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Original article
DNA methylation pattern of hypertriglyceridemic subjects
Patrón de metilación en ADN de sujetos hipertrigliceridémicos
Montse Guardiolaa,b,c,
Corresponding author
montse.guardiola@urv.cat

Corresponding author.
, Daiana Ibarretxea,b,c,d, Núria Planaa,b,c,d, Lluís Masanaa,b,c,d, Josep Ribaltaa,b,c
a Unitat de Recerca en Lípids i Arteriosclerosi, Departament de Medicina i Cirurgia, Universitat Rovira i Virgili, Reus, Tarragona, Spain
b Institut d'Investigació Sanitària Pere Virgili, Reus, Tarragona, Spain
c Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas, Madrid, Spain
d Unitat de Medicina Vascular i del Metabolisme, Hospital Universitari Sant Joan de Reus, Reus, Tarragona, 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">Genetic diagnosis based on identifying causal mutations with a large phenotypic effect is central to the diagnosis of the most severe forms of dyslipidaemia&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Chylomicronaemias or severe hypertriglyceridaemias are disorders with a complex aetiopathogenesis and defined by the abnormal presence of chylomicrons in fasting plasma&#44; producing triglyceride &#40;TG&#41; levels above 500&#8722;1000&#8239;mg&#47;dl&#46; We differentiate between 2 types of severe hypertriglyceridaemia&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Primary hypertriglyceridaemia usually has a monogenic cause and occurs in an autosomal recessive manner&#46; Five genes have now been identified as the main agents that code for key proteins in the TG lipolysis process&#58; <span class="elsevierStyleItalic">LPL</span>&#44; <span class="elsevierStyleItalic">APOC2</span>&#44; <span class="elsevierStyleItalic">GPIHBP1</span>&#44; <span class="elsevierStyleItalic">APOA5</span>&#44; and <span class="elsevierStyleItalic">LMF1</span>&#46; Certain mutations in these genes lead to chronically elevated TG levels&#46; Primary hypertriglyceridaemias have a prevalence of 1&#58;100&#44;000&#8722;1&#58;1&#44;000&#44;000&#59; they are of early onset&#59; their main clinical manifestation is pancreatitis&#44; which can be fatal&#59; and are not usually associated with elevated cardiovascular risk &#40;reviewed in Dron and Hegele<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a>&#41;&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">However&#44; secondary hypertriglyceridaemias have a higher prevalence &#40;1&#58;6&#46; 000&#41;&#59; they usually occur in adults&#59; at the metabolic level they present an increase in the number of chylomicrons&#44; together with VLDL&#44; and their remnants&#44; which means they are associated with an elevated cardiovascular risk&#59; we found a significant influence of secondary factors &#40;such as obesity&#44; metabolic syndrome&#44; diabetes&#44; or high alcohol intake&#44; among others&#41;&#59; and the genetic cause is more complex&#44; involving rare genetic variants in heterozygous form in the abovementioned 5 diagnostic genes&#44; together with variants in other TG-associated genes&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> It seems increasingly clear that this form of chylomicronaemia usually presents as a relatively mild hypertriglyceridaemia but associated with sporadic hyperlipaemic decompensations which&#44; due to certain lipid overload situations&#44; can multiply TG levels up to 10-fold or more&#44; only to decline rapidly again&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">There are clear differences between the two forms of severe hypertriglyceridaemia&#44; and therefore knowing the genetic cause may help to better characterise each patient&#8217;s phenotype&#44; better stratify their cardiovascular risk&#44; improve the identification of new patients&#44; and facilitate the most appropriate treatment for each patient&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Today&#44; the combination of various genetic strategies&#44; and the identification of new mutations with great phenotypic effect thanks to massive sequencing&#44; together with the design of genetic risk-scores that include several TG modulating variants&#44; have helped us improve in the characterisation of these patients&#44;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> but this still leaves around 30&#37; of cases of chylomicronaemia without a known genetic cause&#46;<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">6&#44;7</span></a> Therefore&#44; we do not rule out the possibility that other genetic components play a role in the development of this dyslipidaemia&#46; In this study&#44; we wanted to assess whether epigenetics may be involved in hypertriglyceridaemia&#44; and therefore we used a non-targeted strategy&#44; conducting an association study of the entire epigenome in samples from patients with severe hypertriglyceridaemia of no known genetic cause&#44; to identify new differentially methylated regions in the genome compared to a group of normolipaemic subjects&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Methodology</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Participants</span><p id="par0030" class="elsevierStylePara elsevierViewall">The group of hypertriglyceridaemic patients comprises 16 subjects who were referred to our centre&#8217;s lipid unit for the study of severe hypertriglyceridaemia&#46; These are patients with TG levels above 1000&#8239;mg&#47;dl and in whom none of the main causal mutations in the genes responsible for the most severe forms of hypertriglyceridaemia described in the literature were detected &#40;7 mutations in <span class="elsevierStyleItalic">LPL</span>&#44; 5 in <span class="elsevierStyleItalic">APOA5</span>&#44; 5 in <span class="elsevierStyleItalic">GPIHBP1</span>&#44; one in <span class="elsevierStyleItalic">APOC2</span> and 2 in <span class="elsevierStyleItalic">LMF1</span>&#41;&#46; These patients were compared with age- and sex-matched normolipaemic subjects who were part of the European VITAGE project&#44;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> which included apparently healthy men aged 20&#8211;75 years&#46; Subjects with chronic hepatic&#44; renal&#44; cardiopulmonary&#44; or neoplastic diseases were not included&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">The study was approved by our centre&#8217;s Ethics and Clinical Research Committee and all participants signed the informed consent form&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Samples</span><p id="par0040" class="elsevierStylePara elsevierViewall">Fasting blood samples were obtained from all participants and collected in EDTA plasma tubes &#40;Sarstedt&#44; Ltd&#46;&#44; N&#252;mbrecht&#44; Germany&#41;&#44; protected from light&#44; and centrifuged immediately at 1500&#8239;g for 10&#8239;min at 8&#8239;&#176;<span class="elsevierStyleSmallCaps">C</span>&#46; Plasma was separated and divided into aliquots&#46; The buffy coat was collected for genomic DNA extraction&#46; All samples were stored at &#8722;80&#8239;&#176;<span class="elsevierStyleSmallCaps">C</span> until the analytical tests were performed&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Analysis of plasma lipids</span><p id="par0045" class="elsevierStylePara elsevierViewall">Plasma TG and cholesterol concentrations were measured using enzyme kits &#40;F&#46; Hoffmann-La Roche&#44; Ltd&#46;&#41; adapted for a Cobas Mira autoanalyser &#40;F&#46; Hoffmann-La Roche&#44; Ltd&#46;&#41;&#46; We measured by immunoturbidometry apolipoprotein B and lipoprotein &#40;a&#41; using specific antibodies &#40;F&#46; Hoffmann-La Roche&#44; Ltd&#46;&#44; and Incstar Corp&#46;&#44; respectively&#41;&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">LDL-cholesterol was calculated using the Friedewald formula<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> and could not be calculated in all the hypertriglyceridaemic patients&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Full genome association study</span><p id="par0055" class="elsevierStylePara elsevierViewall">The cytosines were treated with sodium bisulphite to 500&#8239;ng of DNA to convert them to uracils&#44; whereas cytosines with a 5-methyl group do not react to sodium bisulphite&#46; The DNA was then hybridised to the Illumina&#174; array &#40;Infinium MethylationEPIC BeadChip&#41; following the instructions of the manufacturer&#39;s protocol&#46; The data of the intensities of each probe type on the array &#40;idat files&#41; were processed using the R package&#44; ChAMP version 2&#46;9&#46;10&#46;<a class="elsevierStyleCrossRefs" href="#bib0050"><span class="elsevierStyleSup">10&#44;11</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">Probes with a detection p-value above &#46;01 in one or more samples&#44; probes with a bead count &#60;3 in at least 5&#37; of the samples&#44; probes with close SNPs as identified in Zhou et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> probes that align at multiple locations as identified by Nordlund et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> and probes located on X or Y chromosomes were filtered&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">After filtering the probes&#44; intracellular type normalisation was performed using the beta-mixing quantile normalisation method<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> to avoid the bias introduced by the design of the Infinium type 2&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">After beta-mixture quantile normalisation&#44; using SVD analysis we assessed the magnitude of the batch effects&#46; We used Houseman correction<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> to correct for differences in methylation resulting from differences in cell heterogeneity&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a></p><p id="par0075" class="elsevierStylePara elsevierViewall">Differential methylation analysis was performed using the empirical Bayes moderated <span class="elsevierStyleItalic">t</span>-statistic &#40;for the outcome variable&#41; using the limma<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> package of R statistical software&#46; The &#946; value in the methylation experiments is the estimate of the methylation level using the ratio of the methylation probe intensity to the overall intensity&#44; while the M-value is a logarithmic transformation of the &#946; value&#46; The M-value was used for differential methylation analysis and the &#946; value for reporting the results&#44; which provided a more intuitive biological interpretation&#46; Raw <span class="elsevierStyleItalic">P</span>-values were adjusted using the Benjamini-Hochberg procedure&#44; and a cut-off false discovery rate of &#46;05 and delta Beta &#8805;5&#37; in the analyses related to the results was used as a statistically significant threshold&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Statistical analysis</span><p id="par0080" class="elsevierStylePara elsevierViewall">We used the Kolmogorov-Smirnov test to determine whether the quantitative variables were normally distributed&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Descriptive data for quantitative variables are presented as mean&#8239;&#177;&#8239;standard deviation or median &#40;interquartile range&#41;&#44; they are presented as percentages for the qualitative variables&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Correlations between the percentage of differentially methylated cytosine methylation with the different quantitative variables were adjusted by age&#44; sex&#44; and BMI&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Results and discussion</span><p id="par0095" class="elsevierStylePara elsevierViewall">There is now considerable evidence that epigenetic mechanisms play an important role in the regulation of metabolic phenotypes and in complex diseases such as dyslipidaemia&#44;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> although it remains unclear whether most of the described changes in DNA methylation are causal or a consequence of dyslipidaemia&#46; In the present study we used epigenetics as a tool to identify new genomic regions related to severe hypertriglyceridaemia&#44; and for this purpose we wanted to determine the pattern of DNA methylation in a group of patients with severe hypertriglyceridaemia without a clear genetic diagnosis&#44; to compare it with that of a group of normolipaemic subjects&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Both groups were matched by age and sex to minimise biological variability between groups&#46; The participants were middle-aged and mostly male&#46; As shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#44; the group of hypertriglyceridaemic patients had statistically significantly higher BMI&#44; higher TG concentration&#44; lower HDL-cholesterol concentration&#44; higher non-HDL-cholesterol concentration&#44; and higher glucose concentration than the normolipaemic subjects&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0105" class="elsevierStylePara elsevierViewall">We compared global methylation patterns between the samples from the hypertriglyceridaemic patients and the normolipaemic control subjects&#44; and identified 31 differentially methylated cytosines&#46; Most of the associations &#40;75&#37;&#41; represent cytosines that showed a lower degree of methylation &#40;hypomethylated&#41; in the hypertriglyceridaemic samples than in the normolipaemic subjects&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">All the differentially methylated cytosines are listed in <a class="elsevierStyleCrossRefs" href="#tbl0010">Tables 2 and 3</a>&#46; Some of these cytosines are located in genomic regions corresponding to a known gene&#44; and others are located in intergenic regions and could not be assigned to a gene&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="tbl0015"></elsevierMultimedia><p id="par0115" class="elsevierStylePara elsevierViewall">We highlight 4 cytosines located in known gene regions&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">Hypertriglyceridaemic patients have a 10&#37; decrease in the degree of methylation of the cytosine cg0363636183 which is located in the <span class="elsevierStyleItalic">F2RL3</span> gene -F2R Like Thrombin or Trypsin Receptor 3&#46; This gene is involved in processes associated with cardiovascular risk&#44; such as platelet activation&#44;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> intimal hyperplasia and inflammation associated with smoking&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> In particular&#44; hypomethylation of this cytosine cg0363636183 measured in blood cell DNA has been associated with an increased risk of cardiovascular mortality beyond the traditional risk factors in two large prospective studies&#46;<a class="elsevierStyleCrossRefs" href="#bib0100"><span class="elsevierStyleSup">20&#44;21</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall">We also identified 3 cytosines related to vesicular transport&#46; Hypertriglyceridaemic patients show a 10&#37; decrease in the degree of methylation of cg13824500 located in the <span class="elsevierStyleItalic">VTI1A</span> gene-Vesicle Transport through Interaction with T-SNAREs 1A&#46; This is a limiting gene in the formation of chylomicrons&#44; and more specifically in the transit of chylomicrons through the endoplasmic reticulum to the Golgi apparatus in the enterocyte&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> In sum&#44; the process of chylomicron formation takes place during intestinal lipid absorption&#46; In the endoplasmic reticulum of the cell&#44; pre-chylomicrons are formed by the binding of the synthesising apoB48 to complex lipids from the diet&#46; These pre-alkylomicrons now must reach the Golgi apparatus to mature&#44; and this is a complex and sequential process involving vesicles that fuse and interact with various ligands and receptor proteins in the Golgi complex&#46; The prechylomicrons move through the different cisternae of the complex thanks to the transporting vesicles&#44; and mature acquiring essential proteins and undergoing the necessary modifications until they form the chylomicrons found in the bloodstream&#46;<a class="elsevierStyleCrossRefs" href="#bib0115"><span class="elsevierStyleSup">23&#44;24</span></a> This process involves the participation of proteins such as SNARE and RAB&#44; among others&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">We also found that the cytosine cg26468118&#44; located in the <span class="elsevierStyleItalic">RAB20</span> gene-Member RAS Oncogene Family&#44; showed a 13&#37; lower degree of methylation in hypertriglyceridaemic subjects&#46; This gene is involved in processes of apical endocytosis and vesicle recycling&#44; and has recently also been linked to the arteriosclerotic process&#46; A paper designed to identify new genes involved in myocardial infarction identified RAB20 as overexpressed in carotid arteriosclerotic plaques&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a></p><p id="par0135" class="elsevierStylePara elsevierViewall">Finally&#44; cg21560722 is hypermethylated in hypertriglyceridaemic patients and is located in the <span class="elsevierStyleItalic">SBF2</span>-SET Binding Factor 2-gene&#44; which regulates the expression of several members of the RAB family and regulates SNARE proteins&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> This gene has also recently been identified in a full genome association study associated with the concentration of HDL particles determined by nuclear magnetic resonance in the Women&#39;s Genome Health Study cohort&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a></p><p id="par0140" class="elsevierStylePara elsevierViewall">We did not find that the other cytosines identified are located in genes or regions that have already been linked to TG metabolism or lipid metabolism in general&#44; or associated with cardiovascular disease or atherosclerosis&#46; Although&#44; pending validation of the present results&#44; we do not rule out the possibility that the role of these cytosines may be relevant&#44; which should be considered in future studies&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">In conclusion&#44; these results suggest that there are new genomic regions to consider when we perform the genetic characterisation of subjects with severe hypertriglyceridemias&#44; highlighting the genes related to the formation and maturation of chylomicrons in enterocytes&#46; However&#44; it should be noted that this study has several limitations&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">First&#44; these results need to be validated in other larger cohorts to confirm their association and relevance in the management of hypertriglyceridaemia&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">Another limitation is that the degree of methylation was determined on DNA extracted from peripheral blood mononuclear cells and we know that the DNA methylation profile and the regulation of gene expression are tissue specific&#46; However&#44; studies have shown that methylation determined in blood cells&#44; used as a potential marker in easily accessible tissue&#44; has some ability to reflect epigenetic effects occurring in target tissues&#46; Nevertheless&#44; we should not rule out some variation if studies are performed in target organs&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">We should also bear in mind that we do not know what function these methylations may have&#46; Generally&#44; we know that the greater the cytosine methylation&#44; the greater the repression of gene expression&#44; but it has also been described that DNA methylation in different genomic regions can influence gene regulation in different ways&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a></p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Funding</span><p id="par0165" class="elsevierStylePara elsevierViewall">This study was supported by a <span class="elsevierStyleGrantSponsor" id="gs0005">2018 FEA grant</span> for clinicoepidemiological research in arteriosclerosis&#44; and by the <span class="elsevierStyleGrantSponsor" id="gs0010">Instituto de Salud Carlos III</span> through project <span class="elsevierStyleGrantNumber" refid="gs0010">PI19&#47;00832</span> &#40;co-funded by the <span class="elsevierStyleGrantSponsor" id="gs0015">European Regional Development Fund&#47;European Social Fund</span>&#46; &#8220;A way of doing Europe&#8221;&#47;&#8220;ESF invests in your future&#8221;&#41;&#46; Cerca Programme&#47;Generalitat de Catalunya&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Conflict of interests</span><p id="par0170" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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    "fechaRecibido" => "2021-06-14"
    "fechaAceptado" => "2021-09-23"
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            2 => "Triglycerides"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Background</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Chylomicronemias are generally diagnosed genetically by genomic sequencing or screening for mutations in causal genes with a large phenotypic effect&#46; This strategy has allowed to improve the characterization of these patients&#44; but we still have 30&#37; of the patients without a conclusive genetic diagnosis&#46; This is why we hypothesize that by adding the epigenetic component we can improve the genetic diagnosis&#44; and for this we have explored the degree of methylation in the DNA of hypertriglyceridemic patients&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methodology</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Blood cell DNA was obtained from 16 hypertriglyceridemic patients and from 16 age- and sex-matched control subjects&#46; The degree of methylation in genome-wide DNA was determined using the Illumina Infinium Methylation EPIC Array Analysis&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">We identified 31 differentially methylated cytosines by comparing the methylation patterns presented by hypertriglyceridemic patients vs control subjects&#46; The cg03636183 in the F2RL3 gene was 10&#37; hypomethylated in hypertriglyceridemic patients&#44; and has previously been associated with an increased cardiovascular risk&#46; Cg13824500 is 10&#37; hypomethylated in hypertriglyceridemic patients and is located in VTI1A&#44; which is a limiting gene in the transit of chylomicrons in the enterocyte through the endoplasmic reticulum and the Golgi apparatus&#46; Cg26468118 in the RAB20 gene &#40;13&#37; hypomethylated&#41; and cg21560722 in the SBF2 gene &#40;33&#37; hypermethylated&#41; are involved in the regulation of Golgi apparatus vesicles&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Our results suggest that there are differentially methylated regions related to the formation of chylomicrons in hypertriglyceridemic patients&#46;</p></span>"
        "secciones" => array:4 [
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            "identificador" => "abst0005"
            "titulo" => "Background"
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          1 => array:2 [
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            "titulo" => "Methodology"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Antecedentes</span><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Las quilomicronemias generalmente se diagnostican gen&#233;ticamente mediante secuenciaci&#243;n gen&#243;mica o screening de mutaciones en genes causales con un gran efecto fenot&#237;pico&#46; Esta estrategia ha permitido mejorar la caracterizaci&#243;n de estos pacientes&#44; pero a&#250;n tenemos un 30&#37; de los pacientes sin un diagn&#243;stico gen&#233;tico concluyente&#46; Es por esto que hipotetizamos que a&#241;adiendo el componente epigen&#233;tico podemos mejorar el diagn&#243;stico gen&#233;tico y para ello hemos explorado el grado metilaci&#243;n en el DNA de pacientes hipertriglicerid&#233;micos&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Metodolog&#237;a</span><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">El DNA de c&#233;lulas sangu&#237;neas fue obtenido de 16 pacientes hipertriglicerid&#233;micos y de 16 sujetos control apareados por edad y sexo&#46; El grado de metilaci&#243;n en el DNA de todo el genoma fue determinado mediante el Illumina Infinium Methylation EPIC Array Analysis&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Identificamos 31 citosinas diferencialmente metiladas al comparar los patrones de metilaci&#243;n que presentaban los pacientes hipertriglicerid&#233;micos vs los sujetos control&#46; La cg03636183 en el gen <span class="elsevierStyleItalic">F2RL3</span> estaba un 10&#37; hipometilada en los pacientes hipertriglicerid&#233;micos&#44; y ha sido previamente asociada a un mayor riesgo cardiovascular&#46; La cg13824500 est&#225; un 10&#37; hipometilada en pacientes hipertriglicerid&#233;micos y se localiza en <span class="elsevierStyleItalic">VTI1A</span> que es un gen limitante en el tr&#225;nsito de los quilomicrones en el enterocito a trav&#233;s del ret&#237;culo endopl&#225;smico y el aparato de Golgi&#46; La cg26468118 en el gen <span class="elsevierStyleItalic">RAB20</span> &#40;13&#37; hipometilada&#41; y la cg21560722 en el gen <span class="elsevierStyleItalic">SBF2</span> &#40;33&#37; hipermetilada&#41; est&#225;n implicadas en la regulaci&#243;n de ves&#237;culas del aparato de Golgi&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Nuestros resultados sugieren que existen regiones diferencialmente metiladas relacionadas con la formaci&#243;n de los quilomicrones en pacientes hipertriglicerid&#233;micos&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Guardiola M&#44; Ibarretxe D&#44; Plana N&#44; Masana L&#44; Ribalta J&#46; Patr&#243;n de metilaci&#243;n en ADN de sujetos hipertriglicerid&#233;micos&#46; Clin Investig Arterioscler&#46; 2022&#59;34&#58;27&#8211;32&#46;</p>"
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        "mostrarFloat" => true
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          0 => array:3 [
            "identificador" => "at0005"
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          "leyenda" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Data presented as mean&#8239;&#177;&#8239;SD or median &#40;IQR&#41; for the quantitative variables&#46;</p>"
          "tablatextoimagen" => array:1 [
            0 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Hypertrigliceridaemic &#40;n&#8239;&#61;&#8239;16&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Normolipaemic &#40;n&#8239;&#61;&#8239;16&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Age&#44; years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">50&#46;19&#8239;&#177;&#8239;11&#46;36&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">51&#46;95&#8239;&#177;&#8239;9&#46;65&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Sex&#44; &#37; men&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">94&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">100&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Body mass index&#44; kg&#47;m<span class="elsevierStyleSup">2</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">29&#46;93&#8239;&#177;&#8239;4&#46;94&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">25&#46;95 &#40;2&#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="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Total cholesterol&#44; mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">220&#46;50 &#40;77&#46;00&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">215&#46;06&#8239;&#177;&#8239;36&#46;68&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">LDL cholesterol&#44; mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">87&#46;00 &#40;95&#46;00&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">140&#46;93&#8239;&#177;&#8239;27&#46;03&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">HDL cholesterol&#44; mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&#46;00 &#40;13&#46;00&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">54&#46;05&#8239;&#177;&#8239;14&#46;67&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Non-HDL cholesterol&#44; mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">198&#46;00 &#40;82&#46;25&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">161&#46;38&#8239;&#177;&#8239;35&#46;22&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Total triglycerides&#44; mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1687&#46;50&#8239;&#177;&#8239;905&#46;22&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">106&#46;19&#8239;&#177;&#8239;57&#46;52&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Apo B&#44; mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">124&#46;31&#8239;&#177;&#8239;35&#46;14&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">80&#46;25&#8239;&#177;&#8239;17&#46;99&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Lp&#40;a&#41;&#44; mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10&#46;00 &#40;41&#46;50&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">14&#46;50 &#40;34&#46;75&#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="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Glucose&#44; mg&#47;dl&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">99&#46;12&#8239;&#177;&#8239;10&#46;79&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">97&#46;48&#8239;&#177;&#8239;7&#46;93&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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        "identificador" => "tbl0010"
        "etiqueta" => "Table 2"
        "tipo" => "MULTIMEDIATABLA"
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          "leyenda" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">C&#58; normolipaemic control subjects&#59; CHR&#58; chromosome that contains the CG &#40;Build 38&#41;&#59; HT&#58; hypertriglyceridaemic patients&#59; ID&#58; unique identifier from the Illumina&#174; GC database&#59; MAPINFO&#58; coordinates of the CG &#40;Build 38&#41;&#59; Strand&#58; Forward &#40;F&#41; or Reverse &#40;R&#41; chain&#46;</p>"
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              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">ID&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Effect&#95;Size&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Group&#46;HT&#95;AVG&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Group&#46;C&#95;AVG&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">CHR&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">MAPINFO&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Strand&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Gene&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Feature&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">cgi&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">cg21560722&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">20&#46;65&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60&#46;76 &#40;12&#46;42&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">40&#46;27 &#40;17&#46;63&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">7&#46;07E-05&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">&#46;81&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">11&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10293815&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">F&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">SBF2</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Body&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
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          "leyenda" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">C&#58; Normolipaemic control subjects&#59; CHR&#58; Chromosome that contains the CG &#40;Build 38&#41;&#59; HT&#58; Hypertriglyceridaemic patients&#59; ID&#58; Unique identifier from the Illumina&#174; GC database&#59; MAPINFO&#58; Coordinates of the CG &#40;Build 38&#41;&#59; Strand&#58; Forward &#40;F&#41; or Reverse &#40;R&#41; chain&#46;</p>"
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