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Original article
Role of neuropeptide Y gene variant (rs161477) in liver histology in obese patients with non-alcoholic fatty liver disease
Papel de la variante genética del gen neuropéptido Y (rs161477) en la histología hepática en pacientes obesos con enfermedad por hígado graso no alcohólico
Rocio Allera,b,
Corresponding author
dadluis@yahoo.es

Corresponding author.
, Juan Jose López-Gomezb, Olatz Izaolab, David Primob, Daniel de Luisa,b
a Gastroenterology Department, Hospital Clínico Universitario of Valladolid, Spain
b Center of Investigation of Endocrinology and Nutrition, Medicine School and Department of Endocrinology and Nutrition, Hospital Clínico Universitario of Valladolid, Spain
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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">Non-alcoholic fatty liver disease &#40;NAFLD&#41; is one of the most common causes of chronic liver disease&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">1</span></a> NAFLD is an epidemic metabolic liver disease in a lot of countries&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">2</span></a> This liver entity is characterized by accumulation of fat in the liver that could be accompanied by inflammation and necrosis resembling alcoholic hepatitis in the absence of heavy alcohol consumption&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">3</span></a> The rate of NAFLD is strongly linked to obesity&#44; insulin resistance and metabolic syndrome&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">4</span></a> Liver tissue takes up circulating free fatty acids and low-density lipoproteins&#46; Consistently&#44; lipid storage contributes substantially to the liver triglyceride pool and liver steatosis&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">5</span></a> Its spectrum varies from simple steatosis to nonalcoholic steatohepatitis &#40;NASH&#41;&#44; which may progress to cirrhosis&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">6</span></a> In spite of high prevalence of NAFLD&#44; little is known about its pathogenesis&#46; Recent studies suggest that both environmental and genetic factors are involved in the progression and development of NAFLD&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Neuropeptide Y &#40;NPY&#41; is a 36-amino acid peptide neurotransmitter&#46; It is expressed by chromaffin cells as well as noradrenergic cells&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">7</span></a> It has been proposed that increased NPY signaling due to high NPY expression in the hypothalamus contributes to the development of diabetes mellitus type 2&#44; obesity and insulin resistance&#46;<a class="elsevierStyleCrossRefs" href="#bib0215"><span class="elsevierStyleSup">8&#8211;9</span></a> The <span class="elsevierStyleItalic">NPY</span> gene has four exons and it is located at 7p15&#46;1&#46; The main genetic variant in this gene is rs16147 &#40;G-399A&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">10</span></a> This genetic variant is associated with changes in NPY expression&#46; According previous studies might be responsible for more than half of the variation in the expression of NPY in vivo&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">11</span></a> The association between NPY rs16147 SNP and metabolic syndrome &#40;MetS&#41; has seldom been reported&#46; To our knowledge&#44; only one previous have explored the importance of rs16147&#58;T&#62;C for regulation of NPY gene expression and brain function in 314 young adults&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">12</span></a> Recently&#44; receptors of NPY have beed related to NAFLD fibrosis&#46; Of note&#44; in vitro study has demonstrated a reduced expression of Y1&#44; Y4 and Y5 NPY receptors&#44; whereas patients with NAFLD and advanced fibrosis &#40;F4 or cirrhosis&#41; had high expression of Y1&#44; Y4 and Y6 NPY receptors in the liver of patients with NAFLD without fibrosis&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">13</span></a> Given the limited information about the relation of the polymorphisms of <span class="elsevierStyleItalic">NPY</span> gene with NAFLD&#44; we aimed to evaluate the influence of polymorphism rs16147 of NPY gene on liver histology and biochemical parameters in patients with obesity and NAFLD&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Subjects and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Subjects</span><p id="par0015" class="elsevierStylePara elsevierViewall">The study group consisted of eighty nine Caucasian subjects with obesity&#46; Participants were selected according to the following inclusion criteria&#58; body mass index<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>30<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span>&#44; persistently elevated liver enzyme &#40;<span class="elsevierStyleItalic">ALT</span> alanine amino transferase<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>40<span class="elsevierStyleHsp" style=""></span>UI&#47;L or <span class="elsevierStyleItalic">AST</span> aspartate amino transferase<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>31<span class="elsevierStyleHsp" style=""></span>UI&#47;L&#41; with an abdominal ultrasound showing fatty liver&#46; Exclusion criteria were significant alcohol consumption &#40;&#62;30<span class="elsevierStyleHsp" style=""></span>g&#47;day in males and &#62;20<span class="elsevierStyleHsp" style=""></span>g&#47;day in females&#41;&#44; hepatitis B&#44; C&#44; cytomegalovirus&#44; Epstein Barr infections&#44; non-organ-specific autoantibodies&#44; diabetes mellitus&#44; medication &#40;blood-pressure lowering medication and statins&#41;&#44; hereditary defects &#40;iron and copper storage diseases and alpha 1-antitrypsin deficiency&#41; and medication that might induce steatosis &#40;glucocorticoids&#44; estrogens&#44; tamoxifen or valproic acid&#41;&#46; All participants signed an informed consent&#46; This protocol was conducted according to the guidelines laid down in the Declaration of Helsinki&#44; the local ethics committee &#40;HCUVA&#41; approved all procedures involving patients and patient data were codified to guarantee anonymity&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Liver histology</span><p id="par0020" class="elsevierStylePara elsevierViewall">The diagnosis of NAFLD was confirmed in all patients by percutaneous liver biopsy performed with a Menghini-type biopsy needle&#46; The biopsy site was located in the seventh or eighth intercostal space in the mid-axillary line&#46; The site was further confirmed with ultrasonography&#46; Skin&#44; subcutaneous tissue&#44; muscles&#44; and peritoneum were infiltrated with the local anesthetic &#40;procainamide 1&#37;&#44; 1<span class="elsevierStyleHsp" style=""></span>ml at most&#41;&#46; Vim&#8211;Silverman needle &#40;short trocar and cannula&#41; was introduced until the needle reached the liver&#46; Then&#44; trocar was removed and the 1<span class="elsevierStyleHsp" style=""></span>cm long biopsy punched out by the introduction of a longer cannula split longitudinally that turned around to cut the liver piece&#46; Biopsied liver was withdrawn through the cannula&#46; Liver samples were sectioned&#44; and stained with hematoxylin&#8211;eosin and Manson&#39;s trichrome&#46; NAFLD was defined histologically by the presence of minimum 5&#37; of steatosis on liver biopsy&#46; Steatosis was scored as 1 &#40;5&#8211;33&#37;&#41;&#44; 2 &#40;34&#8211;66&#37;&#41;&#44; or 3 &#40;&#62;66&#37;&#41;&#46; Lobular inflammation was scored as 0 &#40;presence of no inflammation&#41;&#44; 1 &#40;&#60;2 foci per 200&#215; field&#41;&#44; 2 &#40;2&#8211;4 foci per 200&#215; field&#41;&#44; or 3 based on &#62;4 foci per 200&#215; field&#46; Ballooning was scored as 0 &#40;no balloon cell&#41;&#44; 1&#40;few balloon cells&#41;&#44; and 2 &#40;many cells&#47;prominent ballooning cells&#41;&#46; A case presenting with at least grade 1 of each of the two features &#40;ballooning&#44; and lobular inflammation&#41; and steatosis &#40;NAS score&#41; was classified as non alcoholic steatohepatitis &#40;NASH&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">14</span></a> Fibrosis was scored as 0 &#40;no fibrosis&#41;&#44; 1 &#40;perisinusoidal or periportal&#41;&#44; 2 &#40;perisinusoidal and portal&#47;periportal&#41;&#44; 3 &#40;bridging&#41; and 4 &#40;cirrhosis&#41;&#46; To minimize inter-observer variability&#44; liver biopsy specimens were read by the same pathologist using the SAF &#40;Steatosis&#44; Activity&#44; Fibrosis&#41; score which assesses the grade of steatosis &#40;S&#44; from S0 to S3&#41;&#44; the grade of activity &#40;A from A0 to A4 by adding grades of ballooning and lobular inflammation&#44; both from 0 to 2&#41; and the stage of fibrosis &#40;F from F0 to F4&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">14</span></a></p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Genotyping and biochemical parameters</span><p id="par0025" class="elsevierStylePara elsevierViewall">DNA was extracted using commercial kit extraction &#40;Biorad&#44; LA&#44; CA&#41;&#46; Primers were designed with the Sequenom Assay Design v4 &#40;SEQUENOM&#44; Inc&#46;&#44; San Diego&#44; CA&#41;&#46; Genotyping for the rs16147 polymorphism was performed by chain reaction real time analysis&#46; This polymerase chain reaction &#40;PCR&#41; was carried out with 20&#8211;25<span class="elsevierStyleHsp" style=""></span>ng of genomic DNA&#44; 0&#46;1&#8211;0&#46;15<span class="elsevierStyleHsp" style=""></span>&#956;l each of oligonucleotide primer for rs16147 &#40;primer forward&#58; 5&#8242;-ACGTTGGATGCACAAAGAGGATTCAGGTGC-3&#8242; and reverse 5&#8242;-ACGTTGGATGAGCCCAGACGATTCTTGTC-3&#8242; in a 2-&#956;l final volume &#40;Termociclador Lifetecnologies&#44; LA&#44; CA&#41;&#46; DNA was denatured at 85<span class="elsevierStyleHsp" style=""></span>&#176;C for 5<span class="elsevierStyleHsp" style=""></span>min&#59; this was followed by 45 cycles of denaturation at 95<span class="elsevierStyleHsp" style=""></span>&#176;C for 15<span class="elsevierStyleHsp" style=""></span>s&#44; and annealing at 58&#46;1<span class="elsevierStyleHsp" style=""></span>&#176;C for 45<span class="elsevierStyleHsp" style=""></span>s&#41;&#46; The PCRs were run in a 2-&#956;l final volume containing 0&#46;1<span class="elsevierStyleHsp" style=""></span>&#956;l of iPLEx Termination mix &#40;Bio-Rad<span class="elsevierStyleSup">&#174;</span>&#44; San Diego&#44; CA&#41; with hot start Taq DNA polymerase&#46; Hardy Weinberg equilibrium was calculated with a statistical test &#40;Chi-square&#41;&#46; The variant of NPY gene was in Hardy Weinberg equilibrium &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;21&#41;&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Blood samples were collected in Na-EDTA tubes from patients after 12<span class="elsevierStyleHsp" style=""></span>h fast&#46; All samples were frozen at &#8722;80<span class="elsevierStyleHsp" style=""></span>&#176;C until laboratory testing&#46; Insulin was assessed by radioimmunoassay &#40;RIA&#41; &#40;RIA Diagnostic Corporation&#44; Los Angeles&#44; CA&#41; with a sensitivity of 0&#46;5<span class="elsevierStyleHsp" style=""></span>mUI&#47;L &#40;normal range 0&#46;5&#8211;30<span class="elsevierStyleHsp" style=""></span>mUI&#47;L&#41;<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">15</span></a> and the homeostasis model assessment for insulin resistance &#40;HOMA-IR&#41; was calculated using the next formula &#40;fasting insulin<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>fasting glucose concentrations&#47;22&#46;5&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">16</span></a> Plasma glucose levels&#44; total cholesterol&#44; triglyceride concentrations&#44; HDL cholesterol&#44; alanine amino transferase&#44; aspartate aminotransferase activity and Gama glutamine transferase were measured by enzymatic colorimetric assay Hitachi 902 analyser &#40;Hitachi Ltd&#46;&#44; Tokyo&#44; Japan&#41;&#46; LDL cholesterol was calculated using Friedewald formula&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">17</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">Resistin was measured by Enzyme-Linked Immunoabsorbent Assay &#40;ELISA&#41; &#40;Biovendor Laboratory&#44; Inc&#46;&#44; Brno&#44; Czech Republic&#41; with a sensitivity of 0&#46;2<span class="elsevierStyleHsp" style=""></span>ng&#47;ml and a normal range of 4&#8211;12<span class="elsevierStyleHsp" style=""></span>ng&#47;ml&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">18</span></a> Leptin was measured by ELISA &#40;Diagnostic Systems Laboratories&#44; Inc&#46;&#44; Texas&#44; USA&#41; with a sensitivity of 0&#46;05<span class="elsevierStyleHsp" style=""></span>ng&#47;ml and a normal range of 10&#8211;100<span class="elsevierStyleHsp" style=""></span>ng&#47;ml&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">19</span></a> Adiponectin was measured by ELISA &#40;R&#38;D systems&#44; Inc&#46;&#44; Minneapolis&#44; USA&#41; with a sensitivity of 0&#46;246<span class="elsevierStyleHsp" style=""></span>ng&#47;ml and a normal range of 8&#46;65&#8211;21&#46;43<span class="elsevierStyleHsp" style=""></span>ng&#47;ml&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">20</span></a></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Anthropometric measurements</span><p id="par0040" class="elsevierStylePara elsevierViewall">Body weight was assessed to an accuracy of 10<span class="elsevierStyleHsp" style=""></span>g and body mass index calculated as body weight in kg&#47;&#40;height in m<span class="elsevierStyleSup">2</span>&#41;&#46; Waist and hip circumferences to derive waist-to hip ratio &#40;WHR&#41; were measured&#44; too&#46; Bioimpedance was used to determine total body fat mass with an accuracy of 10<span class="elsevierStyleHsp" style=""></span>g<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">21</span></a> &#40;Akern&#44; EFG&#44; It&#41;&#46; Resistance and reactance were used to calculate total body water&#44; fat and fat-free mass&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Statistical analysis</span><p id="par0045" class="elsevierStylePara elsevierViewall">Sample size was calculated to detect a 15&#37; of differences in percentage of steatohepatitis between genotype groups in a dominant model&#46; Data are expressed as mean<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard deviation or as frequencies for categorical variables&#46; Categorical variables were analyzed with the Chi-square test&#44; with Yates correction as necessary&#44; and Fisher&#39;s test&#46; Continuous variables with normal distribution were analyzed with a two-tailed Student&#39;s <span class="elsevierStyleItalic">t</span>-test&#46; Non-parametric variables were analyzed with the Mann&#8211;Whitney <span class="elsevierStyleItalic">U</span> test&#46; Logistic regression analysis was used to test the association of rs16147 with liver histology &#40;steatosis&#44; fibrosis&#44; ballooning and lobulillar inflammation as independent dichotomy variables&#44; presence vs&#46; absence&#41; adjusted by sex&#44; age&#44; waist circumference and BMI&#46; It was calculate OR and 95&#37; confidence interval &#40;CI&#41;&#46; The genotype distribution was tested for deviation from Hardy&#8211;Weinberg equilibrium by a Chi-square test with 1 df &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46; The statistical analysis was performed for the combined <span class="elsevierStyleItalic">GA</span> and <span class="elsevierStyleItalic">AA</span> as a group and GG genotype as second group&#44; with a dominant model&#46; The statistical package was SPSS 15&#46;0 &#40;IL&#44; USA&#41;&#46; A <span class="elsevierStyleItalic">p</span>-value under 0&#46;05 was considered statistically significant&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall">Eighty nine patients gave informed consent and were enrolled in the study&#46; The mean age was 45&#46;1<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>8&#46;5 years and the mean body mass index &#40;BMI&#41; 37&#46;2<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>7&#46;0<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span>&#41;&#46; All subjects were weight stable during the 12 weeks period preceding the study &#40;body weight change&#44; 0&#46;16<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;1<span class="elsevierStyleHsp" style=""></span>kg&#41;&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Thirty two were men &#40;35&#46;2&#37;&#41; and 57 women &#40;64&#46;8&#37;&#41;&#46; Twenty three patients &#40;25&#46;0&#37;&#41; had the genotype GG &#40;wild type group&#41; and sixty six patients &#40;75&#37;&#41; patients GA &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>39&#41; or AA &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>27&#41; &#40;mutant type group&#41;&#46; The allelic frequency of A was 0&#46;53&#46; Age and gender distribution were similar in all groups&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> details the anthropometric variables&#46; No differences were reported between both genotype groups&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> details the classic biochemical parameters&#46; Lipid profile&#44; levels of adipokines&#44; liver biochemistry and glucose metabolism did not show statistical differences&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a> shows the histological findings according genotype&#46; Patients with A allele presented a lower percentage of lobulillar inflammation and steatohepatitis &#40;lobulillar inflammation plus ballooning&#41; than patients in the wild type group&#46; Patients with A allele showed lower SAF score than non-A allele carriers &#40;5&#46;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;7 points vs&#46; 4&#46;1<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;1 points&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#46; In the analysis of this score performed without fibrosis &#40;NAS score&#41;&#44; the same differences were also detected &#40;4&#46;5<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;8 points vs&#46; 3&#46;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;8 points&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#46;</p><elsevierMultimedia ident="tbl0015"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">Finally&#44; logistic regression analysis indicated that subjects with A-allele carriers presented lower probability of lobulillar inflammation &#40;OR 0&#46;11&#44; 95&#37; CI 0&#46;02&#8211;0&#46;84&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#41; and steatohepatitis &#40;OR 0&#46;39&#44; 95&#37; CI 0&#46;14&#8211;0&#46;86&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;04&#41; after adjusting by age&#44; sex and BMI&#46; If the BMI is replaced by the waist circumference&#44; the adjustment models are not modified&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Discussion</span><p id="par0080" class="elsevierStylePara elsevierViewall">The main finding of this cross-sectional study was the beneficial effect of A allele on liver histology&#46; This effect was independent of anthropometric and biochemical anthropometric and biochemical parameters&#46; Carriers of A allele exhibited lower percentage of steatohepatitis and lobulillar inflammation than non A allele carriers&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">NPY</span> gene is highly polymorphic&#44; some SNPs &#40;single nucleotide polymorphism&#41; of this gene have been associated with obesity and cardiovascular risk in some<a class="elsevierStyleCrossRefs" href="#bib0285"><span class="elsevierStyleSup">22&#8211;23</span></a> but not all studies&#46;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">24</span></a> The differences of these studies with our design is important&#59; firstly&#44; the population of the previous studies is no a Caucasian population and secondly&#44; the inclusion criteria in some studies are very different from ours&#46; For example&#44; patients of this study<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">24</span></a> had a documented coronary artery disease&#59; however the patients in our study had no coronary disease&#46; The age of the populations studied can also be an important factor in the findings found in the literature&#46; For example&#44; Zain et al&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">25</span></a> reported that A allele of rs16147 is associated with increased risk of obesity&#44; whereas A allele of rs5574 is associated with a reduced risk of obesity&#46; Olza et al&#46;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">26</span></a> reported similar results with rs16147 in a pediatric population&#46; Hohmann et al&#46;<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">27</span></a> reported a positive an increasing association between NPY promoter polymorphism and BMI during the course of development child growth&#44; too&#46; However&#44; all these findings have not been replicated in the adult population&#46;<a class="elsevierStyleCrossRefs" href="#bib0315"><span class="elsevierStyleSup">28&#44;29</span></a> Finally&#44; the samples evaluated are not comparable&#44; and in the particular case of our population of obese adults with cardiovascular risk&#44; other genetic and environmental factors may be involved in our findings&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">To our knowledge&#44; this research is the first to study the effect of this polymorphism of the <span class="elsevierStyleItalic">NPY</span> gene on liver histology in NAFLD subjects&#46; Our results show that the A allele influence on lobulillar inflammation and steatohepatitis independently of body weight&#44; age and sex&#46; A previous study evaluating the NPY pathway has shown that patients with NAFLD presented a positive correlation between saturated fatty acid intake and NPY levels&#46;<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">30</span></a> Perhaps an interaction between the dietary intake in our study participants and the NPY pathway could explain our histopathological findings&#46; On the other hand&#44; in our study did not observe between a relationship between adipokine levels and this SNP&#46; Nevertheless&#44; a negative correlation between NPY and adiponectinemia in NAFLD obese adolescents has been reported&#46;<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">31</span></a> Mutschler et al&#46;<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">27</span></a> reported an interaction of this SNP with leptin levels in females&#44; too&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">The precise molecular mechanisms underlying our observed association between rs16147 and liver histology are unclear&#46; Molecular studies have been developed to NPY after its discovery as an orexigenic neuropeptide&#44; since those initial studies&#44; NPY has also been found to affect energy expenditure independent of food intake&#46;<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">32</span></a> Perhaps this effect on energy expenditure can influence the accumulation of fat at the body and specifically in the liver tissue at the liver level&#46; Another potential hypothesis is the level of expression of different subtypes of NPY receptors in the liver at the hepatic level&#46; Sigala et al&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">13</span></a> have reported a relationship between expression of different types of NPY receptors and liver fibrosis&#46; Since NAFLD patients without fibrosis had reduced expression of Y1&#44; Y4 and Y5 NPY receptors&#44; whereas patients with NAFLD with cirrhosis had high expression of Y1&#44; Y4 and Y6 NPY receptors in an in vitro study&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">13</span></a> Other in vitro study<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">33</span></a> has shown the proliferative effects of NPY on hepatic stellate cells&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">A strength of our study&#44; it is the use of liver biopsy as a diagnostic method for NALFLD&#46; Our study has some limitations&#46; First&#44; we did not measure serum NPY levels in order to evaluate their direct effects on hepatic histology&#46; Secondly&#44; there are uncontrolled non-genetic factors such as exercise&#44; hormone levels&#44; and other lifestyle factors that could influence the relationships observed in our study&#44; none of which were taken to account in the present study&#46; For example&#44; different studies of dietary intervention<a class="elsevierStyleCrossRefs" href="#bib0345"><span class="elsevierStyleSup">34&#44;35</span></a> have shown that the metabolic response to diet is modulated depending on the presence of the allele A&#46; Thirdly&#44; other variants of this gene or other genes that are in imbalance can influence the results obtained in our findings&#46; Fourthly&#44; the difficulties in generalizing the results to other populations of patients with non-alcoholic fatty liver disease&#44; such as patients without significant obesity &#40;the mean BMI of the included patients was &#62;35<span class="elsevierStyleHsp" style=""></span>kg or with diabetes &#40;comorbidity frequently associated with NAFLD&#41;&#46; Finally&#44; our study cannot prove causality due to its cross-sectional design&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">In conclusion&#44; A variant of the polymorphism rs16147 of <span class="elsevierStyleItalic">NPY</span> gene is independently associated with a lower percentage of steatohepatitis and lobulillar inflammation in obesity subjects with proven biopsy NAFLD&#46; Therefore&#44; future studies are necessary to find out if it is necessary to evaluate different polymorphisms in the patient with NAFLD at the time of diagnosis and before initiating the treatment&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Funding</span><p id="par0115" class="elsevierStylePara elsevierViewall">There is no financial support&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Conflict of interest</span><p id="par0120" class="elsevierStylePara elsevierViewall">There is no conflict of interest&#46;</p></span></span>"
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          "titulo" => "Palabras clave"
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          "identificador" => "sec0005"
          "titulo" => "Introduction"
        ]
        5 => array:3 [
          "identificador" => "sec0010"
          "titulo" => "Subjects and methods"
          "secciones" => array:5 [
            0 => array:2 [
              "identificador" => "sec0015"
              "titulo" => "Subjects"
            ]
            1 => array:2 [
              "identificador" => "sec0020"
              "titulo" => "Liver histology"
            ]
            2 => array:2 [
              "identificador" => "sec0025"
              "titulo" => "Genotyping and biochemical parameters"
            ]
            3 => array:2 [
              "identificador" => "sec0030"
              "titulo" => "Anthropometric measurements"
            ]
            4 => array:2 [
              "identificador" => "sec0035"
              "titulo" => "Statistical analysis"
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        ]
        6 => array:2 [
          "identificador" => "sec0040"
          "titulo" => "Results"
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          "titulo" => "Discussion"
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          "identificador" => "sec0050"
          "titulo" => "Funding"
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        9 => array:2 [
          "identificador" => "sec0055"
          "titulo" => "Conflict of interest"
        ]
        10 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2018-05-17"
    "fechaAceptado" => "2018-10-16"
    "PalabrasClave" => array:2 [
      "en" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec1097882"
          "palabras" => array:5 [
            0 => "Adipokines"
            1 => "Obesity"
            2 => "NPY"
            3 => "RS16147"
            4 => "Non-alcoholic fatty liver disease"
          ]
        ]
      ]
      "es" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras clave"
          "identificador" => "xpalclavsec1097881"
          "palabras" => array:5 [
            0 => "Adipoquinas"
            1 => "Obesidad"
            2 => "NPY"
            3 => "RS16147"
            4 => "Enfermedad por h&#237;gado graso no alcoh&#243;lico"
          ]
        ]
      ]
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    "resumen" => array:2 [
      "en" => array:3 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Background and rationale</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">This study was intended to assess the influence of the rs16147 variant of the <span class="elsevierStyleItalic">NPY</span> gene on liver histology in patients with non-alcoholic fatty liver disease &#40;NAFLD&#41;&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Material and methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Eighty-nine patients with NAFLD were recruited into the study&#46; Serum chemistry tests were done including lipid profile&#44; transaminases&#44; adipokines&#44; and insulin resistance&#46; Genotype of polymorphism &#40;rs161477&#41; of the <span class="elsevierStyleItalic">NPY</span> gene was studied&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Twenty-three patients &#40;25&#46;0&#37;&#41; had the GG genotype &#40;wild type&#41; and sixty-six patients &#40;75&#37;&#41; the GA &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>39&#41; or AA &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>27&#41; &#40;mutant&#41; types&#46; Patients with A allele had a lower percentage of lobular inflammation and steatohepatitis &#40;lobular inflammation plus ballooning&#41; than those with wild genotype&#46; Patients with A allele showed lower SAF &#40;Steatosis&#44; Activity&#44; Fibrosis&#41; scores than non-A allele carriers &#40;5&#46;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;7 points vs&#46; 4&#46;1<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;1 points&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#46; In the analysis without fibrosis &#40;NAS score&#41;&#44; the same differences were detected &#40;4&#46;5<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;8 points vs&#46; 3&#46;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;8 points&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#46; In the logistic regression analysis A allele carriers showed lower odds for inflammation &#40;OR 0&#46;11&#44; 95&#37; CI 0&#46;02&#8211;0&#46;84&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#41; and steatohepatitis &#40;OR 0&#46;39&#44; 95&#37; CI 0&#46;14&#8211;0&#46;86&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;04&#41; after adjusting for age&#44; sex&#44; and body mass index&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">A variant of polymorphism rs16147 of the <span class="elsevierStyleItalic">NPY</span> gene is independently associated to a lower percentage of steatohepatitis and lobular inflammation in obese subjects with biopsy-proven NAFLD&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "abst0005"
            "titulo" => "Background and rationale"
          ]
          1 => array:2 [
            "identificador" => "abst0010"
            "titulo" => "Material and methods"
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          2 => array:2 [
            "identificador" => "abst0015"
            "titulo" => "Results"
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          3 => array:2 [
            "identificador" => "abst0020"
            "titulo" => "Conclusions"
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      "es" => array:3 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Antecedentes y justificaci&#243;n</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">El objetivo de nuestro estudio fue estudiar la influencia de la variante rs16147 del gen <span class="elsevierStyleItalic">NPY</span> en la histolog&#237;a hep&#225;tica en pacientes con enfermedad de h&#237;gado graso no alcoh&#243;lico &#40;NAFLD&#41;&#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">Se reclut&#243; una muestra de 89 pacientes con NAFLD&#46; Se realiz&#243; un an&#225;lisis bioqu&#237;mico del suero que incluy&#243; perfil lip&#237;dico&#44; transaminasas&#44; adipoquinas y resistencia a la insulina&#46; Se estudi&#243; el genotipo de polimorfismo &#40;rs161477&#41; del gen <span class="elsevierStyleItalic">NPY</span>&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Un total de 23 pacientes &#40;25&#44;0&#37;&#41; presentaron el genotipo GG &#40;genotipo salvaje&#41; y 66 pacientes &#40;75&#37;&#41; GA &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>39&#41; o AA &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>27&#41; &#40;genotipo mutante&#41;&#46; Los pacientes con alelo A presentaron un menor porcentaje de inflamaci&#243;n lobulillar y esteatohepatitis que los pacientes con genotipo salvaje&#46; Los pacientes con alelo A mostraron una puntuaci&#243;n m&#225;s baja de SAF &#40;esteatosis&#44; actividad&#44; fibrosis&#41; que los no portadores de alelos A &#40;5&#44;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#44;7 puntos vs&#46; 4&#44;1<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#44;1 puntos&#44; p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;01&#41;&#46; En el an&#225;lisis realizado sin fibrosis &#40;solo puntaje NAS&#41;&#44; tambi&#233;n se detectaron las mismas diferencias &#40;4&#44;5<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#44;8 puntos vs&#46; 3&#44;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#44;8 puntos&#44; p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;01&#41;&#46; En el an&#225;lisis de regresi&#243;n log&#237;stica a presencia del alelo A a una menor probabilidad de presentar con inflamaci&#243;n lobulillar &#40;OR 0&#44;11&#44; IC 95&#37;&#58; 0&#44;02-0&#44;84&#59; p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;03&#41; y esteatohepatitis &#40;OR 0&#44;39&#44; IC 95&#37;&#58; 0&#44;14-0&#44;86&#44; p<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#44;04&#41; despu&#233;s de ajustar por edad&#44; sexo e &#237;ndice de masa corporal&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La variante del polimorfismo rs16147 del gen <span class="elsevierStyleItalic">NPY</span> se asocia de forma independiente con un menor porcentaje de esteatohepatitis e inflamaci&#243;n lobulillar en sujetos obesos con NAFLD diagnosticado con biopsia&#46;</p></span>"
        "secciones" => array:4 [
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            "identificador" => "abst0025"
            "titulo" => "Antecedentes y justificaci&#243;n"
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            "identificador" => "abst0030"
            "titulo" => "Material y m&#233;todos"
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            "identificador" => "abst0035"
            "titulo" => "Resultados"
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          "leyenda" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">BMI&#58; body mass index&#46; WC&#58; waist circumference&#46; No statistical differences between groups&#46; Parameters expressed in &#40;mean<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard deviation&#41;&#46;</p>"
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                  \t\t\t\t\tvoid\n
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                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">GG &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>22&#41;&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">&#40;GA or AA&#41; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>66&#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">BMI &#40;kg&#47;m<span class="elsevierStyleSup">2</span>&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">129&#46;8<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>31&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">126&#46;5<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>23&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">122&#46;7<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>12&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">119&#46;7<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;5&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">Fat mass &#40;kg&#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;8<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>11&#46;1&nbsp;\t\t\t\t\t\t\n
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          "leyenda" => "<p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">LDL&#58; low density lipoprotein&#46; HDL&#58; high density lipoprotein&#46; Ch&#58; cholesterol&#46; TG&#58; triglycerides&#46; HOMA-IR&#58; homeostasis model assessment&#46; <span class="elsevierStyleItalic">ALT</span>&#58; alanine amino transferase&#46; <span class="elsevierStyleItalic">AST</span>&#58; aspartate amino transferase&#46; GGT&#58; gamma glutamil transferase&#46; No statistical differences between groups&#46; Parameters expressed in mean<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard deviation&#46;</p>"
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                  \t\t\t\t\tvoid\n
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                  \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">Glucose &#40;mg&#47;dl&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">99&#46;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>15&#46;3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">37&#46;0<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>7&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">180&#46;1<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>71&#46;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">160&#46;5<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>72&#46;7&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">6&#46;3<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \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">Fibrosis&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;85&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Histological parameters &#40;frequencies&#41;&#46;</p>"
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      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
          "bibliografiaReferencia" => array:35 [
            0 => array:3 [
              "identificador" => "bib0180"
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                  "contribucion" => array:1 [
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            4 => array:3 [
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                          "etal" => false
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                            0 => "C&#46; Sitticharoon"
                            1 => "S&#46; Chatree"
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            8 => array:3 [
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