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"documento" => "article" "crossmark" => 1 "subdocumento" => "sco" "cita" => "Med Clin. 2022;158:547-9" "abierto" => array:3 [ "ES" => false "ES2" => false "LATM" => false ] "gratuito" => false "lecturas" => array:1 [ "total" => 0 ] "en" => array:10 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Editorial article</span>" "titulo" => "Approach to lysosomal diseases" "tienePdf" => "en" "tieneTextoCompleto" => "en" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "547" "paginaFinal" => "549" ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Abordaje de las enfermedades lisosomales" ] ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Miguel Ángel Torralba Cabeza, Sofía Aznárez Nogueras" "autores" => array:2 [ 0 => array:2 [ "nombre" => "Miguel Ángel" "apellidos" => "Torralba Cabeza" ] 1 => array:2 [ "nombre" => "Sofía" "apellidos" => "Aznárez Nogueras" ] ] ] ] ] "idiomaDefecto" => "en" "Traduccion" => array:1 [ "es" => array:9 [ "pii" => "S0025775322000598" "doi" => "10.1016/j.medcli.2022.02.001" "estado" => "S300" "subdocumento" => "" "abierto" => array:3 [ "ES" => false "ES2" => false "LATM" => false ] "gratuito" => false "lecturas" => array:1 [ "total" => 0 ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0025775322000598?idApp=UINPBA00004N" ] ] "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S238702062200225X?idApp=UINPBA00004N" "url" => "/23870206/0000015800000011/v1_202206190623/S238702062200225X/v1_202206190623/en/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">Review</span>" "titulo" => "Bariatric surgery and non-alcoholic fatty liver disease" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "550" "paginaFinal" => "555" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Helena Julià, David Benaiges, Juan Pedro-Botet" "autores" => array:3 [ 0 => array:3 [ "nombre" => "Helena" "apellidos" => "Julià" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 1 => array:4 [ "nombre" => "David" "apellidos" => "Benaiges" "email" => array:1 [ 0 => "96002@parcdesalutmar.cat" ] "referencia" => array:5 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] 3 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] 4 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 2 => array:3 [ "nombre" => "Juan" "apellidos" => "Pedro-Botet" "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] ] ] ] "afiliaciones" => array:4 [ 0 => array:3 [ "entidad" => "Endocrinology Department, Hospital Universitari del Mar, 08003 Barcelona, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Department of Medicine, Universitat Autònoma de Barcelona, 08139 Barcelona, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "IMIM (Hospital del Mar Medical Research Institute), 08003 Barcelona, Spain" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Consorci Sanitari de l’Alt Penedès i Garraf, 08720 Vilafranca del Penedès, Spain" "etiqueta" => "d" "identificador" => "aff0020" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Cirugía bariátrica e hígado graso no alcohólico" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1529 "Ancho" => 2515 "Tamanyo" => 192375 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Non-alcoholic fatty liver disease physiopathology and mechanisms through which bariatric surgery improves non-alcoholic fatty liver disease. The mechanisms through which bariatric surgery improves NAFLD are also represented (see green lines). FFA: free fatty acids; NAFLD: non-alcoholic fatty liver disease; NASH: non-alcoholic steatohepatitis; GLP-1: glucagon-like peptid-1; FGF19: fibroblast growth factor 19.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Obesity is a chronic disease with increasing prevalence worldwide and frequently associated to metabolic syndrome. Conditions such as type 2 diabetes (T2D), dyslipidemia, hypertension, vascular disease, obstructive sleep apnea and several malignancies are largely responsible for the higher mortality in this population group.</p><p id="par0010" class="elsevierStylePara elsevierViewall">Non-alcoholic fatty liver disease (NAFLD) is regarded as the hepatic manifestation of metabolic syndrome and is strongly linked to abdominal obesity with increased waist circumference,<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">1</span></a> insulin-resistance, dysfunctional lipid metabolism and chronic inflammation. It represents a heterogeneous spectrum of liver alterations, ranging from simple steatosis and non-alcoholic steatohepatitis (NASH) to cirrhosis and hepatocellular carcinoma. The emergence of new pharmacologic therapies for hepatitis B and C viruses has drastically reduced the rate of chronic viral hepatitis and progression to related cirrhosis and hepatocarcinoma.<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">2</span></a> This is a key reason why NASH is currently the second cause of liver transplantation in the United States. Taking into account that obesity prevalence is dramatically rising together with its strong etiopathogenic relationship, NAFLD is expected to continue growing, and be the most common cause of chronic liver disease and cirrhosis in coming decades.<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">3</span></a> In this respect, in Spain, it has been estimated that obesity in men [body mass index (BMI) 30–39.9<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span>] will increase from the 22.1% in 2016 to 28.7% in 2030 and morbid obesity (BMI<span class="elsevierStyleHsp" style=""></span>><span class="elsevierStyleHsp" style=""></span>40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span>) from 0.87 to 1.34%.<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">4</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">In this worrying scenario, it is crucial to establish effective therapeutic approaches to NAFLD. In this respect, significant weight loss achieved by lifestyle interventions and control of underlying factors of the metabolic syndrome represents the first-line therapeutic strategy for most patients with NAFLD. However, lifestyle modifications have a limited impact and fail to achieve and particularly to maintain a significant percentage of weight loss at mid and long term.<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">5</span></a> Another possible approach involves the use of medications, although their effectiveness seems to be limited.<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">6</span></a> Hopefully, bariatric surgery has demonstrated to be effective for long-term sustained weight loss and has widely proven its beneficial effect on reversing obesity-related comorbidities that contribute to the pathogenesis of NAFLD in patients with obesity.<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">7</span></a> Therefore, this review aims to evaluate bariatric surgery as a potential treatment for NAFLD.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Non-alcoholic fatty liver disease and obesity</span><p id="par0020" class="elsevierStylePara elsevierViewall">NAFLD is a spectrum of liver diseases characterized by the presence of ≥5% of liver fat accumulation (hepatic steatosis) in the absence of any secondary causes and is an exclusion diagnosis. NAFLD includes different severity stages. Initially, lipids accumulate in hepatocytes resulting in simple steatosis. Then, if simple steatosis is matched with inflammatory changes with or without fibrosis, the disease progresses to NASH. Finally, when fibrosis grows, the end-stage of the disease includes cirrhosis and even hepatocellular carcinoma.<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">1</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">A close relationship exists between obesity and NAFLD. From an epidemiologic point of view, 90% of the morbidly obese population is affected by NAFLD, a rate clearly higher than the 6–45% observed in the general population.<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">8</span></a> In this respect, Li et al.,<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">9</span></a> in a meta-analysis including more than 380,000 subjects, found obesity to be independently associated with a 3.5-fold increased risk of NAFLD compared with normal weight subjects, together with a gradual association between BMI and NAFLD risk (relative risk: 1.2; 95% CI: 1.1–1.3 per 1-unit increment in BMI).</p><p id="par0030" class="elsevierStylePara elsevierViewall">From a pathogenic point of view, NAFLD is considered the hepatic manifestation of the metabolic syndrome. For this reason, a group of experts recently suggested a change in nomenclature for these conditions that could better reflect the pathogenesis and heterogeneity of patients: metabolic (dysfunction)-associated fatty liver disease “MAFLD” has been proposed.<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">10</span></a> In this respect, abdominal adiposity and hormones related to insulin resistance trigger the release of free fatty acids (FFA) and promote the accumulation of triglycerides in different tissues including the liver.<a class="elsevierStyleCrossRefs" href="#bib0355"><span class="elsevierStyleSup">11,12</span></a> Furthermore, adipocytes are responsible for increased pro-inflammatory cytokines and deregulated adipokine secretion which also contribute to increased lipid storage in the liver and generate a lipotoxic environment leading to hepatocyte death and liver inflammation, thereby promoting fibrogenesis.<a class="elsevierStyleCrossRef" href="#bib0365"><span class="elsevierStyleSup">13</span></a> These metabolic alterations are strongly related to other metabolic syndrome traits: hyperglycemia and insulin resistance, high blood pressure, hypertriglyceridemia and low high-density lipoprotein cholesterol (HDLc) concentrations<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">14</span></a> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Non-alcoholic fatty liver disease and bariatric surgery outcomes</span><p id="par0035" class="elsevierStylePara elsevierViewall">Liver biopsy is the gold standard for diagnosing and staging NAFLD. In this respect, a number of meta-analyses including studies with liver biopsy-proven resolution of NAFLD identified the benefits of bariatric surgery on NAFLD. In 2008, a meta-analysis<a class="elsevierStyleCrossRef" href="#bib0375"><span class="elsevierStyleSup">15</span></a> found improvement or resolution in steatosis in 91.6% of patients, steatohepatitis in 81.3% and fibrosis in 65.5% following weight loss after bariatric surgery. In that study, patients with cirrhosis were excluded and the impact of bariatric surgery was evaluated only in less advanced stages of fibrosis. A Cochrane review in 2010<a class="elsevierStyleCrossRef" href="#bib0380"><span class="elsevierStyleSup">16</span></a> reported beneficial effects on steatosis, inflammation and fibrosis. Bower et al. in 2015<a class="elsevierStyleCrossRef" href="#bib0385"><span class="elsevierStyleSup">17</span></a> concluded that bariatric surgery improved steatosis in 50.2% of patients, fibrosis in 11.9%, hepatocyte ballooning in 67.7% and lobular inflammation in 50.7%. A more recent meta-analysis<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">18</span></a> with 2374 patients confirmed that steatosis and steatohepatitis improved or resolved in the majority of patients after bariatric surgery, 88% and 59%, respectively, and stated that liver fibrosis improved or resolved in 30% of patients. In that study, malabsorptive procedures, such as the biliopancreatic diversion and duodenal switch, were excluded. Unlike pre-existing studies, Lee et al.,<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">19</span></a> sought to demonstrate complete resolution rather than improvement. Steatosis, inflammation, ballooning degeneration and fibrosis resolved in 66%, 50%, 76% and 40% of patients, respectively.</p><p id="par0040" class="elsevierStylePara elsevierViewall">Nevertheless, these systematic reviews and meta-analyses had several limitations including significant variability in patient selection, follow-up time, reason for biopsy, type of biopsy, interpretation of histology and type of procedure performed that may lead to reporting biases. The heterogeneity of the studies also represented a significant interpretive limitation.</p><p id="par0045" class="elsevierStylePara elsevierViewall">The long-term effect of bariatric surgery in NAFLD patients has scarcely been examined. Two studies<a class="elsevierStyleCrossRefs" href="#bib0400"><span class="elsevierStyleSup">20,21</span></a> demonstrated a mid-term amelioration in all NAFLD histologic parameters after Roux-en-Y gastric bypass (RYGB) at 5 years in one of them and at a median follow-up of 55 months in the other.</p><p id="par0050" class="elsevierStylePara elsevierViewall">Regarding the risk of fibrosis worsening after bariatric surgery, Mathurin et al.,<a class="elsevierStyleCrossRef" href="#bib0410"><span class="elsevierStyleSup">22</span></a> showed fibrosis stage worsened in 19.8% of patients at 5 years post-surgery although the fibrosis score remained maximal 1, suggesting a slight disease progression postoperatively, but with limited clinical effect. Moreover, the surgical techniques employed in the study included bilio-intestinal bypass and gastric band, which have now fallen into disuse. A 2019 meta-analysis<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">19</span></a> reported new or worsened NAFLD in 12% of patients after bariatric surgery; however, a subgroup analyses for RYGB showed greater reduction of liver side effects. Although the evidence so far supports bariatric surgery for treatment of NAFLD, randomized clinical trials are required and should shed light on whether the proportion of patients with disease progression is lower after bariatric surgery compared to medical therapy. A prospective randomized clinical trial is being carried out by Philippe Mathurin and will be completed in 2023 (NASHSURG, ClinicalTrials.gov Identifier NCT03472157). It includes patients with NASH-related advanced fibrosis and BMI 30–35<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span>, and aims to demonstrate the superiority of bariatric surgery (RYGB or sleeve gastrectomy [SG]) in the disappearance of NASH without worsening of fibrosis compared to lifestyle therapy in these patients at 5 years.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Non-alcoholic fatty liver disease diagnosis and monitoring in bariatric surgery patients</span><p id="par0055" class="elsevierStylePara elsevierViewall">Given the close relationship between NAFLD and obesity and its potential progression to fibrosis, cirrhosis and even hepatocarcinoma, it is reasonable to assume that NAFLD should be assessed and monitored in patients undergoing bariatric surgery. Although traditionally liver biopsy has been the gold standard method for diagnosing NAFLD, it is an invasive technique that requires a multidisciplinary team, is prone to complications and too expensive to be conducted recurrently on large segments of the population. Moreover, in severely obese patients, it is particularly problematic since it may be difficult to obtain sufficient material with a standard percutaneous approach owing to a large subcutaneous fat layer. Therefore, the impracticality of performing a routine pre- and post-bariatric liver biopsy has prompted the development of non-invasive scores and radiologic methods.</p><p id="par0060" class="elsevierStylePara elsevierViewall">Alanine aminotransferase (ALT) and gamma-glutamyl transpeptidase (GGT) levels are associated with hepatocyte injury and inflammation.<a class="elsevierStyleCrossRef" href="#bib0385"><span class="elsevierStyleSup">17</span></a> Nevertheless, liver enzymes level's ability as diagnostic tool is limited since 11–30% of patients with biopsy-proven NASH might present normal ALT levels.<a class="elsevierStyleCrossRef" href="#bib0415"><span class="elsevierStyleSup">23</span></a> Furthermore, when fibrosis progresses, the decrease in inflammation is matched with falling liver enzyme levels.<a class="elsevierStyleCrossRef" href="#bib0420"><span class="elsevierStyleSup">24</span></a> However, bariatric surgery has proved to lower transaminase levels even if they are in normal range.<a class="elsevierStyleCrossRef" href="#bib0425"><span class="elsevierStyleSup">25</span></a> The Fakhry et al.,<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">18</span></a> meta-analysis showed that aspartate aminotransferase (AST) improved in 32% of patients, ALT in 62%, alkaline phosphatase (ALP) in 45% and GGT in 96% of patients after bariatric surgery. Similar results were found in the Swedish Obese Subjects study with sustained reduction in AST and ALT levels at 2 and 10 years after bariatric surgery.<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">7</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">Non-invasive fibrosis scores are calculated using routine clinical parameters and inexpensive biochemical measurements. However, the fatty liver index (FLI), which works well in the general population for assessing the presence of steatosis, has shown to poorly predict significant steatosis and has limited utility for steatosis quantification compared to liver histology in obese patients.<a class="elsevierStyleCrossRef" href="#bib0430"><span class="elsevierStyleSup">26</span></a> Many studies showed NAFLD fibrosis score (NFS) and fibrosis-4 score (FIB-4) to be useful for identifying obese patients with NAFLD at higher risk of advanced hepatic fibrosis.<a class="elsevierStyleCrossRef" href="#bib0435"><span class="elsevierStyleSup">27</span></a> However, other studies advocated a lower threshold in FIB-4 and reported a poor performance of NFS in predicting significant fibrosis in morbidly-obese patients.<a class="elsevierStyleCrossRef" href="#bib0440"><span class="elsevierStyleSup">28</span></a> Although reductions in the NFS after bariatric surgery were confirmed in several studies<a class="elsevierStyleCrossRefs" href="#bib0425"><span class="elsevierStyleSup">25,29</span></a> and one study reported higher levels in patients who regained weight after the initial weight loss,<a class="elsevierStyleCrossRef" href="#bib0450"><span class="elsevierStyleSup">30</span></a> none of those studies included post-surgery biopsies as a gold standard for therapeutic effects. In fact, anthropometric parameters used by these scores predictably improved with weight loss after bariatric surgery; therefore, it was unknown whether the liver benefit reported was real.</p><p id="par0070" class="elsevierStylePara elsevierViewall">As for imaging tools, liver ultrasound is widely available in clinical practice and is usually the first-line examination to identify liver steatosis in patients with suspected NAFLD. However, it has low sensitivity in morbidly-obese patients and steatosis might be missed if liver fat content is <20%.<a class="elsevierStyleCrossRef" href="#bib0455"><span class="elsevierStyleSup">31</span></a> Computed tomography has similar sensitivity and, combined with radiation exposure, makes it less suitable for screening. Moreover, clinical guidelines on surgery for obesity endorsed the by the American Society for Nutrition (ASN), American Society for Parenteral and Enteral Nutrition (ASPEN), International Federation for the Surgery of Obesity and Metabolic Disorders (IFSO), International Society for the Perioperative Care of the Obese Patient (ISPCOP), and Obesity Action Coalition (OAC) do not recommend imaging tools as a routine screen for NAFLD because they may identify NAFLD but may not be diagnostic.<a class="elsevierStyleCrossRef" href="#bib0460"><span class="elsevierStyleSup">32</span></a></p><p id="par0075" class="elsevierStylePara elsevierViewall">Various non-invasive diagnostic methods have been based on the assessment of liver stiffness measurement (LSM) calculating the speed of shear wave that is generated by a push pulse as it passes through the liver tissue, which is a surrogate biomarker of liver fibrosis stage. Ultrasonography-based transient elastography (TE) is a promising tool fully implemented in clinical practice that assesses liver steatosis using the continuous attenuation parameter (CAP) along with LSM. CAP measures the attenuation of the ultrasound beam which changes depending on the viscosity of the medium through which the wave travels. It is equipped with two types of probe for adults: an M probe for use in most patients and an XL probe for obese patients with comparable diagnostic accuracy between them. Although the American clinical guidelines on surgery of obesity do also not recommend TE as a routine method for NAFLD diagnosis,<a class="elsevierStyleCrossRef" href="#bib0460"><span class="elsevierStyleSup">32</span></a> studies have proven comparable measurements of TE with liver biopsy in obese patients. One study evaluated patients preoperatively and at one year post-bariatric surgery using paired liver biopsy and TE with significant improvements in both histologic and CAP and LSM cut-off values.<a class="elsevierStyleCrossRef" href="#bib0465"><span class="elsevierStyleSup">33</span></a> These studies point towards using TE as a non-invasive technique for screening and monitoring for NAFLD in patients undergoing bariatric surgery. However, further research with more robust studies is needed to state TE across the field of bariatrics. Magnetic resonance imaging is the most sensitive modality for diagnosing liver steatosis, and magnetic resonance with elastography (MRI-E) also recognizes different degrees of fibrosis but is expensive and with limited availability. A prospective study of 38 obese patients undergoing bariatric surgery demonstrated significant NASH improvement with a good correlation between MRI-E paired with liver biopsy at 12 months post-surgery.<a class="elsevierStyleCrossRef" href="#bib0470"><span class="elsevierStyleSup">34</span></a></p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Bariatric surgery indication in non-alcoholic fatty liver disease</span><p id="par0080" class="elsevierStylePara elsevierViewall">A significant weight loss is mandatory to improve liver function and observe consistent changes in NAFLD. In particular, a 5% weight loss can improve liver steatosis, while 7% and 10% weight loss are necessary to lesser liver inflammation and fibrosis, respectively.<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">6</span></a> Nevertheless, weight loss achieved by lifestyle modifications including dietary changes such as reduction of carbohydrate and saturated fats intake, alcohol withdrawal and physical activity is often insufficient and hard to maintain at long-term. The effectiveness of pharmacotherapy for weight loss is also limited and no specific drugs for NAFLD have been approved thus pharmacologic treatment focuses on coexisting diseases strongly linked to NAFLD such as metformin, pioglitazone, glucagon-like peptide (GLP-1) analogue, statins and vitamins with antioxidant properties.</p><p id="par0085" class="elsevierStylePara elsevierViewall">In light of the foregoing, bariatric surgery has proven not only long-term weight loss in adults with obesity but also significant improvement or even complete resolution of comorbidities associated with obesity and NAFLD. Sustained (>5 years) weight loss of 20% or more on average is reported along with 60–80% resolution or improvement of comorbid conditions.<a class="elsevierStyleCrossRefs" href="#bib0335"><span class="elsevierStyleSup">7,35</span></a> However, it is noteworthy that bariatric surgery is frequently considered the last resort in the treatment of obesity and related health conditions. Therefore, the indication for bariatric surgery in patients with NAFLD and obesity should extensively be addressed.</p><p id="par0090" class="elsevierStylePara elsevierViewall">The criteria for surgical intervention were established by a NIH consensus panel in 1991 indicating that bariatric surgery is appropriate for all patients with BMI<span class="elsevierStyleHsp" style=""></span>>40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span> and for patients with BMI 35–40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span> with associated obesity-related comorbidities<a class="elsevierStyleCrossRef" href="#bib0480"><span class="elsevierStyleSup">36</span></a> defined as conditions caused at least in part by weight excess and that are expected to improve or go into remission with effective and sustained weight loss. The indications for bariatric surgery are evolving rapidly to consider the presence or absence of comorbid conditions as well as the severity of the obesity. However, the American Association for the Study of Liver Disease (AASLD) and American Gastroenterology Association (AGA) state that it is premature to establish bariatric surgery as a treatment option for NAFLD/NASH.<a class="elsevierStyleCrossRef" href="#bib0455"><span class="elsevierStyleSup">31</span></a> These scientific societies only consider bariatric surgery in patients with NAFLD and BMI between 35 and 40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span> if they also present another obesity related comorbidity such as T2D, dyslipidemia or hypertension. However, this approach leaves out of bariatric surgery indication those metabolically healthy patients with grade 2 obesity (BMI 35–40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span>). It is important to point out that metabolically healthy obese subjects are usually younger because obesity related comorbidities are expected to progress over time. Moreover, bariatric surgery has proven benefits on NAFLD in metabolically healthy subjects with obesity grade 3 (BMI<span class="elsevierStyleHsp" style=""></span>><span class="elsevierStyleHsp" style=""></span>40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span>) undergoing bariatric surgery and this improvement remains at 5 years.<a class="elsevierStyleCrossRef" href="#bib0425"><span class="elsevierStyleSup">25</span></a> Fortunately, American Guidelines on surgery for obesity published in 2019 and the Spanish Consensus for bariatric surgery published in 2016 consider bariatric surgery in patients with NAFLD and a BMI of 35–40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span> unresponsive to lifestyle changes and pharmacotherapy.<a class="elsevierStyleCrossRefs" href="#bib0460"><span class="elsevierStyleSup">32,37</span></a> For its part, European guidelines on bariatric surgery advocate for bariatric surgery in patients with BMI of 35–40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span> with associated comorbidities that are expected to improve with weight loss but fail to specify what those comorbidities are.<a class="elsevierStyleCrossRef" href="#bib0490"><span class="elsevierStyleSup">38</span></a></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Bariatric surgery and mechanisms underlying non-alcoholic fatty liver disease improvement</span><p id="par0095" class="elsevierStylePara elsevierViewall">Bariatric surgery induces an improvement in NAFLD via multiple mechanisms that are partially unknown, but likely involve weight loss-dependent and independent factors working in parallel or sequentially. Effects on glucose and lipid metabolic pathways, changes in gut hormones, gastrointestinal motility, bile acids, gut microbiota as well as incomplete nutrient ingestion and absorption have been described.<a class="elsevierStyleCrossRef" href="#bib0495"><span class="elsevierStyleSup">39</span></a></p><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Impact of bariatric surgery on weight and non-alcoholic fatty liver disease -related comorbidities</span><p id="par0100" class="elsevierStylePara elsevierViewall">Multiple metabolic disorders are usually present in patients with NAFLD which has led to NAFLD being considered the hepatic manifestation of the metabolic syndrome.<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">12</span></a> There is growing evidence that bariatric surgery stimulates significant changes in three crucial metabolic domains related to NAFLD: improved lipid metabolism, improved insulin tolerance, and a reduction in obesity-related chronic inflammation.<a class="elsevierStyleCrossRef" href="#bib0500"><span class="elsevierStyleSup">40</span></a> Buchwald et al.,<a class="elsevierStyleCrossRef" href="#bib0475"><span class="elsevierStyleSup">35</span></a> performed a meta-analysis reporting complete resolution of T2D in more than 75% of diabetic patients, hyperlipidemia improvement in almost 80% of patients and excessive weight loss >60% after bariatric surgery.</p><p id="par0105" class="elsevierStylePara elsevierViewall">Metabolic abnormalities are not independent pathways; indeed, a close pathogenic correlation exists between lipid deregulation, insulin resistance and obesity. As mentioned above, insulin resistance is the primary hormonal disorder in most NAFLD patients and leads to increased lipolysis and liver uptake of FFA, triggering the replacement of normal liver tissue with liver fat. Moreover, NAFLD patients present excess adipose tissue and, in particular, visceral adipose tissue, which is responsible for increased proinflammatory cytokine and deregulated adipokine secretion that also contributes to increased lipid storage in the liver.<a class="elsevierStyleCrossRef" href="#bib0505"><span class="elsevierStyleSup">41</span></a> Candidate lipotoxic lipids include palmitate, diacylglycerol and ceramide.<a class="elsevierStyleCrossRef" href="#bib0510"><span class="elsevierStyleSup">42</span></a> In this respect, bariatric surgery has proved to reduce total body fat, and to a major extent, visceral fat,<a class="elsevierStyleCrossRef" href="#bib0365"><span class="elsevierStyleSup">13</span></a> to improve lipid profile<a class="elsevierStyleCrossRef" href="#bib0515"><span class="elsevierStyleSup">43</span></a> and lower plasma ceramide levels<a class="elsevierStyleCrossRef" href="#bib0510"><span class="elsevierStyleSup">42</span></a> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Additionally, T2D is the strongest factor in NAFLD progression, with a higher prevalence of fibrosis in diabetic patients compared to non-diabetics.<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">11</span></a> NAFLD patients are also at increased risk for incident diabetes.<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">12</span></a> A review of key results from the Swedish Obese Subjects study reported a 72% remission rate of T2D and a 78% reduction in the risk of developing T2D at 15 years after bariatric surgery compared to usual care.<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">7</span></a></p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Impact of bariatric surgery on other mechanisms</span><p id="par0110" class="elsevierStylePara elsevierViewall">Other mechanisms play a role in NAFLD improvement after bariatric surgery. Firstly, the increase in bile acid secretion and composition<a class="elsevierStyleCrossRef" href="#bib0520"><span class="elsevierStyleSup">44</span></a> favor metabolic improvement through weight loss, higher energy expenditure, lipid metabolism improvement and a rise in glucagon-like peptid-1 (GLP-1) levels, an important regulator of glucose homeostasis. Secondly, bile acid reciprocally modulates the gut microbiome.<a class="elsevierStyleCrossRef" href="#bib0525"><span class="elsevierStyleSup">45</span></a> In this regard, changes in the gut microbiome after bariatric surgery are involved in both weight loss and improved metabolic effects.<a class="elsevierStyleCrossRef" href="#bib0530"><span class="elsevierStyleSup">46</span></a> Thirdly, increased gut hormone secretion, especially PYY, GLP-1 and adiponectin, contributes to appetite and glycemic control after bariatric surgery.<a class="elsevierStyleCrossRef" href="#bib0535"><span class="elsevierStyleSup">47</span></a> In addition, an increase in fibroblast growth factor 19 (FGF19) has been observed after bariatric surgery. FGF19 promotes glycogen synthesis, reduces neoglucogenesis and lowers hepatic triglycerides. Finally, markedly reduced C-reactive protein, tumo necrosis factor and interleukin 6 have been observed, suggesting improved systemic inflammation.<a class="elsevierStyleCrossRef" href="#bib0495"><span class="elsevierStyleSup">39</span></a> However, exactly how all these mechanisms are modified by bariatric surgery remains to be established. Recently, genetic factors were found to contribute to NAFLD pathogenesis; in particular, the I148M PNPLA3 variant has been identified as the most robust genetic variant associated with NAFLD.<a class="elsevierStyleCrossRef" href="#bib0540"><span class="elsevierStyleSup">48</span></a></p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Differences between surgical techniques</span><p id="par0115" class="elsevierStylePara elsevierViewall">Although bariatric surgery has proved to ameliorate NAFLD, questions remain as to which is the best surgical technique. Laparoscopic RYGB and laparoscopic SG are currently the most commonly performed bariatric surgery procedures.<a class="elsevierStyleCrossRef" href="#bib0460"><span class="elsevierStyleSup">32</span></a> SG removes a large portion of the stomach along with the greater curvature, resulting in decreased circulating ghrelin, accelerated gastric emptying, increased secretion of gut hormones and changes in bile acid metabolism and microbiota.<a class="elsevierStyleCrossRef" href="#bib0495"><span class="elsevierStyleSup">39</span></a> RYGB, in contrast, generates a small gastric pouch and bypasses the stomach, duodenum and first part of the jejunum, which adds a malabsorptive effect.</p><p id="par0120" class="elsevierStylePara elsevierViewall">Both techniques have demonstrated their effectiveness in weight loss and improving NAFLD-related comorbidities although differences exist. RYGB and SG improve glycemia by different pathways: while RYGB increases intestinal glucose disposal, SG reduces the alimentary glucose absorption associated with increased density of GLP-1 secreting cells.<a class="elsevierStyleCrossRef" href="#bib0545"><span class="elsevierStyleSup">49</span></a> A meta-analysis showed RYGB to be superior in the management of hypercholesterolemia and hypertension compared to SG, while the same efficacy was observed with both techniques in excess weight loss and T2D resolution<a class="elsevierStyleCrossRefs" href="#bib0550"><span class="elsevierStyleSup">50,51</span></a>; these results were consistent when only randomized clinical trials were analyzed.<a class="elsevierStyleCrossRef" href="#bib0560"><span class="elsevierStyleSup">52</span></a> Such metabolic superiority could be helpful when targeting NASH.</p><p id="par0125" class="elsevierStylePara elsevierViewall">The best surgical technique in terms of NAFLD improvement or resolution is not well defined and the findings of different studies are conflicting. A recent meta-analysis comparing the effects of RYGB and SG on NAFLD found a significant reduction in steatohepatitis after both techniques, but a reduction in fibrosis only after RYGB.<a class="elsevierStyleCrossRef" href="#bib0565"><span class="elsevierStyleSup">53</span></a> Nevertheless, no differences in histopathologic outcomes were found between procedures. Similarly, Froylich et al.,<a class="elsevierStyleCrossRef" href="#bib0570"><span class="elsevierStyleSup">54</span></a> found that fibrosis improved to a greater degree after RYGB. Along the same lines, Nickel et al.,<a class="elsevierStyleCrossRef" href="#bib0575"><span class="elsevierStyleSup">55</span></a> reported superiority of RYGB in reducing liver stiffness and Yeo et al.,<a class="elsevierStyleCrossRef" href="#bib0580"><span class="elsevierStyleSup">56</span></a> found a non-statistically significant greatest improvement in NFS after RYGB compared to SG or gastric band. Conversely, Baldwin et al.<a class="elsevierStyleCrossRef" href="#bib0585"><span class="elsevierStyleSup">57</span></a> found no differences between techniques in alanine transaminase, aspartate transaminase, NAFLD activity score and NAFLD fibrosis score. By contrast, Billeter et al.<a class="elsevierStyleCrossRef" href="#bib0590"><span class="elsevierStyleSup">58</span></a> reported a greater improvement in transaminase levels after SG in 34 obese patients with T2D and NAFLD. However, NAFLD was defined as ALT<span class="elsevierStyleHsp" style=""></span>><span class="elsevierStyleHsp" style=""></span>35<span class="elsevierStyleHsp" style=""></span>U/L and no biopsies were performed. Motamedi et al.,<a class="elsevierStyleCrossRef" href="#bib0595"><span class="elsevierStyleSup">59</span></a> analyzed a bariatric cohort of 1,037 patients and observed lower transaminase levels after SG with no differences between techniques at 2 years.</p><p id="par0130" class="elsevierStylePara elsevierViewall">The only randomized clinical trial conducted to compare the effects of RYGB and SG on liver function found early transient deterioration of liver function only after RYGB.<a class="elsevierStyleCrossRef" href="#bib0600"><span class="elsevierStyleSup">60</span></a> In that study, liver biopsy was performed during surgery and liver function tests were used for follow-up.</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Conclusion</span><p id="par0135" class="elsevierStylePara elsevierViewall">NAFLD is a chronic disease with a rising prevalence that may lead to cirrhosis and its complications. Therefore, an effective therapy is an unmet clinical need. The gold standard diagnostic technique is liver biopsy but involves considerable difficulties and risks. For this reason, TE applies to become a good alternative given the high reliability proved with respect to liver biopsy. NAFLD is strongly linked with obesity and related comorbidities, especially T2D. Currently available studies reported encouraging results of bariatric surgery as a valuable therapy for NAFLD, reversing not only steatosis but also liver fibrosis and other related comorbidities. However, there is lack of consensus among guidelines on the indication of bariatric surgery in patients with NAFLD and BMI between 35 and 40<span class="elsevierStyleHsp" style=""></span>kg/m<span class="elsevierStyleSup">2</span>. Furthermore, coexisting metabolic conditions improved and resolved after surgery. The mechanisms involved in NAFLD improvement after bariatric surgery included weight loss, lipid and glucose profile amelioration, changes in gut hormones, bile acid secretion and the gut microbiome. However, the lack of randomized clinical trials limits the opportunity to establish a clear recommendation in favor of bariatric surgery for the treatment of NAFLD. The best surgical technique remains to be determined and long-term studies are also required to ascertain whether the benefits of surgery remain over time.</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Funding</span><p id="par0140" class="elsevierStylePara elsevierViewall">This research received no external funding.</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Conflicts of interest</span><p id="par0145" class="elsevierStylePara elsevierViewall">The authors declare no conflict of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:16 [ 0 => array:3 [ "identificador" => "xres1736816" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1532223" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1736815" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1532222" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Non-alcoholic fatty liver disease and obesity" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Non-alcoholic fatty liver disease and bariatric surgery outcomes" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Non-alcoholic fatty liver disease diagnosis and monitoring in bariatric surgery patients" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Bariatric surgery indication in non-alcoholic fatty liver disease" ] 9 => array:3 [ "identificador" => "sec0030" "titulo" => "Bariatric surgery and mechanisms underlying non-alcoholic fatty liver disease improvement" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0035" "titulo" => "Impact of bariatric surgery on weight and non-alcoholic fatty liver disease -related comorbidities" ] 1 => array:2 [ "identificador" => "sec0040" "titulo" => "Impact of bariatric surgery on other mechanisms" ] ] ] 10 => array:2 [ "identificador" => "sec0045" "titulo" => "Differences between surgical techniques" ] 11 => array:2 [ "identificador" => "sec0050" "titulo" => "Conclusion" ] 12 => array:2 [ "identificador" => "sec0055" "titulo" => "Funding" ] 13 => array:2 [ "identificador" => "sec0060" "titulo" => "Conflicts of interest" ] 14 => array:2 [ "identificador" => "xack613373" "titulo" => "Acknowledgments" ] 15 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2021-08-28" "fechaAceptado" => "2021-12-07" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1532223" "palabras" => array:6 [ 0 => "Bariatric surgery" 1 => "Morbid obesity" 2 => "Obesity" 3 => "Metabolic syndrome" 4 => "Non-alcoholic fatty liver disease" 5 => "Non-alcoholic steatohepatitis" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1532222" "palabras" => array:6 [ 0 => "Cirugía bariátrica" 1 => "Obesidad mórbida" 2 => "Obesidad" 3 => "Síndrome metabólico" 4 => "Hígado graso no alcohólico" 5 => "Esteatohepatitis no alcohólica" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Non-alcoholic fatty liver disease (NAFLD) is a chronic disease that may lead to cirrhosis and hepatocellular carcinoma; its close relationship with obesity and the metabolic syndrome involves an increasing prevalence. Invasive liver biopsy is the gold standard diagnosis technique for NAFLD but entails risks. Therefore, transient elastography, a non-invasive technique with high reliability, is frequently used in clinical practice. Bariatric surgery is the only effective treatment for long-term weight loss and obesity-related metabolic conditions improvement. Although studies report encouraging results of bariatric surgery as a valuable therapy for NAFLD, guidelines for its use in NAFLD are ambiguous. Indeed, the mechanisms driving this improvement are largely unknown, but likely involve weight loss-dependent and independent factors including anatomic and hormonal changes. This review aims to update the relationship between NAFLD and bariatric surgery, focusing on the indications for surgery and the mechanisms implied in NAFLD improvement.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">El hígado graso no alcohólico (HGNA) es una enfermedad crónica que puede conducir a cirrosis y hepatocarcinoma; su relación con la obesidad y el síndrome metabólico supone un aumento en su prevalencia. La biopsia hepática es la prueba diagnóstica de elección, pero implica riesgos. En consecuencia, la elastografía hepática, una técnica no invasiva con una alta fiabilidad, es utilizada frecuentemente en la práctica clínica. La cirugía bariátrica es el único tratamiento eficaz para la pérdida de peso y la mejoría de las comorbilidades a largo plazo. Aunque los estudios demuestran que la cirugía bariátrica es efectiva para el tratamiento del HGNA, la mayoría de los mecanismos implicados en esta mejoría se desconocen. De hecho, las guías clínicas son ambiguas en cuanto a su indicación. Esta revisión tiene como objetivo actualizar la relación entre el HGNA y la cirugía bariátrica, centrándose en las indicaciones de la cirugía y los mecanismos implicados en la mejoría del HGNA.</p></span>" ] ] "multimedia" => array:1 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1529 "Ancho" => 2515 "Tamanyo" => 192375 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Non-alcoholic fatty liver disease physiopathology and mechanisms through which bariatric surgery improves non-alcoholic fatty liver disease. The mechanisms through which bariatric surgery improves NAFLD are also represented (see green lines). FFA: free fatty acids; NAFLD: non-alcoholic fatty liver disease; NASH: non-alcoholic steatohepatitis; GLP-1: glucagon-like peptid-1; FGF19: fibroblast growth factor 19.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:60 [ 0 => array:3 [ "identificador" => "bib0305" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Clinical epidemiology and disease burden of nonalcoholic fatty liver disease" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:6 [ 0 => "B.J. Perumpail" 1 => "M.A. Khan" 2 => "E.R. Yoo" 3 => "G. Cholankeril" 4 => "D. Kim" 5 => "A. 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Bariatric surgery and non-alcoholic fatty liver disease
Cirugía bariátrica e hígado graso no alcohólico
a Endocrinology Department, Hospital Universitari del Mar, 08003 Barcelona, Spain
b Department of Medicine, Universitat Autònoma de Barcelona, 08139 Barcelona, Spain
c IMIM (Hospital del Mar Medical Research Institute), 08003 Barcelona, Spain
d Consorci Sanitari de l’Alt Penedès i Garraf, 08720 Vilafranca del Penedès, Spain