y metabolismo óseo en pacientes en hemodiálisis. Correlación con la hormona paratifoidea, el 25(OH)D3 y la leptina
A.. Polymerisa, K.. Doumouchtsisa, E.. Grapsab
a Second Division of Endocrinology, Alexandra Hospital, Athens, Greece,
b Renal Unit, Alexandra Hospital, Athens, Greece,
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fluorosis&#44; strontium overload or mixed types have also been described<span class="elsevierStyleSup">3</span>&#46;</p><p class="elsevierStylePara">It is well known that bone mineral density &#40;BMD&#41; is reduced in patients with chronic renal failure and they are at higher fracture risk<span class="elsevierStyleSup">6&#44;7</span>&#46; Uremic patients usually exhibit high plasma intact PTH and high serum concentration of biochemical markers of bone metabolism such as bone specific alkaline phosphatase &#40;bSAP&#41; and collagen breakdown products<span class="elsevierStyleSup">8</span>&#46;<span class="elsevierStyleSup"> </span>Some studies showed low 25OHD3 levels in uremic patients&#44; which is probably implicated in CKD-MBD<span class="elsevierStyleSup">9</span>&#46;</p><p class="elsevierStylePara">Leptin&#44; a hormone produced by fat tissue&#44; decreases appetite and increases basal metabolic rate&#46; Besides that&#44; leptin induces <span class="elsevierStyleItalic">in vitro</span> stem cells differentiation to osteoblasts and reduces osteoclastogenesis&#44; also having an <span class="elsevierStyleItalic">in vivo</span> positive effect on bone mass in mice<span class="elsevierStyleSup">10-13</span>&#46;<span class="elsevierStyleSup"> </span>Intracerebroventricular administration of leptin in wild or ob&#47;ob leptin deficient mice resulted in bone loss<span class="elsevierStyleSup">14</span>&#46;<span class="elsevierStyleSup"> </span>In renal failure serum leptin levels are increased&#44; as leptin is cleared by the kidneys<span class="elsevierStyleSup">15</span>&#46;<span class="elsevierStyleSup"> </span>In ESRD patients&#44; in particular&#44; the blood purification modality appears to affect leptin concentrations<span class="elsevierStyleSup">16</span>&#46;<span class="elsevierStyleSup"> </span>This fact might contribute to the development of CKD-MBD<span class="elsevierStyleSup">17-19</span>&#46;</p><p class="elsevierStylePara">The aim of current study is to investigate&#44; the bone mass density and the bone metabolism in hemodialysed patients as estimated by serum markers of bone metabolism &#40;bSAP and NTx&#41; and to correlate with serum Ca&#44; P&#44; PTH&#44; 25OHD3 and leptin&#46;</p><p class="elsevierStylePara">&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">SUBJECTS AND METHODS&#160;</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Patients</span></p><p class="elsevierStylePara">Thirty seven patients&#44; 18 postmenopausal female and 19 male&#44; on maintenance HD were included in the present study after their informed consent&#46; The study was performed during the period April-May&#46; Females were 43-73 years old&#44; mean age 56&#46;7 years and were on HD for 6-222 months with mean HD duration 68&#46;1 months&#46; Males were 41-79 years old&#44; mean age 58 years and were on HD for 24-207 months with mean HD duration 67&#46;1 months&#46; All the patients were treated by conventional HD 4-5 hours&#44; three times a week&#46; None of the patients had a past history of parathyroidectomy or renal transplantation&#44; of fracture or radiographic evidence of vertebral&#44; rib or hip fracture&#46; At the moment of the evaluation none of the patients&#44; in particular the postmenopausal women&#44; was receiving or had received previous to the study&#44; oestrogen or raloxifene&#44; calcitonin&#44; bisphosphonates&#44; PTH or corticosteroids&#46; Thirteen patients received an active vitamin D derivative &#40;one alpha&#41; orally&#46; None of the patients received vitamin K or aluminum hydroxide&#46; There was no clinical or biological evidence for other bone disease such as osteomalacia or Paget&#8217;s disease&#46; All patients were measured for BMD at lumbar spine and at femoral neck and for body weight and height and their body mass index &#40;BMI&#41; was calculated&#46; &#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Biochemistry</span></p><p class="elsevierStylePara">Pre-midweek dialysis blood sampling was collected in the morning from the arteriovenus fistula after a 12h fast&#46; The serum obtained after centrifugation was stored in aliquots at -20 <span class="elsevierStyleSup">o</span>C until assayed&#44; with measurements made immediately after thawing&#46; Serum calcium&#44; phosphorus&#44; total protein&#44; albumin&#44; urea&#44; creatinine&#44; magnesium and total alkaline phosphatase were determined routinely using an automatic analyzer&#46; Serum bSAP was measured by ELISA &#40;Metra BAP EIA&#44; sensitivity 0&#46;7 U&#47;l&#44; intra-assay variation 5&#46;8&#37;&#44; inter-assay variation 5&#46;2&#37;&#41; and serum NTx was also measured by ELISA &#40;Wampole Laboratories&#44; USA&#44; intra-assay variation 4&#46;6&#37;&#44; inter-assay variation 6&#46;9&#37;&#41;&#46; Serum bioactive PTH and 25OHD3 were measured by chemiluminescence&#8217;s assay &#40;Nichols advantage&#44; functional sensitivity &#8804;4 ng&#47;ml&#44; CV 20&#37; for bioactive PTH and functional sensitivity &#8804;7 ng&#47;ml&#44; CV 20&#37; for 25OHD3&#41;&#46; Serum leptin was measured by RIA &#40;Linco Research&#44; sensitivity 0&#46;5 ng&#47;ml&#44; intra-assay variation 4&#46;6&#37;&#44; inter-assay variation 5&#37;&#41;&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Bone mineral density</span></p><p class="elsevierStylePara">Bone mineral density &#40;BMD&#41; of the lumbar spine&#44; total hip&#44; femoral neck and trochanter were measured using Lunar DPX-L densitometer &#40;Lunar&#44; Madison&#44; Wis&#44; USA&#41;&#46; All BMD measurements were performed by the same experienced operator&#46; The densitometer was calibrated everyday with a standard phantom specimen&#46; BMD results were obtained in absolute values &#40;g&#47;cm<span class="elsevierStyleSup">2</span>&#41;&#44; in T score and in Z score&#46; T score is the number of standard deviations from the mean of a healthy young adult population &#40;20-40 years old&#41; and is used to determine osteoporosis or osteopenia&#46; Zscore is the number of standard deviations from the mean of a healthy age- and gender-matched normal population&#44; which allows the comparison of BMD between patients of different age and gender&#46; Osteoporosis was defined as a BMD T score at any site less than -2&#44;5 and osteopenia as a BMD Tscore between -1 and &#8211;2&#44;5&#46; The reference values were obtained from an Italian normal population&#44; similar to Greek normal population&#44; provided by Lunar&#46;&#160; &#160;&#160;&#160;&#160;&#160;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Statistical analysis</span></p><p class="elsevierStylePara">All results are shown as means &#177; SD&#44; unless otherwise indicated&#46; Correlations between variables were assessed using simple linear regression and p &#60;0&#46;05 was accepted as statistically significant&#46; Comparison of categorical variables was performed using chi-square analyses&#46;</p><p class="elsevierStylePara">&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">RESULTS</span></p><p class="elsevierStylePara"><span class="elsevierStyleBold">Demographic and biochemical data</span></p><p class="elsevierStylePara">Table 1 depicts the demographic data for the 18 female patients and table 2 for the 19 male patients&#46; Table 3 depicts the biochemical data for all 37 patients&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Bone densinometric data</span></p><p class="elsevierStylePara">The prevalence of osteoporosis &#40;T score &#60;-2&#46;5&#41; at lumbar spine and femoral neck was 14&#46;3&#37; and 21&#46;4&#37; respectively&#46; The prevalence of osteopenia &#40;T score between &#8211;1 and &#8211;2&#46;5&#41; at the same sites was 32&#46;1&#37; and 50&#37; respectively&#46; Lumbar spine Z score&#160;&#40;m &#177; SD&#41; was -0&#46;09 &#177; 1&#46;69 and femoral neck Z- score was &#8211;0&#46;76 &#177; 1&#46;14&#46; &#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Bone markers&#44; PTH&#44; 25OHD3 and leptin</span></p><p class="elsevierStylePara">Serum levels of bone markers &#40;NTx and bSAP&#41; were very high &#40;table 3&#41;&#46; Serum PTH and phosphorus levels were also high as expected&#46; Serum 25OHD3 levels were low and the prevalence of vitamin D deficiency was 89&#46;2&#37; among patients&#46; Only 4 patients had normal 25OHD3 levels&#46; Serum leptin was increased particularly in women &#40;table 3&#41;&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Correlation of BMD with PTH&#44; leptin&#44; duration of hemodialysis&#44; body weight and BMI</span></p><p class="elsevierStylePara">Lumbar spine and femoral neck Z-score correlated significantly in a negative manner with serum PTH &#40;p &#60;0&#46;025&#41; &#40;figure 1&#44; figure 2&#41;&#46; Lumbar spine and femoral neck Z-score was not related with serum leptin or with the duration of hemodialysis&#46; We found that 10&#37; of lumbar spine Z-score and 22&#46;9&#37; of femoral neck Z-score variability is due to serum PTH levels&#46; No correlation was found between body weight or BMI and Z-score at any site&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Correlation of PTH with bone markers&#44; 25OHD3 and leptin</span>&#160;</p><p class="elsevierStylePara">Serum PTH correlated significantly in a positive manner with serum NTx and bSAP &#40;R &#61; 0&#46;715&#59; p &#60;0&#46;001 and R &#61; 0&#46;690&#59; p &#60;0&#46;001 respectively&#41; &#40;figure 3&#44; figure 4&#41;&#46; We found that 50&#37; of serum NTx and bSAP variability is due to PTH levels&#46; No correlation was found between serum PTH and 25OHD3 or leptin levels&#46; &#160;&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Correlation of 25OHD3 with bone markers and leptin</span></p><p class="elsevierStylePara">No correlation was found between 25OHD3&#44; bone markers &#40;NTx and bSAP&#41; or leptin levels&#46;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Correlation of leptin with bone markers&#44; BMI&#44; body weight&#44; age and duration of hemodialysis</span></p><p class="elsevierStylePara">Serum leptin was not correlated with bone markers &#40;NTx and bSAP&#41;&#46; As expected&#44; serum leptin levels were positively correlated with BMI &#40;R &#61; 0&#46;697&#59; p &#60;0&#46;001&#41; and with body weight &#40;R &#61; 0&#46;577&#59; p &#60;0&#46;001&#41; &#40;figure 5&#44; figure 6&#41;&#46; We also found that 48&#46;5&#37; of serum leptin variability is due to BMI&#46; Leptin levels had no correlation with age or hemodialysis duration&#46; Serum leptin had a positive correlation with serum creatinine &#40;R &#61; 0&#46;419&#59; p &#61; 0&#46;012&#41;&#46;</p><p class="elsevierStylePara">&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">DISCUSSION </span></p><p class="elsevierStylePara">The data on the effect of hemodialysis in end stage renal disease patients on bone density are limited&#46; To date most of the work has been focused on predialysis&#44; HD and kidney transplanted patients and scarce information is available for patients on peritoneal dialysis&#44; haemofiltration and haemodialfiltration<span class="elsevierStyleSup">20-23</span>&#46; The prevalence of osteoporosis in hemodialysed patients is quite variable and depends on several factors including the method used for BMD measurement&#44; the skeletal site and patients&#8217; characteristics&#46; Nonetheless&#44; most of the studies showed reduced BMD in HD patients&#44; which appears to be more pronounced than in peritoneal dialysis patients<span class="elsevierStyleSup">24</span>&#46; The prevalence of osteoporosis in HD patients has been estimated to be 13-29&#37; at lumbar spine<span class="elsevierStyleSup">4&#44;5&#44;24</span> and 16-19&#37; at femoral neck<span class="elsevierStyleSup">4</span>&#46; Our findings are in accordance with these studies&#46; Additionally&#44; we found a high prevalence of osteopenia particularly at femoral neck&#46; In CKD-MBD bone loss is site specific and in patients with uremic hyperparathyroidism&#44; PTH has a preferential effect on cortical bone<span class="elsevierStyleSup">25&#44;26</span>&#46;<span class="elsevierStyleSup"> </span></p><p class="elsevierStylePara">&#160;It has been reported that serum NTx is significantly higher in HD patients than in healthy individuals<span class="elsevierStyleSup">27</span> and appears to be the most reliable and useful bone resorption marker in renal osteodystrophy<span class="elsevierStyleSup">28</span>&#46; In the present study we found extremely high levels of serum NTx and a significant positive correlation between serum NTx and PTH which is in line with previous published results<span class="elsevierStyleSup">27&#44;28</span>&#46;</p><p class="elsevierStylePara">The clearance of bSAP is not performed by the kidney and serum bSAP concentration is therefore not affected by renal function&#46; In our study a number of patients exhibited slightly increased serum bSAP&#46; The significant positive correlation between serum bSAP and NTx with PTH probably suggests that the increased bone turnover is due to secondary hyperparathyroidism&#46;</p><p class="elsevierStylePara">Plasma 25OHD3 levels are often abnormally low in normal population&#44; particularly in the elderly<span class="elsevierStyleSup">29</span> and in unselected medical inpatients<span class="elsevierStyleSup">30</span>&#44; as well as in HD patients<span class="elsevierStyleSup">31</span>&#46; In our cohort of patients there was also a high prevalence of vitamin D deficiency&#46; Ghazali A et al in their study found that low plasma 25OHD3 appears to be a major risk factor for hyperparathyroidism and Looser&#8217;s zones independent of calcitriol levels<span class="elsevierStyleSup">9</span>&#46; Interestingly&#44; and in contrast&#44; we found no correlation between 25OHD3 and PTH or bone markers&#46;</p><p class="elsevierStylePara">Leptin&#44; an adipocyte-derived hormone&#44; is cleared by the kidney&#44; and thus&#44; plasma leptin levels are elevated in HD patients<span class="elsevierStyleSup">17</span>&#46; We also found increased serum leptin levels in our HD patients&#44; particularly in women&#44; which is in accordance with previous studies&#46; It has been reported that there is a link between leptin and bone metabolism in vitro and in vivo experiments<span class="elsevierStyleSup">10-12</span>&#46; Furthermore some studies in humans have shown a positive relationship between leptin and bone parameters<span class="elsevierStyleSup">32-34</span>&#44; while others have not<span class="elsevierStyleSup">35-37</span>&#46;<span class="elsevierStyleSup"> </span>In our study simple regression analysis showed no correlation between serum leptin and Z-score at lumbar spine and femoral neck&#46; Similarly&#44; no correlation was found between leptin and bone markers &#40;NTx and bSAP&#41;&#46; Serum leptin showed a significant positive correlation only with BMI and body weight as expected&#46;</p><p class="elsevierStylePara">In conclusion the prevalence of osteoporosis&#47;osteopenia is increased in HD patients and bone mineral density appears to correlate with high serum levels of bioactive PTH but not with 25OH vitamin D or high serum leptin&#46; Interestingly&#44; the duration of hemodialysis does not appear to affect bone density&#46; The impact of leptin on bone metabolism in HD patients remains to be elucidated with further studies&#46;</p><p class="elsevierStylePara">&#160;</p><p class="elsevierStylePara"><span class="elsevierStyleBold">Conflict of interest</span></p><p class="elsevierStylePara">The authors declare they have no potential conflicts of interest related to the contents of this article&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15578&#95;en&#95;t1&#95;109163&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15578_en_t1_109163.jpg" alt="Demographic data in 18 female patients"></img></a></p><p class="elsevierStylePara">Table 1&#46; Demographic data in 18 female patients</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15579&#95;en&#95;t2109163&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15579_en_t2109163.jpg" alt="Demographic data in 19 male patients"></img></a></p><p class="elsevierStylePara">Table 2&#46; Demographic data in 19 male patients</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15580&#95;en&#95;t310916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15580_en_t310916.jpg" alt="Biochemical data in all patients"></img></a></p><p class="elsevierStylePara">Table 3&#46; Biochemical data in all patients</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15581&#95;en&#95;f110916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15581_en_f110916.jpg" alt="Lumbar spine Z score vs PTH&#46;"></img></a></p><p class="elsevierStylePara">Figure 1&#46; Lumbar spine Z score vs PTH&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15582&#95;en&#95;f210916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15582_en_f210916.jpg" alt="Femoral neck Z score vs PTH&#46;"></img></a></p><p class="elsevierStylePara">Figure 2&#46; Femoral neck Z score vs PTH&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15583&#95;en&#95;f310916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15583_en_f310916.jpg" alt="PTH vs NTx&#46;"></img></a></p><p class="elsevierStylePara">Figure 3&#46; PTH vs NTx&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15584&#95;en&#95;f410916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15584_en_f410916.jpg" alt="PTH vs bSAP&#46;"></img></a></p><p class="elsevierStylePara">Figure 4&#46; PTH vs bSAP&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15585&#95;en&#95;f510916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15585_en_f510916.jpg" alt="Leptin vs BMI&#46;"></img></a></p><p class="elsevierStylePara">Figure 5&#46; Leptin vs BMI&#46;</p><p class="elsevierStylePara"><a href="grande&#47;10916&#95;16025&#95;15586&#95;en&#95;f610916&#46;jpg" class="elsevierStyleCrossRefs"><img src="10916_16025_15586_en_f610916.jpg" alt="Leptin vs Body Weight&#46;"></img></a></p><p class="elsevierStylePara">Figure 6&#46; Leptin vs Body Weight&#46;</p>"
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        "resumen" => "<p class="elsevierStylePara"><span class="elsevierStyleBold">Antecedentes&#58; </span>Los trastornos del metabolismo &#243;seo en pacientes en hemodi&#225;lisis &#40;HD&#41; implican varios factores humorales&#44; de los cuales la funci&#243;n central recae sobre la hormona paratiroidea&#46; Cuando hay insuficiencia renal normalmente se detectan niveles elevados de leptina y su relaci&#243;n con el metabolismo &#243;seo est&#225; a&#250;n por esclarecer&#46; Investigamos la densidad mineral &#243;sea &#40;DMO&#41; y el metabolismo &#243;seo en relaci&#243;n con la hormona paratiroidea s&#233;rica&#44; el 25&#40;OH&#41;D3 y la leptina en pacientes en HD&#46; <span class="elsevierStyleBold">M&#233;todos&#58; </span>Medimos la fosfatasa alcalina &#243;sea &#40;FAO&#41;&#44; el telop&#233;ptido N&#44; la hormona paratiroidea&#44; el 25&#40;OH&#41;D3 y la leptina en 37 pacientes en HD&#46; Asimismo&#44; evaluamos el IMC y la DMO en la columna lumbar &#40;CL&#41; y en el cuello femoral &#40;CF&#41; mediante DXA&#46; Las evaluaciones estad&#237;sticas se basaron en an&#225;lisis de regresi&#243;n simples&#46; Entrecruzamiento del telop&#233;ptido N del col&#225;geno &#243;seo tipo I&#46; <span class="elsevierStyleBold">Resultados&#58;</span> 1&#41; De nuestros pacientes&#44; el 32&#44;1&#37; presentaba osteopenia en CL y 50&#37; en CF y el 14&#44;3&#37; y el 21&#44;4&#37; osteoporosis&#44; respectivamente&#46; El puntaje Z en CL o CF no estaba relacionado con la duraci&#243;n de la HD&#46; 2&#41; Los marcadores &#243;seos&#44; la hormona paratiroidea&#44; y los niveles de f&#243;sforo y leptina se vieron incrementados&#46; 3&#41; El 25&#40;OH&#41;D3 era bajo y no estaba relacionado con el telop&#233;ptido N&#44; la FAO o la hormona paratiroidea&#46; 4&#41; La hormona paratiroidea estaba correlacionada con los marcadores &#243;seos y con el puntaje Z en CL y CF&#46; 5&#41; La leptina no presentaba correlaci&#243;n con los marcadores &#243;seos o con el puntaje Z &#40;con excepci&#243;n del IMC&#41;&#46; <span class="elsevierStyleBold">Conclusiones&#58; </span>En nuestros pacientes en hemodi&#225;lisis&#44; los marcadores del metabolismo &#243;seo se vieron incrementados en relaci&#243;n con los niveles elevados de hormona paratiroidea s&#233;rica&#46; La elevada leptina s&#233;rica observada no estaba asociada al metabolismo &#243;seo&#46; Adem&#225;s&#44; la duraci&#243;n de la hemodi&#225;lisis no pareci&#243; afectar a la densidad &#243;sea&#46;<br /><br /></p>"
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        "resumen" => "<p class="elsevierStylePara"><span class="elsevierStyleBold">Background&#58;</span> Bone metabolism disorders in hemodialysed patients &#40;HD&#41; involve several humoral factors&#44; of which PTH plays the central role&#46; Leptin is usually found increased in renal failure and its link with bone metabolism&#160; has not been elucidated&#46; We investigated the BMD and bone metabolism&#160; in association with serum&#160; PTH&#44; 25OHD3 and leptin in HD patients&#46; <span class="elsevierStyleBold">Methods&#58; </span>We measured bone alkaline phosphatase &#40;bSAP&#41;&#44; cross linked N telopeptide of type 1 collagen &#40;NTx&#41;&#44; PTH&#44; 25OHD3 and leptin in 37 HD patients&#46; We also evaluated BMI and BMD in lumbar spine &#40;LS&#41; and in femoral neck &#40;FN&#41; by DXA&#46; Statistical evaluations were based on simple regression analysis&#46; <span class="elsevierStyleBold">Results&#58; </span>1&#41; Osteopenia was found in 32&#44;1&#37; in LS and 50&#37; in FN and osteoporosis in 14&#46;3&#37; and 21&#46;4&#37; of our patients&#44; respectively&#46; LS or FN Z score was not related&#160; to HD duration&#46; 2&#41; Bone markers&#44; PTH&#44; phosphorus and leptin levels were increased&#46; 3&#41; 25OHD3 was low and was not related to NTx&#44; bSAP or PTH&#46; 4&#41; PTH correlated with bone markers and Z score in LS and FN&#46; 5&#41; Leptin had no correlation with bone markers or Z score &#40;except BMI&#41;&#46; <span class="elsevierStyleBold">Conclusions&#58; </span>In our hemodialysed patients bone metabolism markers were increased in relation with high serum&#160; PTH levels&#46; The observed high serum leptin was not associated with bone metabolism&#46; Additionally the duration of hemodialysis did not appear to affect bone density&#46;<span class="elsevierStyleBold"></span></p>"
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