Serum ghrelin and obestatin levels in HIV-infected patients: Effect of 36 weeks of antiretroviral treatment

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Rivera-Leon, Iris M. Llamas-Covarrubias, Raul A. Soria-Rodriguez, Sergio Sanchez-Enriquez, Luz A. González-Hernández, Jaime F. Andrade-Villanueva, Mara A. Llamas-Covarrubias" "autores" => array:7 [ 0 => array:3 [ "nombre" => "Edgar A." "apellidos" => "Rivera-Leon" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "1" "identificador" => "fn1" ] ] ] 1 => array:3 [ "nombre" => "Iris M." "apellidos" => "Llamas-Covarrubias" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "1" "identificador" => "fn1" ] ] ] 2 => array:3 [ "nombre" => "Raul A." "apellidos" => "Soria-Rodriguez" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Sergio" "apellidos" => "Sanchez-Enriquez" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 4 => array:3 [ "nombre" => "Luz A." "apellidos" => "González-Hernández" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 5 => array:3 [ "nombre" => "Jaime F." "apellidos" => "Andrade-Villanueva" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 6 => array:4 [ "nombre" => "Mara A." "apellidos" => "Llamas-Covarrubias" "email" => array:1 [ 0 => "mara.llamas@academicos.udg.mx" ] "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] 2 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "Departamento de Biología Molecular y Genómica, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Instituto de Investigación en Inmunodeficiencias y VIH, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Asociación Mexicana para el Fomento a Innovación, El Arenal, Jalisco, Mexico" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Niveles séricos de Ghrelina y Obestatina en pacientes infectados con VIH: efecto de 36 semanas de tratamiento antirretroviral" ] ] "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" => 2204 "Ancho" => 1500 "Tamanyo" => 153157 ] ] "descripcion" => array:1 [ "en" => "Ghrelin levels in HIV infected patients prior and post-36 weeks of ART. (A) Median ghrelin levels of HIV patients before (BL) and after 36 weeks of ART (W36), unpaired comparison was performed by means of Mann–Whitney test. (B) Paired comparison of ghrelin levels before and after 36 weeks of ART, Wilcoxon matched-pairs signed rank test was performed." ] ] ] "textoCompleto" => "IntroductionHuman immunodeficiency virus (HIV) infection affects more than 30 million people worldwide and constitutes an important health concern. The introduction of antiretroviral therapy (ART) has shown great effectiveness in controlling viral replication among HIV infected patients. Nevertheless, ARTs’ use has been associated with a number of important adverse effects that lead to a higher prevalence of cardiovascular risk factors.<a class="elsevierStyleCrossRef" href="#bib0150">1</a> This increased risk is partially related to metabolic disorders, including alterations in lipids and their metabolism.<a class="elsevierStyleCrossRef" href="#bib0155">2</a> Although there are consistent reports of lipid level alterations in ART treated patients,<a class="elsevierStyleCrossRefs" href="#bib0155">2–4</a> the mechanism of these alterations is not entirely clear.Ghrelin and obestatin are hormones coded in the same gene and produced mainly in the stomach and the gastrointestinal tract but with different functions.<a class="elsevierStyleCrossRefs" href="#bib0170">5,6</a>Ghrelin is mainly involved on growth hormone (GH) secretion, appetite stimulation and food intake; secondary functions include the promotion of gastric acid secretion, the increase in intestinal motility, regulation of: body weight, glucose and lipid metabolism, and suppression of inflammation. Its function as an orexigenic hormone is independent of the stimulatory effects on GH secretion.<a class="elsevierStyleCrossRefs" href="#bib0175">6–8</a> Ghrelin's food intake induction is exerted by the stimulation of hypothalamic neurons that expresses the ghrelin receptor GHS-R<a class="elsevierStyleCrossRef" href="#bib0190">9</a> and it also shows direct adipogenic and lipogenic effects in adipose tissue.<a class="elsevierStyleCrossRef" href="#bib0195">10</a> Further investigations have also demonstrated positive actions of ghrelin on blood pressure and cardiovascular system, involving promotion of diuresis and vasodilatation trough dependent and independent nitric oxide mechanisms and cardiac output by the activity of central nerve system.<a class="elsevierStyleCrossRefs" href="#bib0200">11,12</a>Obestatin has been implicated in suppressing food and water intake, decreasing body weight, promoting sleep, and decreasing the contractile force of jejunal muscle fibers.<a class="elsevierStyleCrossRefs" href="#bib0210">13–15</a> However, suppression of food intake action is controversial given the fact that recent studies have shown that obestatin putative receptor GPR39, is not expressed in the hypothalamus,<a class="elsevierStyleCrossRef" href="#bib0210">13</a> nonetheless, GPR39 is expressed on adipose tissue<a class="elsevierStyleCrossRef" href="#bib0225">16</a> and obestatin stimulates adipogenesis by the upregulation of adipogenic transcription factors such as PPAR gamma and C/EBP, and by the activation of Akt and further GLUT4 translocation in adipocytes.<a class="elsevierStyleCrossRef" href="#bib0230">17</a> Additionally, obestatin favors the survival of pancreatic beta cells thus increasing insulin secretion.<a class="elsevierStyleCrossRef" href="#bib0215">14</a> Both ghrelin and obestatin have a direct role in the regulation of hunger and satiety, as well as adipogenesis; alterations in their serum concentrations have been associated with very prevalent metabolic diseases such as obesity and DM2.<a class="elsevierStyleCrossRef" href="#bib0235">18</a>It has been shown that ghrelin levels are increased in HIV-infected patients who develop hypertriglyceridemia, suggesting a role for ghrelin on metabolic disorders associated with HIV infection<a class="elsevierStyleCrossRef" href="#bib0160">3</a>; nevertheless, the effect of ART has not been controlled and then, its impact on ghrelin or obestatin levels has not been studied so far.Then, it is not clear if ghrelin and obestatin have any say in the metabolic derangements that affect HIV-infected patients after the use of ART, and it is unknown if ART has any effect on circulating levels of these hormones. Therefore, the aim of this study was to determine the effect of 36 weeks of ART on ghrelin and obestatin circulating levels and its association with metabolic markers and cardiovascular risk in HIV+ patients. This will further develop our understanding of the pathogenesis behind metabolic disorders associated with HIV and their association with ART.Materials and methodsStudy populationThe study was designed as descriptive, observational, prospective and analytical. For that, 20 HIV+ ART naïve patients were assessed at baseline and prospectively followed for 36 weeks after initiation of ART. We included all patients older than 18 years that were deemed candidates for tenofovir/emtricitabine+lopinavir/ritonavir (FTC/TDF+LPV/r) as initial therapy by an infectious diseases specialist. By using the same ART regime, we aimed at treatment bias avoidance. Patients with any previous ART scheme, known primary resistance to any of the FTC/TDF or LPV/r medication, or active illicit drug use, were not included. The Atherogenic Index of Plasma (AIP) was used to determine cardiovascular risk as described elsewhere.<a class="elsevierStyleCrossRef" href="#bib0240">19</a>The study was approved by the local ethics committee in accordance to the Declaration of Helsinki and all patients provided written informed consent before enrollment.Biochemical and hormonal analysisBlood samples were drawn after an 8 hour fast at baseline and after 36 weeks of ART. A minimum treatment adherence of 80%, evaluated by direct questioning and remaining pills, was required to be included in the analysis. Concentrations of plasma glucose (FPG), total cholesterol (TC), high-density lipoprotein cholesterol (HDL-c), low-density lipoprotein cholesterol (LDL-c), very low-density lipoprotein cholesterol (VLDL-c), and triglycerides (TG) were obtained by standard biochemical methods (BioSystems®, Barcelona, Spain). Total plasma ghrelin and obestatin levels were measured separately by Enzyme Immunoassay with a detection range of 0.1–1000ng/mL each (RayBiothech, Inc., Norcross GA, USA); intra- and inter-assay coefficients of variation were <10% and <15% respectively, for both assays.Statistical analysisAll the analyses were performed using GraphPad Prism 6.0 (GraphPad Software®, La Jolla, CA, USA). Comparative analysis consisted of paired and unpaired non-parametric tests. To test for the association of changes on ghrelin or obestatin levels with changes on metabolic parameters Δvalues were calculated according to the formula: Δvalue=Week36 value−Baseline value; then, Spearman's correlation test was performed. A two-tailed p-value <0.05 was considered statistically significant.ResultsAll patients completed follow-up assessment at 36 weeks after ART initiation. Baseline demographic and HIV-relevant characteristics are depicted on <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>. Median age was 33 years and median baseline body mass index (BMI) was 24kg/m2 (interquartile range: 20–24kg/m2); as expected, all patients were on active viral replication at inclusion.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>After 36 weeks of ART, all patients achieved undetectable HIV RNA levels (median: 1.6log10copies/mL) and increased their CD4+ T cell counts (median: 544cells/μL). We observed a statistically significant increase of TC (p<0.001), LDL-c (p=0.019), HDL-c (p=0.003), VLDL-c (p=0.002) and TG levels (p=0.021) after ART. However, no changes were detected in BMI and FPG. The baseline median AIP was elevated [0.65 (0.31–0.88)] and no significant differences were perceived after 36 weeks of ART [0.70 (0.50–0.81)] (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>).<elsevierMultimedia ident="tbl0010"></elsevierMultimedia>Median baseline ghrelin levels were 56.52ng/ml (43.86–71.17ng/ml) and a slight increase was observed after 36 weeks of ART [64.15 (49.33–82.80) ng/ml], however, it was not statistically significant (p=0.194; <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>A). When performing a paired analysis, no significance was also observed (p=0.154; <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>B).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>On the other hand, median basal obestatin levels were 0.33pg/mL (0.10–0.50pg/mL) and after 36 weeks of ART, the levels increased to 0.75pg/mL (0.41–0.89pg/mL). Obestatin levels showed a statistically significant increase both in the unpaired and paired analyses (p<0.001 for both; <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>).<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Finally, to test the association of changes in ghrelin or obestatin serum levels with changes in metabolic parameters, we first calculated a delta (Δ) value for each parameter according to the formula: Δvalue=Week36 value−Baseline value. After that, we tested for correlations of obestatin and ghrelin Δvalues with Δvalues of metabolic parameters, results are shown in <a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>. Only a positive correlation was detected for ΔGhrelin and ΔObestatin values which indicates that an increase (or decrease) in ghrelin levels is accompanied by an increase (or decrease) in obestatin levels in the same patient. Nevertheless, no correlation was observed for ΔGhrelin or ΔObestatin and any other metabolic parameter.<elsevierMultimedia ident="tbl0015"></elsevierMultimedia>DiscussionGhrelin and obestatin are peptide hormones with apparently antagonic metabolic actions despite being coded on the same gene.<a class="elsevierStyleCrossRef" href="#bib0175">6</a> HIV-infected patients suffer from a number of metabolic disorders through the course of their illness and, although undeniably efficacious for viral replication control, ART exacerbates those alterations.<a class="elsevierStyleCrossRef" href="#bib0150">1</a> To date, the association between HIV-related metabolic disorders with ghrelin and obestatin and the possible influence that ART may have on these hormones remains elusive. Therefore, we aimed to determine the effect of 36 weeks of ART on ghrelin and obestatin levels and their association with metabolic parameters on HIV patients.The fact that HIV infected individuals on ART develop dyslipidemia (hypertriglyceridemia and hypercholesterolemia) has been thoroughly demonstrated, especially after the use of protease inhibitors.<a class="elsevierStyleCrossRef" href="#bib0245">20</a> In our study, individuals showed increased levels of cholesterol, triglycerides, HDL-c and LDL-c after 36 weeks of an ART scheme consisting of FTC/TDF+LPV/r. In addition, our data show that even before initiating ART, patients had an increased AIP index, thus a moderate to high cardiovascular risk, even higher than what has been reported for hypertensive or type 2 diabetes mellitus.<a class="elsevierStyleCrossRef" href="#bib0250">21</a>Also, we observed increased levels of both ghrelin and obestatin after ART, although only obestatin levels reached statistical significance. Despite ART associated ghrelin increase, HIV patients showed significantly lower ghrelin levels than lean healthy individuals as previously reported by our group (177.6±72.8pg/mL)<a class="elsevierStyleCrossRef" href="#bib0255">22</a> (a statistical comparison was performed with data and a p value of 0.002 was determined). The same is observed for obestatin, although in this case, the difference on HIV positive and HIV negative values is about three orders of magnitude (unpublished data; p<0.001).Even though literature is scarce in terms of why and what causes obestatin levels to change, we found an increment after ART, suggesting that some pathway involved in this treatment could favor obestatin production. Also, it has previously been shown that obestatin acts to restrict the development of foam cells formation by preventing low-density lipoproteins oxidation,<a class="elsevierStyleCrossRef" href="#bib0260">23</a> and it could be possible that the ART consequent dyslipidemia in which levels of LDL increases as well set an impulse to secrete more obestatin as a mean to avoid the possible cardiovascular damage.One study compared ghrelin levels among HIV infected patients with and without hypertriglyceridemia and found that hypertriglyceridemic patients have higher ghrelin levels and that ghrelin and triglyceride levels correlate among these patients,<a class="elsevierStyleCrossRef" href="#bib0160">3</a> suggesting a role for ghrelin on HIV-associated metabolic disorders. Nevertheless, all patients included in this study were under ART for long-term (>1 year), and ART schemes were heterogeneous; then, the role of ghrelin on ART-induced metabolic disorders was not examined.In agreement to our results, low ghrelin levels have been reported in HIV+ lipodystrophic patients when compared to non-lipodystrophic HIV+ patients.<a class="elsevierStyleCrossRef" href="#bib0265">24</a> This may suggest the presence of a process directly related to HIV infection that negatively affects ghrelin. On the other hand, Freitas et al., reported significantly increased ghrelin levels in HIV infected patients as compared to uninfected subjects<a class="elsevierStyleCrossRef" href="#bib0270">25</a> nevertheless, a heterogeneous group of HIV+ subjects in terms of ART and clinical characteristics of disease was included in that study and this may explain the differences observed. To the best of our knowledge, this is the first study that measures serum obestatin levels on HIV-infected patients and that explores the effect of ART on ghrelin and obestatin levels.The gastrointestinal tract is a fundamental site of HIV replication. In turn, this leads to HIV enteropathy which is characterized by the chronic inflammation of the intestinal mucosa due to the vast depletion of CD4+ T cells accompanied by a decreased mucosal repair and regeneration.<a class="elsevierStyleCrossRef" href="#bib0275">26</a> It is then possible that ghrelin and obestatin intestinal producing cells are affected in number or function and the reduction in levels observed in HIV patients is a consequence of this effect. The use of ART efficiently suppresses viral replication but is not as efficient in recovering the immune function of patients<a class="elsevierStyleCrossRef" href="#bib0280">27</a>; so, a partial recovery of intestinal immune and barrier function after ART may be reflected as an increase on ghrelin and obestatin levels, which nevertheless, remain lower than those of healthy subjects. HIV enteropathy also increases intestinal barrier permeability and microbial translocation, which favors a chronic systemic inflammatory state. Ghrelin protects against chronic intestinal inflammation<a class="elsevierStyleCrossRef" href="#bib0285">28</a> and the decrease of ghrelin levels seen on HIV patients may favor the persistence of HIV enteropathy thus potentially creating a vicious cycle.It is important to point out that ghrelin exists in two forms: acylated and unacylated ghrelin, and some studies have shown that these two forms have different functions. Acylated ghrelin is a hormone that promotes appetite leading to a positive energy balance and weight gain. This hormone has been proposed as an adaptive mechanism to caloric restriction conditions. On the other hand, unacylated ghrelin was first described as an inactive molecule, nevertheless it has shown to be an appetite inducer, temperature regulator, glucose-dependent insulin secretor, to be active in muscle atrophy, and to be involved in lipid metabolism, favoring lipid storage.<a class="elsevierStyleCrossRefs" href="#bib0175">6,29</a> Nevertheless, in this study we only measured total ghrelin, and this must be considered as a limitation.Other limitations of our study include the lack of other metabolic measures such as insulin or C reactive protein, as well as the restricted sample size. Nonetheless we identify other possible research questions that will better delineate the metabolic alterations seen in HIV patients. For example, a detailed body composition and an evaluation of hunger and satiety in HIV patients with respect to hormone levels and ART would be interesting to perform, as well as it would be to test the association of ghrelin and obestatin with HIV enteropathy and immune parameters of chronic inflammation both in the presence and absence of ART, and maybe in the future, the possible effect of ghrelin or obestatin analogs on such variables.More studies are needed in order to better understand the role of HIV infection and ART on ghrelin and obestatin levels and their function, as well as their metabolic effect and the immunologic interplay on the context of a chronic infection.ConclusionsThe use of ART during 36 weeks is associated with an increase in obestatin, but not ghrelin levels in HIV infected subjects.FundingThis research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.Conflict of interestsThe authors declare that there is no conflict of interests regarding the publication of this paper." "textoCompletoSecciones" => array:1 [ "secciones" => array:13 [ 0 => array:3 [ "identificador" => "xres1133368" "titulo" => "Abstract" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Material and methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusion" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1065694" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1133367" "titulo" => "Resumen" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Material y métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusión" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1065695" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Study population" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Biochemical and hormonal analysis" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Statistical analysis" ] ] ] 6 => array:2 [ "identificador" => "sec0030" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0035" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0040" "titulo" => "Conclusions" ] 9 => array:2 [ "identificador" => "sec0045" "titulo" => "Funding" ] 10 => array:2 [ "identificador" => "sec0050" "titulo" => "Conflict of interests" ] 11 => array:2 [ "identificador" => "xack385838" "titulo" => "Acknowledgment" ] 12 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2017-11-28" "fechaAceptado" => "2018-05-30" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1065694" "palabras" => array:4 [ 0 => "Ghrelin" 1 => "Obestatin" 2 => "Human immunodeficiency virus" 3 => "Dyslipidemia" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1065695" "palabras" => array:4 [ 0 => "Ghrelina" 1 => "Obestatina" 2 => "Virus de la inmunodeficiencia humana" 3 => "Dislipidemia" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "IntroductionPatients with HIV+ often present lipid disturbances. The role of ghrelin and obestatin in these lipid disturbances is not clear. The effect of antiretroviral (ART) drugs on those molecules is also unknown. This study measured ghrelin and obestatin levels, as well as metabolic markers, in patients with HIV+ before and after 36 weeks of ART. Material and methodsTwenty HIV-positive, ART-naïve patients who started a scheme consisting of tenofovir/emtricitabine+lopinavir/ritonavir were enrolled. Plasma samples were collected before and after 36 weeks of treatment. Serum ghrelin and obestatin levels were quantitated by ELISA; glucose, cholesterol, and triglyceride levels were measured by colorimetric and enzymatic methods, and cardiovascular risk was calculated by the atherogenic index of plasma (AIP). ResultsAll patients completed 36 weeks of ART. Total cholesterol (p<0.001), LDL-C (p=0.019), HDL-C (p=0.003), VLDL-C (p=0.002), and triglyceride levels (p=0.021) significantly increased after treatment. AIP revealed increased cardiovascular risk at baseline, which remained high after treatment. There was a statistically significant increase in obestatin level in the unpaired and paired analyses, while ghrelin levels only showed a trend to increase. Changes in ghrelin and obestatin levels positively correlated, but no correlation was seen with any metabolic parameter. ConclusionAfter 36 weeks of ART, patients showed an altered lipid profile, but there were no significant changes in cardiovascular risk. Ghrelin and obestatin levels increased after 36 weeks of ART, but the increase was only significant for obestatin. Changes in ghrelin and obestatin positively correlate." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Material and methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusion" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "IntroducciónLos pacientes con VIH+ frecuentemente presentan alteraciones del perfil lípidico. El papel de ghrelina y obestatina en estas complicaciones no está claro. El efecto del tratamiento antirretroviral (TAR) en dichas moléculas es desconocido. Este estudio determinó los niveles de ghrelina y obestatina, así como los parámetros metabólicos en pacientes VIH+ antes y después de 36 semanas del TAR. Material y métodosParticiparon 20 pacientes VIH+, vírgenes a TAR, que iniciaron con un esquema de tenofovir/emtricitabina + lopinavir/ritonavir. Se tomaron muestras de plasma antes y después de 36 semanas de tratamiento. Los niveles séricos de ghrelina y obestatina fueron cuantificados por ELISA, los parámetros bioquímicos fueron determinados por métodos colorimétricos, se evaluó el riesgo cardiovascular por medio del índice aterogénico del plasma (AIP). ResultadosLos pacientes completaron 36 semanas del TAR. Los niveles de colesterol total (p<0,001), c-LDL (p=0,019), c-HDL (p=0,003), c-VLDL (p=0,002) y triglicéridos (p=0,021) mostraron un incremento estadísticamente significativo posterior al tratamiento. El AIP reveló un riesgo cardiovascular alto. Los niveles de obestatina se incrementaron significativamente en el análisis pareado y no pareado; y ghrelina solo mostró tendencia al incremento. Los cambios en ghrelina y obestatina correlacionaron positivamente, sin embargo no correlacionaron con los parámetros metabólicos. ConclusiónLos pacientes VIH+ mostraron un perfil lipídico alterado después de 36 semanas del TAR. Los niveles de ghrelina y obestatina se incrementaron tras 36 semanas del TAR. El riesgo cardiovascular es persistente. Los cambios en ghrelina y obestatina mostraron una correlación positiva." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Material y métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusión" ] ] ] ] "NotaPie" => array:1 [ 0 => array:3 [ "etiqueta" => "1" "nota" => "These authors contributed equally to this work." "identificador" => "fn1" ] ] "multimedia" => array:5 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2204 "Ancho" => 1500 "Tamanyo" => 153157 ] ] "descripcion" => array:1 [ "en" => "Ghrelin levels in HIV infected patients prior and post-36 weeks of ART. (A) Median ghrelin levels of HIV patients before (BL) and after 36 weeks of ART (W36), unpaired comparison was performed by means of Mann–Whitney test. (B) Paired comparison of ghrelin levels before and after 36 weeks of ART, Wilcoxon matched-pairs signed rank test was performed." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2273 "Ancho" => 1511 "Tamanyo" => 171465 ] ] "descripcion" => array:1 [ "en" => "Obestatin levels in HIV infected patients prior and post-36 weeks of ART. (A) Median obestatin levels of HIV patients before (BL) and after 36 weeks of ART (W36), unpaired comparison was performed by means of Mann–Whitney test. (B) Paired comparison of obestatin levels before and after 36 weeks of ART, Wilcoxon matched-pairs signed rank test was performed." ] ] 2 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "Data are presented as median (interquartile range)." "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"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">HIV patients (n=20) \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Age (years) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">33 (30–36) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Gender (male/female) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">17/3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Time since HIV diagnosis (days) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">119 (33–307) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top">Clinical stage at baseline (n)</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">13 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">B \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="2" align="left" valign="top"></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">CD4+ T cell counts (cells/μL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">349 (203–413) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">HIV RNA (copies/mL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">84,944.5 (29,812.25–179,124.25) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">HIV RNA (log10 copies/mL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">5 (4.5–5.3) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1933723.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Clinical and demographical characteristics of study subjects." ] ] 3 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:1 [ "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"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Parameter \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Baseline \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">36 weeks post-ART \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">p \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">BMI (kg/m2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">24.00 (21.00–26.00) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">24.50 (20.00–26.25) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">NS \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">FPG (mg/dL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">85.50 (79.75–94.25) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">85.50 (80.25–89.25) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">NS \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Total cholesterol (mg/dL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">145.00 (130.00–165.30) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">176.50 (163.50–217.30) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top"><0.001 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">HDL-c (mg/dL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">30.00 (25.88–38.25) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">37.50 (33.00–47.25) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.003 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">LDL-c (mg/dL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">93.50 (76.73–102.40) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">106.50 (85.75–130.80) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.019 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">VLDL-c (mg/dL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">43.10 (69.00–214.30) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">133.50 (108.75–154.75) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.002 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Triglycerides (mg/dL) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">128.00 (69.00–214.30) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">171.50 (133.80–216.50) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.021 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">AIP \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.65 (0.31–0.88) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.70 (0.50–0.81) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">NS \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1933724.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Metabolic parameters of HIV+ patients before and after 36 weeks of ART." ] ] 4 => array:8 [ "identificador" => "tbl0015" "etiqueta" => "Table 3" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at3" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:1 [ "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"><th class="td-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Parameter \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col">Median Δvalue \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Correlation with ΔGhrelin</th><th class="td" title="table-head " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Correlation with ΔObestatin</th></tr><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">r coefficient \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">p \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">r coefficient \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">p \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ghrelin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7.34 (−11.34–27.58) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">– \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">– \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.49 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.028 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Obestatin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.32 (0.24–0.53) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.49 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.028 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">– \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">– \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Glucose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−3 (−6.5–3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.542 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.29 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.205 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cholesterol \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">26.5 (10.25–58.00) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.41 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.075 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.35 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.130 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Triglycerides \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">31.50 (−8.75–92.25) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.03 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.890 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.18 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.450 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">HDL-c \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.5 (−0.25–10.15) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.00 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.995 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.276 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">LDL-c \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8.00 (−5.35–36.53) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.27 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.251 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.23 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.337 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">VLDL-c \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">66.7 (1.7–112) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.22 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.345 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">−0.150 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.527 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1933725.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Correlation of changes in ghrelin or obestatin and metabolic parameters." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:29 [ 0 => array:3 [ "identificador" => "bib0150" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "The pathophysiology of HIV-/HAART-related metabolic syndrome leading to cardiovascular disorders: the emerging role of adipokines" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "J. 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Serum ghrelin and obestatin levels in HIV-infected patients: Effect of 36 weeks of antiretroviral treatment

Niveles séricos de Ghrelina y Obestatina en pacientes infectados con VIH: efecto de 36 semanas de tratamiento antirretroviral

Edgar A. Rivera-Leona,1, Iris M. Llamas-Covarrubiasa,1, Raul A. Soria-Rodriguezb, Sergio Sanchez-Enriqueza, Luz A. González-Hernándezb, Jaime F. Andrade-Villanuevab, Mara A. Llamas-Covarrubiasa,c,

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mara.llamas@academicos.udg.mx

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a Departamento de Biología Molecular y Genómica, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico

b Instituto de Investigación en Inmunodeficiencias y VIH, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico

c Asociación Mexicana para el Fomento a Innovación, El Arenal, Jalisco, Mexico

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          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Ghrelin levels in HIV infected patients prior and post-36 weeks of ART&#46; &#40;A&#41; Median ghrelin levels of HIV patients before &#40;BL&#41; and after 36 weeks of ART &#40;W36&#41;&#44; unpaired comparison was performed by means of Mann&#8211;Whitney test&#46; &#40;B&#41; Paired comparison of ghrelin levels before and after 36 weeks of ART&#44; Wilcoxon matched-pairs signed rank test was performed&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Human immunodeficiency virus &#40;HIV&#41; infection affects more than 30 million people worldwide and constitutes an important health concern&#46; The introduction of antiretroviral therapy &#40;ART&#41; has shown great effectiveness in controlling viral replication among HIV infected patients&#46; Nevertheless&#44; ARTs&#8217; use has been associated with a number of important adverse effects that lead to a higher prevalence of cardiovascular risk factors&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">1</span></a> This increased risk is partially related to metabolic disorders&#44; including alterations in lipids and their metabolism&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">2</span></a> Although there are consistent reports of lipid level alterations in ART treated patients&#44;<a class="elsevierStyleCrossRefs" href="#bib0155"><span class="elsevierStyleSup">2&#8211;4</span></a> the mechanism of these alterations is not entirely clear&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Ghrelin and obestatin are hormones coded in the same gene and produced mainly in the stomach and the gastrointestinal tract but with different functions&#46;<a class="elsevierStyleCrossRefs" href="#bib0170"><span class="elsevierStyleSup">5&#44;6</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Ghrelin is mainly involved on growth hormone &#40;GH&#41; secretion&#44; appetite stimulation and food intake&#59; secondary functions include the promotion of gastric acid secretion&#44; the increase in intestinal motility&#44; regulation of&#58; body weight&#44; glucose and lipid metabolism&#44; and suppression of inflammation&#46; Its function as an orexigenic hormone is independent of the stimulatory effects on GH secretion&#46;<a class="elsevierStyleCrossRefs" href="#bib0175"><span class="elsevierStyleSup">6&#8211;8</span></a> Ghrelin&#39;s food intake induction is exerted by the stimulation of hypothalamic neurons that expresses the ghrelin receptor GHS-R<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">9</span></a> and it also shows direct adipogenic and lipogenic effects in adipose tissue&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">10</span></a> Further investigations have also demonstrated positive actions of ghrelin on blood pressure and cardiovascular system&#44; involving promotion of diuresis and vasodilatation trough dependent and independent nitric oxide mechanisms and cardiac output by the activity of central nerve system&#46;<a class="elsevierStyleCrossRefs" href="#bib0200"><span class="elsevierStyleSup">11&#44;12</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Obestatin has been implicated in suppressing food and water intake&#44; decreasing body weight&#44; promoting sleep&#44; and decreasing the contractile force of jejunal muscle fibers&#46;<a class="elsevierStyleCrossRefs" href="#bib0210"><span class="elsevierStyleSup">13&#8211;15</span></a> However&#44; suppression of food intake action is controversial given the fact that recent studies have shown that obestatin putative receptor GPR39&#44; is not expressed in the hypothalamus&#44;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">13</span></a> nonetheless&#44; GPR39 is expressed on adipose tissue<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">16</span></a> and obestatin stimulates adipogenesis by the upregulation of adipogenic transcription factors such as PPAR gamma and C&#47;EBP&#44; and by the activation of Akt and further GLUT4 translocation in adipocytes&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">17</span></a> Additionally&#44; obestatin favors the survival of pancreatic beta cells thus increasing insulin secretion&#46;<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">14</span></a> Both ghrelin and obestatin have a direct role in the regulation of hunger and satiety&#44; as well as adipogenesis&#59; alterations in their serum concentrations have been associated with very prevalent metabolic diseases such as obesity and DM2&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">18</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">It has been shown that ghrelin levels are increased in HIV-infected patients who develop hypertriglyceridemia&#44; suggesting a role for ghrelin on metabolic disorders associated with HIV infection<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">3</span></a>&#59; nevertheless&#44; the effect of ART has not been controlled and then&#44; its impact on ghrelin or obestatin levels has not been studied so far&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Then&#44; it is not clear if ghrelin and obestatin have any say in the metabolic derangements that affect HIV-infected patients after the use of ART&#44; and it is unknown if ART has any effect on circulating levels of these hormones&#46; Therefore&#44; the aim of this study was to determine the effect of 36 weeks of ART on ghrelin and obestatin circulating levels and its association with metabolic markers and cardiovascular risk in HIV&#43; patients&#46; This will further develop our understanding of the pathogenesis behind metabolic disorders associated with HIV and their association with ART&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Study population</span><p id="par0035" class="elsevierStylePara elsevierViewall">The study was designed as descriptive&#44; observational&#44; prospective and analytical&#46; For that&#44; 20 HIV&#43; ART na&#239;ve patients were assessed at baseline and prospectively followed for 36 weeks after initiation of ART&#46; We included all patients older than 18 years that were deemed candidates for tenofovir&#47;emtricitabine<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>lopinavir&#47;ritonavir &#40;FTC&#47;TDF<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>LPV&#47;r&#41; as initial therapy by an infectious diseases specialist&#46; By using the same ART regime&#44; we aimed at treatment bias avoidance&#46; Patients with any previous ART scheme&#44; known primary resistance to any of the FTC&#47;TDF or LPV&#47;r medication&#44; or active illicit drug use&#44; were not included&#46; The Atherogenic Index of Plasma &#40;AIP&#41; was used to determine cardiovascular risk as described elsewhere&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">19</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">The study was approved by the local ethics committee in accordance to the Declaration of Helsinki and all patients provided written informed consent before enrollment&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Biochemical and hormonal analysis</span><p id="par0045" class="elsevierStylePara elsevierViewall">Blood samples were drawn after an 8 hour fast at baseline and after 36 weeks of ART&#46; A minimum treatment adherence of 80&#37;&#44; evaluated by direct questioning and remaining pills&#44; was required to be included in the analysis&#46; Concentrations of plasma glucose &#40;FPG&#41;&#44; total cholesterol &#40;TC&#41;&#44; high-density lipoprotein cholesterol &#40;HDL-c&#41;&#44; low-density lipoprotein cholesterol &#40;LDL-c&#41;&#44; very low-density lipoprotein cholesterol &#40;VLDL-c&#41;&#44; and triglycerides &#40;TG&#41; were obtained by standard biochemical methods &#40;BioSystems<span class="elsevierStyleSup">&#174;</span>&#44; Barcelona&#44; Spain&#41;&#46; Total plasma ghrelin and obestatin levels were measured separately by Enzyme Immunoassay with a detection range of 0&#46;1&#8211;1000<span class="elsevierStyleHsp" style=""></span>ng&#47;mL each &#40;RayBiothech&#44; Inc&#46;&#44; Norcross GA&#44; USA&#41;&#59; intra- and inter-assay coefficients of variation were &#60;10&#37; and &#60;15&#37; respectively&#44; for both assays&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Statistical analysis</span><p id="par0050" class="elsevierStylePara elsevierViewall">All the analyses were performed using GraphPad Prism 6&#46;0 &#40;GraphPad Software<span class="elsevierStyleSup">&#174;</span>&#44; La Jolla&#44; CA&#44; USA&#41;&#46; Comparative analysis consisted of paired and unpaired non-parametric tests&#46; To test for the association of changes on ghrelin or obestatin levels with changes on metabolic parameters &#916;values were calculated according to the formula&#58; &#916;value<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>Week36 value<span class="elsevierStyleHsp" style=""></span>&#8722;<span class="elsevierStyleHsp" style=""></span>Baseline value&#59; then&#44; Spearman&#39;s correlation test was performed&#46; A two-tailed <span class="elsevierStyleItalic">p</span>-value &#60;0&#46;05 was considered statistically significant&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Results</span><p id="par0055" class="elsevierStylePara elsevierViewall">All patients completed follow-up assessment at 36 weeks after ART initiation&#46; Baseline demographic and HIV-relevant characteristics are depicted on <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46; Median age was 33 years and median baseline body mass index &#40;BMI&#41; was 24<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span> &#40;interquartile range&#58; 20&#8211;24<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span>&#41;&#59; as expected&#44; all patients were on active viral replication at inclusion&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">After 36 weeks of ART&#44; all patients achieved undetectable HIV RNA levels &#40;median&#58; 1&#46;6<span class="elsevierStyleHsp" style=""></span>log<span class="elsevierStyleInf">10</span><span class="elsevierStyleHsp" style=""></span>copies&#47;mL&#41; and increased their CD4&#43; T cell counts &#40;median&#58; 544<span class="elsevierStyleHsp" style=""></span>cells&#47;&#956;L&#41;&#46; We observed a statistically significant increase of TC &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#44; LDL-c &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;019&#41;&#44; HDL-c &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;003&#41;&#44; VLDL-c &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;002&#41; and TG levels &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;021&#41; after ART&#46; However&#44; no changes were detected in BMI and FPG&#46; The baseline median AIP was elevated &#91;0&#46;65 &#40;0&#46;31&#8211;0&#46;88&#41;&#93; and no significant differences were perceived after 36 weeks of ART &#91;0&#46;70 &#40;0&#46;50&#8211;0&#46;81&#41;&#93; &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall">Median baseline ghrelin levels were 56&#46;52<span class="elsevierStyleHsp" style=""></span>ng&#47;ml &#40;43&#46;86&#8211;71&#46;17<span class="elsevierStyleHsp" style=""></span>ng&#47;ml&#41; and a slight increase was observed after 36 weeks of ART &#91;64&#46;15 &#40;49&#46;33&#8211;82&#46;80&#41; ng&#47;ml&#93;&#44; however&#44; it was not statistically significant &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;194&#59; <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>A&#41;&#46; When performing a paired analysis&#44; no significance was also observed &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;154&#59; <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>B&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">On the other hand&#44; median basal obestatin levels were 0&#46;33<span class="elsevierStyleHsp" style=""></span>pg&#47;mL &#40;0&#46;10&#8211;0&#46;50<span class="elsevierStyleHsp" style=""></span>pg&#47;mL&#41; and after 36 weeks of ART&#44; the levels increased to 0&#46;75<span class="elsevierStyleHsp" style=""></span>pg&#47;mL &#40;0&#46;41&#8211;0&#46;89<span class="elsevierStyleHsp" style=""></span>pg&#47;mL&#41;&#46; Obestatin levels showed a statistically significant increase both in the unpaired and paired analyses &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001 for both&#59; <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">Finally&#44; to test the association of changes in ghrelin or obestatin serum levels with changes in metabolic parameters&#44; we first calculated a delta &#40;&#916;&#41; value for each parameter according to the formula&#58; &#916;value<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>Week36 value<span class="elsevierStyleHsp" style=""></span>&#8722;<span class="elsevierStyleHsp" style=""></span>Baseline value&#46; After that&#44; we tested for correlations of obestatin and ghrelin &#916;values with &#916;values of metabolic parameters&#44; results are shown in <a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#46; Only a positive correlation was detected for &#916;Ghrelin and &#916;Obestatin values which indicates that an increase &#40;or decrease&#41; in ghrelin levels is accompanied by an increase &#40;or decrease&#41; in obestatin levels in the same patient&#46; Nevertheless&#44; no correlation was observed for &#916;Ghrelin or &#916;Obestatin and any other metabolic parameter&#46;</p><elsevierMultimedia ident="tbl0015"></elsevierMultimedia></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Discussion</span><p id="par0080" class="elsevierStylePara elsevierViewall">Ghrelin and obestatin are peptide hormones with apparently antagonic metabolic actions despite being coded on the same gene&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">6</span></a> HIV-infected patients suffer from a number of metabolic disorders through the course of their illness and&#44; although undeniably efficacious for viral replication control&#44; ART exacerbates those alterations&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">1</span></a> To date&#44; the association between HIV-related metabolic disorders with ghrelin and obestatin and the possible influence that ART may have on these hormones remains elusive&#46; Therefore&#44; we aimed to determine the effect of 36 weeks of ART on ghrelin and obestatin levels and their association with metabolic parameters on HIV patients&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">The fact that HIV infected individuals on ART develop dyslipidemia &#40;hypertriglyceridemia and hypercholesterolemia&#41; has been thoroughly demonstrated&#44; especially after the use of protease inhibitors&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">20</span></a> In our study&#44; individuals showed increased levels of cholesterol&#44; triglycerides&#44; HDL-c and LDL-c after 36 weeks of an ART scheme consisting of FTC&#47;TDF<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>LPV&#47;r&#46; In addition&#44; our data show that even before initiating ART&#44; patients had an increased AIP index&#44; thus a moderate to high cardiovascular risk&#44; even higher than what has been reported for hypertensive or type 2 diabetes mellitus&#46;<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">21</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">Also&#44; we observed increased levels of both ghrelin and obestatin after ART&#44; although only obestatin levels reached statistical significance&#46; Despite ART associated ghrelin increase&#44; HIV patients showed significantly lower ghrelin levels than lean healthy individuals as previously reported by our group &#40;177&#46;6<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>72&#46;8<span class="elsevierStyleHsp" style=""></span>pg&#47;mL&#41;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">22</span></a> &#40;a statistical comparison was performed with data and a <span class="elsevierStyleItalic">p</span> value of 0&#46;002 was determined&#41;&#46; The same is observed for obestatin&#44; although in this case&#44; the difference on HIV positive and HIV negative values is about three orders of magnitude &#40;unpublished data&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">Even though literature is scarce in terms of why and what causes obestatin levels to change&#44; we found an increment after ART&#44; suggesting that some pathway involved in this treatment could favor obestatin production&#46; Also&#44; it has previously been shown that obestatin acts to restrict the development of foam cells formation by preventing low-density lipoproteins oxidation&#44;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">23</span></a> and it could be possible that the ART consequent dyslipidemia in which levels of LDL increases as well set an impulse to secrete more obestatin as a mean to avoid the possible cardiovascular damage&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">One study compared ghrelin levels among HIV infected patients with and without hypertriglyceridemia and found that hypertriglyceridemic patients have higher ghrelin levels and that ghrelin and triglyceride levels correlate among these patients&#44;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">3</span></a> suggesting a role for ghrelin on HIV-associated metabolic disorders&#46; Nevertheless&#44; all patients included in this study were under ART for long-term &#40;&#62;1 year&#41;&#44; and ART schemes were heterogeneous&#59; then&#44; the role of ghrelin on ART-induced metabolic disorders was not examined&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">In agreement to our results&#44; low ghrelin levels have been reported in HIV&#43; lipodystrophic patients when compared to non-lipodystrophic HIV&#43; patients&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">24</span></a> This may suggest the presence of a process directly related to HIV infection that negatively affects ghrelin&#46; On the other hand&#44; Freitas et al&#46;&#44; reported significantly increased ghrelin levels in HIV infected patients as compared to uninfected subjects<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">25</span></a> nevertheless&#44; a heterogeneous group of HIV&#43; subjects in terms of ART and clinical characteristics of disease was included in that study and this may explain the differences observed&#46; To the best of our knowledge&#44; this is the first study that measures serum obestatin levels on HIV-infected patients and that explores the effect of ART on ghrelin and obestatin levels&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">The gastrointestinal tract is a fundamental site of HIV replication&#46; In turn&#44; this leads to HIV enteropathy which is characterized by the chronic inflammation of the intestinal mucosa due to the vast depletion of CD4&#43; T cells accompanied by a decreased mucosal repair and regeneration&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">26</span></a> It is then possible that ghrelin and obestatin intestinal producing cells are affected in number or function and the reduction in levels observed in HIV patients is a consequence of this effect&#46; The use of ART efficiently suppresses viral replication but is not as efficient in recovering the immune function of patients<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">27</span></a>&#59; so&#44; a partial recovery of intestinal immune and barrier function after ART may be reflected as an increase on ghrelin and obestatin levels&#44; which nevertheless&#44; remain lower than those of healthy subjects&#46; HIV enteropathy also increases intestinal barrier permeability and microbial translocation&#44; which favors a chronic systemic inflammatory state&#46; Ghrelin protects against chronic intestinal inflammation<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">28</span></a> and the decrease of ghrelin levels seen on HIV patients may favor the persistence of HIV enteropathy thus potentially creating a vicious cycle&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">It is important to point out that ghrelin exists in two forms&#58; acylated and unacylated ghrelin&#44; and some studies have shown that these two forms have different functions&#46; Acylated ghrelin is a hormone that promotes appetite leading to a positive energy balance and weight gain&#46; This hormone has been proposed as an adaptive mechanism to caloric restriction conditions&#46; On the other hand&#44; unacylated ghrelin was first described as an inactive molecule&#44; nevertheless it has shown to be an appetite inducer&#44; temperature regulator&#44; glucose-dependent insulin secretor&#44; to be active in muscle atrophy&#44; and to be involved in lipid metabolism&#44; favoring lipid storage&#46;<a class="elsevierStyleCrossRefs" href="#bib0175"><span class="elsevierStyleSup">6&#44;29</span></a> Nevertheless&#44; in this study we only measured total ghrelin&#44; and this must be considered as a limitation&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">Other limitations of our study include the lack of other metabolic measures such as insulin or C reactive protein&#44; as well as the restricted sample size&#46; Nonetheless we identify other possible research questions that will better delineate the metabolic alterations seen in HIV patients&#46; For example&#44; a detailed body composition and an evaluation of hunger and satiety in HIV patients with respect to hormone levels and ART would be interesting to perform&#44; as well as it would be to test the association of ghrelin and obestatin with HIV enteropathy and immune parameters of chronic inflammation both in the presence and absence of ART&#44; and maybe in the future&#44; the possible effect of ghrelin or obestatin analogs on such variables&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">More studies are needed in order to better understand the role of HIV infection and ART on ghrelin and obestatin levels and their function&#44; as well as their metabolic effect and the immunologic interplay on the context of a chronic infection&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Conclusions</span><p id="par0130" class="elsevierStylePara elsevierViewall">The use of ART during 36 weeks is associated with an increase in obestatin&#44; but not ghrelin levels in HIV infected subjects&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Funding</span><p id="par0135" class="elsevierStylePara elsevierViewall">This research did not receive any specific grant from funding agencies in the public&#44; commercial&#44; or not-for-profit sectors&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Conflict of interests</span><p id="par0140" class="elsevierStylePara elsevierViewall">The authors declare that there is no conflict of interests regarding the publication of this paper&#46;</p></span></span>"
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    "fechaRecibido" => "2017-11-28"
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            2 => "Human immunodeficiency virus"
            3 => "Dyslipidemia"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Patients with HIV&#43; often present lipid disturbances&#46; The role of ghrelin and obestatin in these lipid disturbances is not clear&#46; The effect of antiretroviral &#40;ART&#41; drugs on those molecules is also unknown&#46; This study measured ghrelin and obestatin levels&#44; as well as metabolic markers&#44; in patients with HIV&#43; before and after 36 weeks of ART&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Material and methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Twenty HIV-positive&#44; ART-na&#239;ve patients who started a scheme consisting of tenofovir&#47;emtricitabine<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>lopinavir&#47;ritonavir were enrolled&#46; Plasma samples were collected before and after 36 weeks of treatment&#46; Serum ghrelin and obestatin levels were quantitated by ELISA&#59; glucose&#44; cholesterol&#44; and triglyceride levels were measured by colorimetric and enzymatic methods&#44; and cardiovascular risk was calculated by the atherogenic index of plasma &#40;AIP&#41;&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">All patients completed 36 weeks of ART&#46; Total cholesterol &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#44; LDL-C &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;019&#41;&#44; HDL-C &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;003&#41;&#44; VLDL-C &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;002&#41;&#44; and triglyceride levels &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;021&#41; significantly increased after treatment&#46; AIP revealed increased cardiovascular risk at baseline&#44; which remained high after treatment&#46; There was a statistically significant increase in obestatin level in the unpaired and paired analyses&#44; while ghrelin levels only showed a trend to increase&#46; Changes in ghrelin and obestatin levels positively correlated&#44; but no correlation was seen with any metabolic parameter&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">After 36 weeks of ART&#44; patients showed an altered lipid profile&#44; but there were no significant changes in cardiovascular risk&#46; Ghrelin and obestatin levels increased after 36 weeks of ART&#44; but the increase was only significant for obestatin&#46; Changes in ghrelin and obestatin positively correlate&#46;</p></span>"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Los pacientes con VIH&#43; frecuentemente presentan alteraciones del perfil l&#237;pidico&#46; El papel de ghrelina y obestatina en estas complicaciones no est&#225; claro&#46; El efecto del tratamiento antirretroviral &#40;TAR&#41; en dichas mol&#233;culas es desconocido&#46; Este estudio determin&#243; los niveles de ghrelina y obestatina&#44; as&#237; como los par&#225;metros metab&#243;licos en pacientes VIH&#43; antes y despu&#233;s de 36 semanas del TAR&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Material y m&#233;todos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Participaron 20 pacientes VIH&#43;&#44; v&#237;rgenes a TAR&#44; que iniciaron con un esquema de tenofovir&#47;emtricitabina &#43; lopinavir&#47;ritonavir&#46; Se tomaron muestras de plasma antes y despu&#233;s de 36 semanas de tratamiento&#46; Los niveles s&#233;ricos de ghrelina y obestatina fueron cuantificados por ELISA&#44; los par&#225;metros bioqu&#237;micos fueron determinados por m&#233;todos colorim&#233;tricos&#44; se evalu&#243; el riesgo cardiovascular por medio del &#237;ndice aterog&#233;nico del plasma &#40;AIP&#41;&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Los pacientes completaron 36 semanas del TAR&#46; Los niveles de colesterol total &#40;p<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#44;001&#41;&#44; c-LDL &#40;p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;019&#41;&#44; c-HDL &#40;p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;003&#41;&#44; c-VLDL &#40;p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;002&#41; y triglic&#233;ridos &#40;p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;021&#41; mostraron un incremento estad&#237;sticamente significativo posterior al tratamiento&#46; El AIP revel&#243; un riesgo cardiovascular alto&#46; Los niveles de obestatina se incrementaron significativamente en el an&#225;lisis pareado y no pareado&#59; y ghrelina solo mostr&#243; tendencia al incremento&#46; Los cambios en ghrelina y obestatina correlacionaron positivamente&#44; sin embargo no correlacionaron con los par&#225;metros metab&#243;licos&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusi&#243;n</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Los pacientes VIH&#43; mostraron un perfil lip&#237;dico alterado despu&#233;s de 36 semanas del TAR&#46; Los niveles de ghrelina y obestatina se incrementaron tras 36 semanas del TAR&#46; El riesgo cardiovascular es persistente&#46; Los cambios en ghrelina y obestatina mostraron una correlaci&#243;n positiva&#46;</p></span>"
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          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Ghrelin levels in HIV infected patients prior and post-36 weeks of ART&#46; &#40;A&#41; Median ghrelin levels of HIV patients before &#40;BL&#41; and after 36 weeks of ART &#40;W36&#41;&#44; unpaired comparison was performed by means of Mann&#8211;Whitney test&#46; &#40;B&#41; Paired comparison of ghrelin levels before and after 36 weeks of ART&#44; Wilcoxon matched-pairs signed rank test was performed&#46;</p>"
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          "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Obestatin levels in HIV infected patients prior and post-36 weeks of ART&#46; &#40;A&#41; Median obestatin levels of HIV patients before &#40;BL&#41; and after 36 weeks of ART &#40;W36&#41;&#44; unpaired comparison was performed by means of Mann&#8211;Whitney test&#46; &#40;B&#41; Paired comparison of obestatin levels before and after 36 weeks of ART&#44; Wilcoxon matched-pairs signed rank test was performed&#46;</p>"
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                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">HIV patients<br>&#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>20&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Age &#40;years&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">33 &#40;30&#8211;36&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Gender &#40;male&#47;female&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">17&#47;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Time since HIV diagnosis &#40;days&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">119 &#40;33&#8211;307&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="2" align="left" valign="top"><span class="elsevierStyleItalic">Clinical stage at baseline &#40;n&#41;</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">13&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">B</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">C</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="2" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">CD4&#43; T cell counts &#40;cells&#47;&#956;L&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">349 &#40;203&#8211;413&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">HIV RNA &#40;copies&#47;mL&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">84&#44;944&#46;5 &#40;29&#44;812&#46;25&#8211;179&#44;124&#46;25&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">HIV RNA &#40;log</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">10 copies&#47;mL&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">5 &#40;4&#46;5&#8211;5&#46;3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Parameter&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Baseline&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">36 weeks post-ART&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">BMI &#40;kg&#47;m<span class="elsevierStyleSup">2</span>&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">24&#46;00 &#40;21&#46;00&#8211;26&#46;00&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">24&#46;50 &#40;20&#46;00&#8211;26&#46;25&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">NS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">FPG &#40;mg&#47;dL&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">85&#46;50 &#40;79&#46;75&#8211;94&#46;25&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">85&#46;50 &#40;80&#46;25&#8211;89&#46;25&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">NS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Total cholesterol &#40;mg&#47;dL&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">145&#46;00 &#40;130&#46;00&#8211;165&#46;30&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">176&#46;50 &#40;163&#46;50&#8211;217&#46;30&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#60;0&#46;001&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">HDL-c &#40;mg&#47;dL&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">30&#46;00 &#40;25&#46;88&#8211;38&#46;25&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">37&#46;50 &#40;33&#46;00&#8211;47&#46;25&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0&#46;003&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">LDL-c &#40;mg&#47;dL&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">93&#46;50 &#40;76&#46;73&#8211;102&#46;40&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">106&#46;50 &#40;85&#46;75&#8211;130&#46;80&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0&#46;019&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">VLDL-c &#40;mg&#47;dL&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">43&#46;10 &#40;69&#46;00&#8211;214&#46;30&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">133&#46;50 &#40;108&#46;75&#8211;154&#46;75&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0&#46;002&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Triglycerides &#40;mg&#47;dL&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">128&#46;00 &#40;69&#46;00&#8211;214&#46;30&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">171&#46;50 &#40;133&#46;80&#8211;216&#46;50&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0&#46;021&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">AIP&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;65 &#40;0&#46;31&#8211;0&#46;88&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;70 &#40;0&#46;50&#8211;0&#46;81&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">NS&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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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"><th class="td-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Parameter&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col">Median &#916;value&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Correlation with &#916;Ghrelin</th><th class="td" title="table-head  " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Correlation with &#916;Obestatin</th></tr><tr title="table-row"><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">r</span> coefficient&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">r</span> coefficient&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ghrelin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">7&#46;34 &#40;&#8722;11&#46;34&#8211;27&#46;58&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;49&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;028&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Obestatin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;32 &#40;0&#46;24&#8211;0&#46;53&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;49&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;028&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Glucose&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8722;3 &#40;&#8722;6&#46;5&#8211;3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8722;0&#46;14&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;542&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8722;0&#46;29&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;205&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cholesterol&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">26&#46;5 &#40;10&#46;25&#8211;58&#46;00&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8722;0&#46;41&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;075&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8722;0&#46;35&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;130&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Triglycerides&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">31&#46;50 &#40;&#8722;8&#46;75&#8211;92&#46;25&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;03&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;890&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;18&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;450&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">HDL-c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;5 &#40;&#8722;0&#46;25&#8211;10&#46;15&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;00&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;995&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8722;0&#46;26&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;276&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">LDL-c&nbsp;\t\t\t\t\t\t\n
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Article information

ISSN: 25300164
Original language: English

DOI:10.1016/j.endinu.2018.05.016

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Year/Month	Html	Pdf	Total

2024 October	9	2	11
2024 September	28	14	42
2024 August	27	5	32
2024 July	22	4	26
2024 June	21	4	25
2024 May	46	8	54
2024 April	22	11	33
2024 March	37	5	42
2024 February	20	2	22
2024 January	19	2	21
2023 December	20	2	22
2023 November	12	4	16
2023 October	20	5	25
2023 September	15	0	15
2023 August	5	0	5
2023 July	13	0	13
2023 June	13	2	15
2023 May	19	11	30
2023 April	10	1	11
2023 March	7	4	11
2023 February	10	7	17
2023 January	10	1	11
2022 December	17	4	21
2022 November	14	7	21
2022 October	20	8	28
2022 September	17	15	32
2022 August	12	5	17
2022 July	16	6	22
2022 June	20	6	26
2022 May	20	7	27
2022 April	8	8	16
2022 March	13	6	19
2022 February	6	6	12
2022 January	12	12	24
2021 December	22	8	30
2021 November	17	14	31
2021 October	16	14	30
2021 September	15	12	27
2021 August	7	11	18
2021 July	18	8	26
2021 June	26	14	40
2021 May	15	12	27
2021 April	15	11	26
2021 March	11	8	19
2021 February	10	4	14
2021 January	11	19	30
2020 December	19	15	34
2020 November	6	3	9
2020 October	13	5	18
2020 September	11	9	20
2020 August	12	15	27
2020 July	20	7	27
2020 June	16	8	24
2020 May	15	16	31
2020 April	10	7	17
2020 March	23	6	29
2020 February	21	10	31
2020 January	17	3	20
2019 December	11	4	15
2019 November	11	8	19
2019 October	11	4	15
2019 September	15	9	24
2019 August	10	3	13
2019 July	5	15	20
2019 February	6	4	10
2019 January	33	18	51

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