Microbiota and nonalcoholic fatty liver disease/nonalcoholic steatohepatitis (NAFLD/NASH)

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"documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Ann Hepatol. 2019;18:422-8" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 538 "formatos" => array:3 [ "EPUB" => 33 "HTML" => 314 "PDF" => 191 ] ] "en" => array:12 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "The basis of liver regeneration: A systems biology approach" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => "en" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "422" "paginaFinal" => "428" ] ] "contieneResumen" => array:1 [ "en" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 3563 "Ancho" => 2833 "Tamanyo" => 644170 ] ] "descripcion" => array:1 [ "en" => "(A) Flow chart detailing the steps in our study, from data curation to final generation of networks based on protein-protein interactions. (B) Venn Diagram illustrating the distinct and overlapping dysregulated genes between human and mouse datasets. There were 75 dysregulated genes in humans, 502 dysregulated genes in mice, and 22 shared genes between human and mice (list of genes reported in Supplementary file 1). (C) Network analysis demonstrates the genes common to human and mouse early liver regeneration in the center, with the red triangles depicting up-modulated genes, and the green triangles depicting the down-modulated genes." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Mamatha Bhat, Elisa Pasini, Cristina Baciu, Marc Angeli, Atul Humar, Sonya Macparland, Jordan Feld, Ian McGilvray" "autores" => array:8 [ 0 => array:2 [ "nombre" => "Mamatha" "apellidos" => "Bhat" ] 1 => array:2 [ "nombre" => "Elisa" "apellidos" => "Pasini" ] 2 => array:2 [ "nombre" => "Cristina" "apellidos" => "Baciu" ] 3 => array:2 [ "nombre" => "Marc" "apellidos" => "Angeli" ] 4 => array:2 [ "nombre" => "Atul" "apellidos" => "Humar" ] 5 => array:2 [ "nombre" => "Sonya" "apellidos" => "Macparland" ] 6 => array:2 [ "nombre" => "Jordan" "apellidos" => "Feld" ] 7 => array:2 [ "nombre" => "Ian" "apellidos" => "McGilvray" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1665268119300468?idApp=UINPBA00004N" "url" => "/16652681/0000001800000003/v2_201906020907/S1665268119300468/v2_201906020907/en/main.assets" ] "itemAnterior" => array:19 [ "pii" => "S1665268119300390" "issn" => "16652681" "doi" => "10.1016/j.aohep.2019.04.004" "estado" => "S300" "fechaPublicacion" => "2019-05-01" "aid" => "31" "copyright" => "Fundación Clínica Médica Sur, A.C." "documento" => "simple-article" "crossmark" => 0 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "sco" "cita" => "Ann Hepatol. 2019;18:410-5" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 779 "formatos" => array:3 [ "EPUB" => 22 "HTML" => 456 "PDF" => 301 ] ] "en" => array:11 [ "idiomaDefecto" => true "cabecera" => "Viewpoints" "titulo" => "Antioxidants benefits in hepatitis C infection in the new DAAs era" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => "en" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "410" "paginaFinal" => "415" ] ] "contieneResumen" => array:1 [ "en" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Sonia A. Lozano-Sepúlveda, Ana R. Rincón-Sanchez, Ana M. Rivas-Estilla" "autores" => array:3 [ 0 => array:2 [ "nombre" => "Sonia A." "apellidos" => "Lozano-Sepúlveda" ] 1 => array:2 [ "nombre" => "Ana R." "apellidos" => "Rincón-Sanchez" ] 2 => array:2 [ "nombre" => "Ana M." "apellidos" => "Rivas-Estilla" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1665268119300390?idApp=UINPBA00004N" "url" => "/16652681/0000001800000003/v2_201906020907/S1665268119300390/v2_201906020907/en/main.assets" ] "en" => array:18 [ "idiomaDefecto" => true "cabecera" => "Concise review" "titulo" => "Microbiota and nonalcoholic fatty liver disease/nonalcoholic steatohepatitis (NAFLD/NASH)" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "416" "paginaFinal" => "421" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Sebastião M.B. Duarte, Jose Tadeu Stefano, Claudia P. Oliveira" "autores" => array:3 [ 0 => array:3 [ "nombre" => "Sebastião M.B." "apellidos" => "Duarte" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 1 => array:3 [ "nombre" => "Jose Tadeu" "apellidos" => "Stefano" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 2 => array:4 [ "nombre" => "Claudia P." "apellidos" => "Oliveira" "email" => array:1 [ 0 => "cpm@usp.br" ] "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Laboratório de Gastroenterologia Clínica e Experimental (LIM-07) do Departamento de Gastroenterologia e Hepatologia do Hospital das Clínicas HCFMUSP da Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brazil" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brazil" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author at: Laboratório de Gastroenterologia Clínica e Experimental (LIM-07) do Departamento de Gastroenterologia e Hepatologia do Hospital das Clínicas HCFMUSP da Faculdade de Medicina da Universidade de São Paulo, Av. Dr. Enéas, 455, 3° andar, sala 3115, CEP 01246903, São Paulo, SP, Brazil." ] ] ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2535 "Ancho" => 3000 "Tamanyo" => 420405 ] ] "descripcion" => array:1 [ "en" => "The role of the intestinal microbiota in the development of fatty liver. Intestinal dysbiosis may be a determining factor for the development and progression of NAFLD/NASH. The increase in pathogenic bacteria and Gram-negative bacteria increases dietary energy extraction, leading to increased intestinal permeability and bacterial translocation, stimulating de novo fatty acid synthesis and increasing LPS expression, as well as the expression of NF-kβ and TNF-α. LPS, lipopolysaccharides; NF-kβ, nuclear factor-kappa β; TNF-α, tumor necrosis factor-alpha." ] ] ] "textoCompleto" => "1Human intestinal microbiotaThe human intestinal epithelium has an absorptive surface comparable to 300–400m2, with approximately 1014 resident bacterial species. Bacterial colonization occurs before birth and continues for life. Most of the bacteria that colonize the intestine are of the anaerobic type and comprise approximately 36,000 different species <a class="elsevierStyleCrossRefs" href="#bib0410">[1,2]</a>, constituting a variety of species of microorganisms that, quantitatively and qualitatively, differ between individuals <a class="elsevierStyleCrossRef" href="#bib0420">[3]</a>.The main functions of the intestinal microbiota (IM) include metabolic and immunological activities. The prominent metabolic function of the IM is the fermentation of nondigestible components of the diet. The products of this complex metabolic activity are a spectrum of organic acids, which are an important source of energy for the host. The epithelial cells of the gut participate in immunological processes. The signaling pathways of these cells are highly regulated to avert uncontrolled inflammatory responses <a class="elsevierStyleCrossRef" href="#bib0425">[4]</a>. The gut epithelium is a major barrier between the host and the environment. This barrier is formed by tight junctions that act as a highly regulated entry that open and close depending on signals, such as those from cytokines and bacterial components from the lumen, and excessive contact with bacteria may cause an increase in the proinflammatory immune response <a class="elsevierStyleCrossRef" href="#bib0430">[5]</a>. Therefore, the IM supports immune regulation and ensures that effector immune responses are activated in response to invading pathogens <a class="elsevierStyleCrossRef" href="#bib0435">[6]</a>. Another important function of the IM is protection against exogenous microorganisms. These bacteria can inhibit the growth of pathogenic microorganisms through the synthesis of antimicrobial substances or by competing for nutrients and reducing the attachment and penetration of the enteroinvasive pathogen into epithelial cells <a class="elsevierStyleCrossRef" href="#bib0440">[7]</a>.The IM has a heterogeneous distribution, with the colon being the place with the greatest density due to the favorable conditions for the proliferation of microorganisms, characterized by slow peristalsis, absence of intestinal secretions and presence of a nutritional supply <a class="elsevierStyleCrossRef" href="#bib0445">[8]</a>. Dysbiosis generates bacterial overgrowth, toxin production and increased intestinal permeability, resulting in changes in immunological and hormonal effects. Thus, lifestyle habits such as diet, stress and the use of antibiotics, for example, cause the transient microbiota to prevail over the resident microbiota, predisposing the host to gastrointestinal disorders. The actions that the IM exerts on the various systems of the organism also reflect the maintenance of the metabolism <a class="elsevierStyleCrossRef" href="#bib0450">[9]</a>.Approximately 98% of all bacterial species that make up the IM belong to the following phyla: Firmicutes (64%) and Bacteroidetes (23%), which represent most of the IM in addition to Proteobacteria (8%) and Actinobacteria (3%) <a class="elsevierStyleCrossRef" href="#bib0455">[10]</a>. The Firmicutes phylum contains more than 250 genera, including Lactobacillus<a class="elsevierStyleCrossRef" href="#bib0460">[11]</a>. The phylum Bacteroidetes, similar to Firmicutes, is found in the small and large intestines, especially in the colon, and encompasses several genera, such as Bacteroides, Flavobacteria and Sphingobacteriales, with Bacteroides thetaiotaomicron being one of the most abundant <a class="elsevierStyleCrossRef" href="#bib0465">[12]</a>.Although the functions of the bacteria belonging to the Firmicutes phylum have not yet been fully elucidated, evidence suggests that some members of this phylum, such as Clostridium butyricum bacteria, are among the bacteria producing butyric acid from lactic acid or lactose in a chemical reaction known as butyric fermentation, and this type of fermentation increases the energy extracted from the diet <a class="elsevierStyleCrossRef" href="#bib0470">[13]</a>. On the other hand, members of the Bacteroidetes phylum participate in the metabolism of carbohydrates and perform this metabolism by expressing enzymes similar to the glycosyltransferases, which promote glycosylation, that is, to join carbohydrates to the proteins formed in the ribosomes. Members of the Bacteroidetes phylum also express glycoside hydrolases that degrade biomass, such as cellulose and hemicellulose, in antibacterial defense strategies. Finally, they also express the polysaccharide-lyase enzyme that catalyzes the breakdown of a carbon–oxygen bond in polysaccharides, leading to an unsaturated product and the elimination of alcohol <a class="elsevierStyleCrossRef" href="#bib0475">[14]</a>.2Intestinal microbiota and obesityIntestinal microorganisms influence energy production, energy homeostasis and, potentially, the development of obesity and metabolic disorders <a class="elsevierStyleCrossRef" href="#bib0460">[11]</a>. Increasing evidence supports the importance of the composition of the IM for the development of obesity and demonstrates that the type and quantity of the bacterial population can determine some important characteristics of metabolic pathways that play an important role in obesity <a class="elsevierStyleCrossRefs" href="#bib0480">[15,16]</a>.Microbial signals regulate the release of fasting-induced adipose factor (FIAF) from intestinal epithelial cells, acting as a lipoprotein lipase inhibitor and regulating the storage of peripheral fat. In addition, by unknown mechanisms, the IM regulates the energy mediator in the liver and muscle via phosphorylation of AMP-activated protein kinase (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>) <a class="elsevierStyleCrossRef" href="#bib0490">[17]</a>.<elsevierMultimedia ident="fig0005"></elsevierMultimedia>Microbial metabolites, such as short chain fatty acids (SCFAs), bind to conjugate receptors of G protein on intestinal epithelial cells by regulating energy from gut-derived hormones, such as the intestinal peptide hormone, and controlling the inflammatory response of the host. The activation of Toll-like receptor-5) in the epithelia or myeloid cells affects the structural composition of the intestinal microbiota, which regulates appetite, weight gain and insulin sensitivity (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>) <a class="elsevierStyleCrossRef" href="#bib0495">[18]</a>.It is suspected that the intestinal microbiota of obese individuals presents peculiarities that may induce chronic inflammation. The induction of endotoxemia in obesity, diabetes mellitus and insulin resistance causes the expression of inflammatory factors that resemble those present in a diet rich in fat <a class="elsevierStyleCrossRef" href="#bib0500">[19]</a>.Obesity and diet composition can cause sensitivity to the intestinal barrier and result in the malfunction of the intestine–liver axis, allowing the indiscriminate passage of bacterial components into circulation. The intestinal barrier is a complex functional unit composed of luminal and mucosal elements, such as the epithelial cell layer, the mucosal barrier, and innate and acquired immune components. This barrier plays a key role in protecting against enteric organisms, potentially harmful toxins and bacterial bioproducts that are closely associated with health and disease susceptibility <a class="elsevierStyleCrossRefs" href="#bib0505">[20,21]</a>. The intestine–liver axis refers to the anatomical and functional relationship between the gastrointestinal (GI) tract and the liver. The interaction between the two organs, whether healthy or diseased, includes the transfer of the IM and its potential hepatotoxic products to the liver <a class="elsevierStyleCrossRef" href="#bib0515">[22]</a>. Alterations in this axis (consisting of the intestinal barrier, the IM and the liver) may lead to changes in intestinal permeability favoring excessive pathogenic bacterial growth (dysbiosis). In particular, the excessive growth of Gram-negative bacteria increases the production of hepatotoxic products such as lipopolysaccharides (LPS), which in turn stimulate Toll-like receptor-4 and ultimately nuclear factor kappa B (NF-kβ) and proinflammatory cytokines, such as interleukin-6, transforming growth factor-beta and tumor necrosis factor-alpha (TNF-α) <a class="elsevierStyleCrossRefs" href="#bib0520">[23,24]</a>.3Intestinal microbiota and dietThe relationship between the diet and the composition and function of the IM is evident. Indeed, bacteria in the gut are responsible for the digestion and production of many essential vitamins and minerals. The dietary components provide nutrients for bacteria, which then produce metabolites involved in energy balance, metabolism, and immune response, but these metabolites can also result in obesity and metabolic diseases <a class="elsevierStyleCrossRefs" href="#bib0530">[25,26]</a>. The high caloric content of the Western diet (high in fat and carbohydrates) is a major contributor to weight gain, which is associated with an altered IM <a class="elsevierStyleCrossRefs" href="#bib0540">[27,28]</a>. A recent study showed that the IM promotes intestinal absorption and the transfer of monosaccharides to the portal circulation by increasing the expression of the glucose-1 transporter in the small intestine. This increased carbohydrate flow stimulates lipogenesis in the liver and adipose tissue <a class="elsevierStyleCrossRef" href="#bib0480">[15]</a>. A study comparing a control diet vs. diets high in nondigestible carbohydrates (fibers) demonstrated that nondigestible carbohydrates produce significant changes in the species composition (E. rectale and Ruminococcus bromii) of the IM within a number of days <a class="elsevierStyleCrossRef" href="#bib0550">[29]</a>. The link between diet, IM, and health has been shown in animal models that were switched from low-fat/fiber rich plant diets to high-fat/high-sugar diets and exhibited significant increases in Bacilli and Erysipelotrichia from the Firmicutes phylum, which were associated with a significant decrease in the abundance of members of the Bacteroidetes phylum <a class="elsevierStyleCrossRef" href="#bib0555">[30]</a>. The GI transit time could be affected by the IM according to Kashyap et al. They proposed an animal model to evaluate the interactions between diet, IM, and GI transit time in the host. Diet can independently affect both GI transit time and IM composition and function (as determined by metabolite profiles). However, diet-induced changes in microbial composition may be mediated in part by changes in GI transit time, and the effect of diet on GI transit time may be a result of altered functionality of the IM community caused by the dietary change <a class="elsevierStyleCrossRef" href="#bib0560">[31]</a>.4Intestinal microbiota and NAFLD/NASHNonalcoholic fatty liver disease (NAFLD) is one of the most common chronic liver disorders worldwide due to the epidemic increase in the prevalence of obesity in affluent societies <a class="elsevierStyleCrossRef" href="#bib0565">[32]</a>. NAFLD includes a wide spectrum of hepatic pathological characteristics ranging from simple steatosis to nonalcoholic steatohepatitis (NASH) with or without fibrosis, cirrhosis, and hepatocellular carcinoma <a class="elsevierStyleCrossRef" href="#bib0570">[33]</a>. The development and progression of NAFLD involve complex pathophysiological processes <a class="elsevierStyleCrossRef" href="#bib0565">[32]</a> that are influenced by host factors such as genetic polymorphisms, diet, and, as reported more recently, the composition of the IM <a class="elsevierStyleCrossRefs" href="#bib0575">[34,35]</a>.The IM and its derived metabolites may also contribute to the development of NAFLD. Increased intestinal permeability stimulates monosaccharide absorption from the intestinal lumen, leading to bacterial translocation. The endotoxins produced by these bacteria penetrate the portal vein and decrease FIAF secretion by increasing LPL activity, promoting de novo fatty acid synthesis and triglyceride production <a class="elsevierStyleCrossRef" href="#bib0450">[9]</a> and activating inflammatory Toll-like receptors in hepatocytes <a class="elsevierStyleCrossRef" href="#bib0520">[23]</a>. A permeable intestinal barrier and small intestine bacterial overgrowth, which is a condition in which elevated levels of small intestinal bacteria lead to abdominal distension and other common symptoms related to irritable bowel syndrome, are frequent in obese patients and induce liver injury by increasing LPS production derived from Gram-negative bacteria in the gut, which activates NF-kβ and TNF-α production. This suggests that IM increases liver exposure to endotoxins, which play an important role in the progression of NASH (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>) <a class="elsevierStyleCrossRefs" href="#bib0585">[36,37]</a>.<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Miele et al. showed that NAFLD is associated with increased intestinal permeability and SIBO, and these factors are associated with the severity of hepatic steatosis. They reported evidence of a “leaky” intestine with tight junction disruption in human NAFLD with evidence of increased small intestine bacterial overgrowth <a class="elsevierStyleCrossRef" href="#bib0595">[38]</a>. Some studies in animal models and NAFLD or NASH patients showed an association with small bowel overgrowth and increased intestinal permeability <a class="elsevierStyleCrossRefs" href="#bib0600">[39–42]</a>. Brun et al. demonstrated that leptin-deficient obese mice naturally presented increased intestinal permeability, higher circulation of inflammatory cytokines and increased serum levels of LPS <a class="elsevierStyleCrossRef" href="#bib0605">[40]</a>. Another study showed that LPS in mice simulated the effects of a high-fat diet by metabolic endotoxemia, which led to dysregulation of inflammation and triggered body weight gain, IR, and the development of NAFLD <a class="elsevierStyleCrossRef" href="#bib0620">[43]</a>. Studies involving obese and NAFLD patients showed an association between metabolic endotoxemia and hepatic and systemic inflammation <a class="elsevierStyleCrossRefs" href="#bib0610">[41,43,44]</a>. Verdam et al. also observed an increase in plasma antibodies against LPS in patients with NASH compared to healthy controls. This increase was directly proportional to the increased severity of liver disease <a class="elsevierStyleCrossRef" href="#bib0630">[45]</a>. A recent study showed that obese patients with NASH had a decreased abundance of Faecalibacterium<a class="elsevierStyleCrossRef" href="#bib0635">[46]</a>. Species of Faecalibacterium exhibited anti-inflammatory effects, partly due to secreted metabolites that block NF-kB activation and interleukin 8 (IL-8) secretion. In addition, the effects were associated with a decrease in proinflammatory colonic cytokine synthesis and with the induction of anti-inflammatory cytokine secretion <a class="elsevierStyleCrossRef" href="#bib0640">[47]</a>.Recently, our group demonstrated a decreased abundance of Faecalibacterium and Ruminococcus in lean NASH patients <a class="elsevierStyleCrossRef" href="#bib0645">[48]</a>. Ruminococcus belongs to the family Ruminococcaceae, which are also fermenting anaerobes that lead to the production of SCFAs, promoting the development of NAFLD <a class="elsevierStyleCrossRef" href="#bib0650">[49]</a>. Interestingly, in the same study, advanced fibrosis (stage >2) was associated with an increase in Lactobacillus in obese NASH patients <a class="elsevierStyleCrossRef" href="#bib0645">[48]</a>. The genus Lactobacillus comprises more than 180 species with important immunological functions and metabolic activities <a class="elsevierStyleCrossRef" href="#bib0655">[50]</a>. Some of these bacteria produce lactic acid from the fermentation of carbohydrates in the diet and can produce acetate and ethanol <a class="elsevierStyleCrossRef" href="#bib0660">[51]</a>, which can induce liver damage, such as inflammation, leading to the progression of NASH <a class="elsevierStyleCrossRef" href="#bib0665">[52]</a>.Some studies have shown an association between Bacteroides and Escherichia and advanced fibrosis <a class="elsevierStyleCrossRefs" href="#bib0670">[53,54]</a>; Bifidobacterium spp. and Akkermansia muciniphila were strongly associated with markers of lipid metabolism and negatively associated with inflammation in adipose tissue and circulating glucose, leptin, triglycerides and insulin <a class="elsevierStyleCrossRef" href="#bib0680">[55]</a>. Despite the fact that the diet is directly connected to dysbiosis, a study showed that the IM of a genetically obese human could promote the onset of liver steatosis independent of dietary factors <a class="elsevierStyleCrossRef" href="#bib0510">[21]</a>.A possible mechanism by which the MI contributes to the development of NAFLD may be related to the amount of ethanol produced by bacteria (Escherichia coli) <a class="elsevierStyleCrossRef" href="#bib0685">[56]</a>. The ethanol produced by these bacteria contributes to physiological and morphological changes in the intestinal barrier associated with small intestine bacterial overgrowth by increasing intestinal permeability and thereby increasing the passage of endotoxins from the intestinal lumen to the portal blood, leading to an increase in the production of reactive oxygen species, which stimulates hepatic inflammation <a class="elsevierStyleCrossRef" href="#bib0690">[57]</a>. Ethanol is constantly produced by the MI even in the absence of alcohol ingestion. It has been found that a diet rich in refined sugar can lead to increased levels of alcohol in the blood and that ingested ethanol is eliminated via the enzyme alcohol dehydrogenase in the liver. This enzyme converts the alcohol into acetaldehyde, which, even in small concentrations, is toxic to the body <a class="elsevierStyleCrossRef" href="#bib0695">[58]</a>. The production of ethanol by the MI in obese and eutrophic patients with NASH suggests that it may contribute to the development and progression of the disease <a class="elsevierStyleCrossRef" href="#bib0700">[59]</a>.Another product of the metabolism of nutrients by bacteria that may be toxic to the liver is trimethylamine N-oxide. The IM can promote the conversion of choline to trimethylamine, which will then reach the liver by the circulation gate and will be converted into trimethylamine N-oxide <a class="elsevierStyleCrossRef" href="#bib0615">[42]</a>. The increase in the production of this compound leads to a decrease in the exportation of hepatic very-low-density lipoprotein and the modulation of bile acid synthesis, which has detrimental effects on the liver, such as increased liver fat deposition and inflammatory and oxidative lesions and decreased glucose metabolism <a class="elsevierStyleCrossRef" href="#bib0705">[60]</a>.NAFLD patients are characterized by a significant increase in circulating levels of endotoxins, which may represent an important early marker of potential liver abnormality <a class="elsevierStyleCrossRef" href="#bib0710">[61]</a>. Furthermore, gut dysbiosis may be associated with changes in the level of serum metabolites, including branched-chain amino acids and aromatic amino acids. Moreover, BCAAs are increased in individuals with IR, which is considered the major risk factor for hepatic steatosis <a class="elsevierStyleCrossRef" href="#bib0715">[62]</a>.5Prebiotics and probiotics and the intestinal microbiotaCurrent studies have shown that the use of prebiotics and probiotics can modulate the MI in several diseases, including NAFLD <a class="elsevierStyleCrossRefs" href="#bib0720">[63–65]</a>.Probiotics improve the composition of the MI, which is associated with a reduction in liver inflammation, a decrease in LPS concentrations and an improvement in aminotransferase concentrations <a class="elsevierStyleCrossRefs" href="#bib0735">[66,67]</a>. Probiotic supplementation can improve inflammatory factors <a class="elsevierStyleCrossRefs" href="#bib0745">[68,69]</a> and improve metabolic parameters of NAFLD, such as visceral fat, total cholesterol and IR <a class="elsevierStyleCrossRef" href="#bib0755">[70]</a>. In addition, the consumption of probiotics has been associated with a decrease in low-density lipoprotein levels in animals and in humans with hypercholesterolemia <a class="elsevierStyleCrossRefs" href="#bib0760">[71,72]</a>. Cano et al. demonstrated that the consumption of the Bifidobacterium pseudocatenulatum probiotic bacteria improved glucose tolerance, inflammatory status and hepatic steatosis <a class="elsevierStyleCrossRef" href="#bib0770">[73]</a>.Prebiotics can modulate the IM by increasing beneficial bacteria in the intestine, particularly Bifidobacteria and Lactobacilli, and inhibit bacterial activities that are detrimental to host health <a class="elsevierStyleCrossRef" href="#bib0775">[74]</a>. In addition, in the large intestine, inulin-type fructan and resistant starches are completely catabolized by the microbiota and are transformed into SCFAs, bacterial biomass and organic acids such as lactic acid and gases (carbon dioxide, hydrogen and methane) <a class="elsevierStyleCrossRef" href="#bib0735">[66]</a>. Data suggest that altering the microbiota through the use of prebiotics leads to decreased hepatic lipogenesis and blood TG levels and increases the concentration of SCFAs; however, the ability to modulate the intestinal microbiota and liver function in patients with NAFLD should be investigated <a class="elsevierStyleCrossRefs" href="#bib0780">[75–77]</a>.Recent studies have shown that the use of prebiotics and probiotics can be an alternative therapy in the treatment of NAFLD. In an experimental model of NAFLD, it was observed that the use of synbiotics can reduce hepatic aminotransferases and IL-6 expression. However, the histology showed that the synbiotic was not able to prevent the progression of the disease <a class="elsevierStyleCrossRef" href="#bib0795">[78]</a>. A randomized clinical trial demonstrated that the use of multistrain probiotics was able to modulate the IM, thereby significantly reducing fatty liver and aminotransferase activity and reducing the expression of TNF-α and IL6 in NAFLD patients <a class="elsevierStyleCrossRef" href="#bib0800">[79]</a>. Another randomized study showed that synbiotic supplementation improves hepatic steatosis, aspartate aminotransferase levels, lipid profile and homeostatic model assessment) in NAFLD patients <a class="elsevierStyleCrossRef" href="#bib0725">[64]</a>. A study in NASH patients also showed that the use of synbiotics (Bifidobacterium longum and fructooligosaccharide), in combination with lifestyle modification (diet and exercise), improved aspartate aminotransferase, low-density lipoprotein, and TNF-α, leading to decreased endotoxins, IR and steatosis <a class="elsevierStyleCrossRef" href="#bib0805">[80]</a>. In addition, a study conducted by Eslamparast et al. corroborated the conclusion that the use of synbiotics combined with physical exercise improves aminotransferase levels, TNF-α and NF-kβ <a class="elsevierStyleCrossRef" href="#bib0810">[81]</a>.In conclusion, some evidence has demonstrated the role of the IM in the pathogenesis of NAFLD/NASH; however, it is necessary to explore how the IM can be modulated to improve NAFLD/NASH progression. Future randomized studies involving diet and/or probiotics should be performed.AbbreviationsGIgastrointestinalIMintestinal microbiotaLPSlipopolysaccharidesNAFLDnonalcoholic fatty liver diseaseNASHnonalcoholic steatohepatitisNF-kβnuclear factor-kappa BSCFAshort-chain fatty acidTNF-αtumor necrosis factor-alphaConflict of interestThe authors have no conflicts of interest to declare." "textoCompletoSecciones" => array:1 [ "secciones" => array:9 [ 0 => array:3 [ "identificador" => "xres1199031" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1117471" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "sec0005" "titulo" => "Human intestinal microbiota" ] 3 => array:2 [ "identificador" => "sec0010" "titulo" => "Intestinal microbiota and obesity" ] 4 => array:2 [ "identificador" => "sec0015" "titulo" => "Intestinal microbiota and diet" ] 5 => array:2 [ "identificador" => "sec0020" "titulo" => "Intestinal microbiota and NAFLD/NASH" ] 6 => array:2 [ "identificador" => "sec0025" "titulo" => "Prebiotics and probiotics and the intestinal microbiota" ] 7 => array:2 [ "identificador" => "sec0030" "titulo" => "Conflict of interest" ] 8 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2019-01-07" "fechaAceptado" => "2019-01-09" "PalabrasClave" => array:1 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1117471" "palabras" => array:5 [ 0 => "NAFLD" 1 => "NASH" 2 => "Intestinal microbiota" 3 => "Dysbiosis" 4 => "Probiotics" ] ] ] ] "tieneResumen" => true "resumen" => array:1 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Genetic predisposition, the intestinal microbiota (IM) and environmental factors, such as sedentary lifestyle and inadequate diet, should be considered as critical factors for the development of nonalcoholic fatty liver disease (NAFLD). Recently, some studies have demonstrated an association between dysbiosis and NAFLD; however, the exact mechanisms that lead to intestinal membrane damage, bacterial translocation and inflammation are not well elucidated. Due to the relevance of this theme, the IM and its metabolites have received special attention in recent years in an attempt to better understand the mechanisms related to the prevention, physiopathology, and treatment of NAFLD. In this paper, we provide a review of the human IM and its role in diet, obesity, and the development/progression of NAFLD/NASH, as well as the use of prebiotics and probiotics in the modulation of IM." ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2195 "Ancho" => 2667 "Tamanyo" => 732516 ] ] "descripcion" => array:1 [ "en" => "Possible mechanisms related to the intestinal microbiota that lead to energy imbalance and consequently obesity. FIAF, fasting-induced adipose factor; Gpr41/43, G-protein coupled receptor; LPL, lipoprotein lipase; SCFAs, short chain fatty acids; AMPK, AMP-activated protein kinase; TRL5, Toll-like receptor-5." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2535 "Ancho" => 3000 "Tamanyo" => 420405 ] ] "descripcion" => array:1 [ "en" => "The role of the intestinal microbiota in the development of fatty liver. Intestinal dysbiosis may be a determining factor for the development and progression of NAFLD/NASH. The increase in pathogenic bacteria and Gram-negative bacteria increases dietary energy extraction, leading to increased intestinal permeability and bacterial translocation, stimulating de novo fatty acid synthesis and increasing LPS expression, as well as the expression of NF-kβ and TNF-α. 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Sebastião M.B. Duartea,b, Jose Tadeu Stefanoa, Claudia P. Oliveiraa,b,

Corresponding author

cpm@usp.br

Corresponding author at: Laboratório de Gastroenterologia Clínica e Experimental (LIM-07) do Departamento de Gastroenterologia e Hepatologia do Hospital das Clínicas HCFMUSP da Faculdade de Medicina da Universidade de São Paulo, Av. Dr. Enéas, 455, 3° andar, sala 3115, CEP 01246903, São Paulo, SP, Brazil.

a Laboratório de Gastroenterologia Clínica e Experimental (LIM-07) do Departamento de Gastroenterologia e Hepatologia do Hospital das Clínicas HCFMUSP da Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brazil

b Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brazil

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include metabolic and immunological activities&#46; The prominent metabolic function of the IM is the fermentation of nondigestible components of the diet&#46; The products of this complex metabolic activity are a spectrum of organic acids&#44; which are an important source of energy for the host&#46; The epithelial cells of the gut participate in immunological processes&#46; The signaling pathways of these cells are highly regulated to avert uncontrolled inflammatory responses <a class="elsevierStyleCrossRef" href="#bib0425">&#91;4&#93;</a>&#46; The gut epithelium is a major barrier between the host and the environment&#46; This barrier is formed by tight junctions that act as a highly regulated entry that open and close depending on signals&#44; such as those from cytokines and bacterial components from the lumen&#44; and excessive contact with bacteria may cause an increase in the proinflammatory immune response <a class="elsevierStyleCrossRef" href="#bib0430">&#91;5&#93;</a>&#46; Therefore&#44; the IM supports immune regulation and ensures that effector immune responses are activated in response to invading pathogens <a class="elsevierStyleCrossRef" href="#bib0435">&#91;6&#93;</a>&#46; Another important function of the IM is protection against exogenous microorganisms&#46; These bacteria can inhibit the growth of pathogenic microorganisms through the synthesis of antimicrobial substances or by competing for nutrients and reducing the attachment and penetration of the enteroinvasive pathogen into epithelial cells <a class="elsevierStyleCrossRef" href="#bib0440">&#91;7&#93;</a>&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">The IM has a heterogeneous distribution&#44; with the colon being the place with the greatest density due to the favorable conditions for the proliferation of microorganisms&#44; characterized by slow peristalsis&#44; absence of intestinal secretions and presence of a nutritional supply <a class="elsevierStyleCrossRef" href="#bib0445">&#91;8&#93;</a>&#46; Dysbiosis generates bacterial overgrowth&#44; toxin production and increased intestinal permeability&#44; resulting in changes in immunological and hormonal effects&#46; Thus&#44; lifestyle habits such as diet&#44; stress and the use of antibiotics&#44; for example&#44; cause the transient microbiota to prevail over the resident microbiota&#44; predisposing the host to gastrointestinal disorders&#46; The actions that the IM exerts on the various systems of the organism also reflect the maintenance of the metabolism <a class="elsevierStyleCrossRef" href="#bib0450">&#91;9&#93;</a>&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">Approximately 98&#37; of all bacterial species that make up the IM belong to the following phyla&#58; <span class="elsevierStyleItalic">Firmicutes</span> &#40;64&#37;&#41; and <span class="elsevierStyleItalic">Bacteroidetes</span> &#40;23&#37;&#41;&#44; which represent most of the IM in addition to <span class="elsevierStyleItalic">Proteobacteria</span> &#40;8&#37;&#41; and <span class="elsevierStyleItalic">Actinobacteria</span> &#40;3&#37;&#41; <a class="elsevierStyleCrossRef" href="#bib0455">&#91;10&#93;</a>&#46; The Firmicutes phylum contains more than 250 genera&#44; including <span class="elsevierStyleItalic">Lactobacillus</span><a class="elsevierStyleCrossRef" href="#bib0460">&#91;11&#93;</a>&#46; The phylum <span class="elsevierStyleItalic">Bacteroidetes</span>&#44; similar to Firmicutes&#44; is found in the small and large intestines&#44; especially in the colon&#44; and encompasses several genera&#44; such as <span class="elsevierStyleItalic">Bacteroides</span>&#44; <span class="elsevierStyleItalic">Flavobacteria</span> and <span class="elsevierStyleItalic">Sphingobacteriales</span>&#44; with <span class="elsevierStyleItalic">Bacteroides thetaiotaomicron</span> being one of the most abundant <a class="elsevierStyleCrossRef" href="#bib0465">&#91;12&#93;</a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Although the functions of the bacteria belonging to the Firmicutes phylum have not yet been fully elucidated&#44; evidence suggests that some members of this phylum&#44; such as <span class="elsevierStyleItalic">Clostridium butyricum</span> bacteria&#44; are among the bacteria producing butyric acid from lactic acid or lactose in a chemical reaction known as butyric fermentation&#44; and this type of fermentation increases the energy extracted from the diet <a class="elsevierStyleCrossRef" href="#bib0470">&#91;13&#93;</a>&#46; On the other hand&#44; members of the Bacteroidetes phylum participate in the metabolism of carbohydrates and perform this metabolism by expressing enzymes similar to the glycosyltransferases&#44; which promote glycosylation&#44; that is&#44; to join carbohydrates to the proteins formed in the ribosomes&#46; Members of the <span class="elsevierStyleItalic">Bacteroidetes</span> phylum also express glycoside hydrolases that degrade biomass&#44; such as cellulose and hemicellulose&#44; in antibacterial defense strategies&#46; Finally&#44; they also express the polysaccharide-lyase enzyme that catalyzes the breakdown of a carbon&#8211;oxygen bond in polysaccharides&#44; leading to an unsaturated product and the elimination of alcohol <a class="elsevierStyleCrossRef" href="#bib0475">&#91;14&#93;</a>&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">2</span><span class="elsevierStyleSectionTitle" id="sect0020">Intestinal microbiota and obesity</span><p id="par0030" class="elsevierStylePara elsevierViewall">Intestinal microorganisms influence energy production&#44; energy homeostasis and&#44; potentially&#44; the development of obesity and metabolic disorders <a class="elsevierStyleCrossRef" href="#bib0460">&#91;11&#93;</a>&#46; Increasing evidence supports the importance of the composition of the IM for the development of obesity and demonstrates that the type and quantity of the bacterial population can determine some important characteristics of metabolic pathways that play an important role in obesity <a class="elsevierStyleCrossRefs" href="#bib0480">&#91;15&#44;16&#93;</a>&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Microbial signals regulate the release of fasting-induced adipose factor &#40;FIAF&#41; from intestinal epithelial cells&#44; acting as a lipoprotein lipase inhibitor and regulating the storage of peripheral fat&#46; In addition&#44; by unknown mechanisms&#44; the IM regulates the energy mediator in the liver and muscle via phosphorylation of AMP-activated protein kinase &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41; <a class="elsevierStyleCrossRef" href="#bib0490">&#91;17&#93;</a>&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall">Microbial metabolites&#44; such as short chain fatty acids &#40;SCFAs&#41;&#44; bind to conjugate receptors of G protein on intestinal epithelial cells by regulating energy from gut-derived hormones&#44; such as the intestinal peptide hormone&#44; and controlling the inflammatory response of the host&#46; The activation of Toll-like receptor-5&#41; in the epithelia or myeloid cells affects the structural composition of the intestinal microbiota&#44; which regulates appetite&#44; weight gain and insulin sensitivity &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41; <a class="elsevierStyleCrossRef" href="#bib0495">&#91;18&#93;</a>&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">It is suspected that the intestinal microbiota of obese individuals presents peculiarities that may induce chronic inflammation&#46; The induction of endotoxemia in obesity&#44; diabetes mellitus and insulin resistance causes the expression of inflammatory factors that resemble those present in a diet rich in fat <a class="elsevierStyleCrossRef" href="#bib0500">&#91;19&#93;</a>&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Obesity and diet composition can cause sensitivity to the intestinal barrier and result in the malfunction of the intestine&#8211;liver axis&#44; allowing the indiscriminate passage of bacterial components into circulation&#46; The intestinal barrier is a complex functional unit composed of luminal and mucosal elements&#44; such as the epithelial cell layer&#44; the mucosal barrier&#44; and innate and acquired immune components&#46; This barrier plays a key role in protecting against enteric organisms&#44; potentially harmful toxins and bacterial bioproducts that are closely associated with health and disease susceptibility <a class="elsevierStyleCrossRefs" href="#bib0505">&#91;20&#44;21&#93;</a>&#46; The intestine&#8211;liver axis refers to the anatomical and functional relationship between the gastrointestinal &#40;GI&#41; tract and the liver&#46; The interaction between the two organs&#44; whether healthy or diseased&#44; includes the transfer of the IM and its potential hepatotoxic products to the liver <a class="elsevierStyleCrossRef" href="#bib0515">&#91;22&#93;</a>&#46; Alterations in this axis &#40;consisting of the intestinal barrier&#44; the IM and the liver&#41; may lead to changes in intestinal permeability favoring excessive pathogenic bacterial growth &#40;dysbiosis&#41;&#46; In particular&#44; the excessive growth of Gram-negative bacteria increases the production of hepatotoxic products such as lipopolysaccharides &#40;LPS&#41;&#44; which in turn stimulate Toll-like receptor-4 and ultimately nuclear factor kappa B &#40;NF-k&#946;&#41; and proinflammatory cytokines&#44; such as interleukin-6&#44; transforming growth factor-beta and tumor necrosis factor-alpha &#40;TNF-&#945;&#41; <a class="elsevierStyleCrossRefs" href="#bib0520">&#91;23&#44;24&#93;</a>&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">3</span><span class="elsevierStyleSectionTitle" id="sect0025">Intestinal microbiota and diet</span><p id="par0055" class="elsevierStylePara elsevierViewall">The relationship between the diet and the composition and function of the IM is evident&#46; Indeed&#44; bacteria in the gut are responsible for the digestion and production of many essential vitamins and minerals&#46; The dietary components provide nutrients for bacteria&#44; which then produce metabolites involved in energy balance&#44; metabolism&#44; and immune response&#44; but these metabolites can also result in obesity and metabolic diseases <a class="elsevierStyleCrossRefs" href="#bib0530">&#91;25&#44;26&#93;</a>&#46; The high caloric content of the Western diet &#40;high in fat and carbohydrates&#41; is a major contributor to weight gain&#44; which is associated with an altered IM <a class="elsevierStyleCrossRefs" href="#bib0540">&#91;27&#44;28&#93;</a>&#46; A recent study showed that the IM promotes intestinal absorption and the transfer of monosaccharides to the portal circulation by increasing the expression of the glucose-1 transporter in the small intestine&#46; This increased carbohydrate flow stimulates lipogenesis in the liver and adipose tissue <a class="elsevierStyleCrossRef" href="#bib0480">&#91;15&#93;</a>&#46; A study comparing a control diet vs&#46; diets high in nondigestible carbohydrates &#40;fibers&#41; demonstrated that nondigestible carbohydrates produce significant changes in the species composition &#40;<span class="elsevierStyleItalic">E&#46; rectale</span> and <span class="elsevierStyleItalic">Ruminococcus bromii</span>&#41; of the IM within a number of days <a class="elsevierStyleCrossRef" href="#bib0550">&#91;29&#93;</a>&#46; The link between diet&#44; IM&#44; and health has been shown in animal models that were switched from low-fat&#47;fiber rich plant diets to high-fat&#47;high-sugar diets and exhibited significant increases in <span class="elsevierStyleItalic">Bacilli</span> and <span class="elsevierStyleItalic">Erysipelotrichia</span> from the <span class="elsevierStyleItalic">Firmicutes</span> phylum&#44; which were associated with a significant decrease in the abundance of members of the <span class="elsevierStyleItalic">Bacteroidetes</span> phylum <a class="elsevierStyleCrossRef" href="#bib0555">&#91;30&#93;</a>&#46; The GI transit time could be affected by the IM according to Kashyap <span class="elsevierStyleItalic">et al&#46;</span> They proposed an animal model to evaluate the interactions between diet&#44; IM&#44; and GI transit time in the host&#46; Diet can independently affect both GI transit time and IM composition and function &#40;as determined by metabolite profiles&#41;&#46; However&#44; diet-induced changes in microbial composition may be mediated in part by changes in GI transit time&#44; and the effect of diet on GI transit time may be a result of altered functionality of the IM community caused by the dietary change <a class="elsevierStyleCrossRef" href="#bib0560">&#91;31&#93;</a>&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">4</span><span class="elsevierStyleSectionTitle" id="sect0030">Intestinal microbiota and NAFLD&#47;NASH</span><p id="par0060" class="elsevierStylePara elsevierViewall">Nonalcoholic fatty liver disease &#40;NAFLD&#41; is one of the most common chronic liver disorders worldwide due to the epidemic increase in the prevalence of obesity in affluent societies <a class="elsevierStyleCrossRef" href="#bib0565">&#91;32&#93;</a>&#46; NAFLD includes a wide spectrum of hepatic pathological characteristics ranging from simple steatosis to nonalcoholic steatohepatitis &#40;NASH&#41; with or without fibrosis&#44; cirrhosis&#44; and hepatocellular carcinoma <a class="elsevierStyleCrossRef" href="#bib0570">&#91;33&#93;</a>&#46; The development and progression of NAFLD involve complex pathophysiological processes <a class="elsevierStyleCrossRef" href="#bib0565">&#91;32&#93;</a> that are influenced by host factors such as genetic polymorphisms&#44; diet&#44; and&#44; as reported more recently&#44; the composition of the IM <a class="elsevierStyleCrossRefs" href="#bib0575">&#91;34&#44;35&#93;</a>&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">The IM and its derived metabolites may also contribute to the development of NAFLD&#46; Increased intestinal permeability stimulates monosaccharide absorption from the intestinal lumen&#44; leading to bacterial translocation&#46; The endotoxins produced by these bacteria penetrate the portal vein and decrease FIAF secretion by increasing LPL activity&#44; promoting de novo fatty acid synthesis and triglyceride production <a class="elsevierStyleCrossRef" href="#bib0450">&#91;9&#93;</a> and activating inflammatory Toll-like receptors in hepatocytes <a class="elsevierStyleCrossRef" href="#bib0520">&#91;23&#93;</a>&#46; A permeable intestinal barrier and small intestine bacterial overgrowth&#44; which is a condition in which elevated levels of small intestinal bacteria lead to abdominal distension and other common symptoms related to irritable bowel syndrome&#44; are frequent in obese patients and induce liver injury by increasing LPS production derived from Gram-negative bacteria in the gut&#44; which activates NF-k&#946; and TNF-&#945; production&#46; This suggests that IM increases liver exposure to endotoxins&#44; which play an important role in the progression of NASH &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41; <a class="elsevierStyleCrossRefs" href="#bib0585">&#91;36&#44;37&#93;</a>&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">Miele <span class="elsevierStyleItalic">et al&#46;</span> showed that NAFLD is associated with increased intestinal permeability and SIBO&#44; and these factors are associated with the severity of hepatic steatosis&#46; They reported evidence of a &#8220;leaky&#8221; intestine with tight junction disruption in human NAFLD with evidence of increased small intestine bacterial overgrowth <a class="elsevierStyleCrossRef" href="#bib0595">&#91;38&#93;</a>&#46; Some studies in animal models and NAFLD or NASH patients showed an association with small bowel overgrowth and increased intestinal permeability <a class="elsevierStyleCrossRefs" href="#bib0600">&#91;39&#8211;42&#93;</a>&#46; Brun <span class="elsevierStyleItalic">et al&#46;</span> demonstrated that leptin-deficient obese mice naturally presented increased intestinal permeability&#44; higher circulation of inflammatory cytokines and increased serum levels of LPS <a class="elsevierStyleCrossRef" href="#bib0605">&#91;40&#93;</a>&#46; Another study showed that LPS in mice simulated the effects of a high-fat diet by metabolic endotoxemia&#44; which led to dysregulation of inflammation and triggered body weight gain&#44; IR&#44; and the development of NAFLD <a class="elsevierStyleCrossRef" href="#bib0620">&#91;43&#93;</a>&#46; Studies involving obese and NAFLD patients showed an association between metabolic endotoxemia and hepatic and systemic inflammation <a class="elsevierStyleCrossRefs" href="#bib0610">&#91;41&#44;43&#44;44&#93;</a>&#46; Verdam <span class="elsevierStyleItalic">et al&#46;</span> also observed an increase in plasma antibodies against LPS in patients with NASH compared to healthy controls&#46; This increase was directly proportional to the increased severity of liver disease <a class="elsevierStyleCrossRef" href="#bib0630">&#91;45&#93;</a>&#46; A recent study showed that obese patients with NASH had a decreased abundance of <span class="elsevierStyleItalic">Faecalibacterium</span><a class="elsevierStyleCrossRef" href="#bib0635">&#91;46&#93;</a>&#46; Species of <span class="elsevierStyleItalic">Faecalibacterium</span> exhibited anti-inflammatory effects&#44; partly due to secreted metabolites that block NF-kB activation and interleukin 8 &#40;IL-8&#41; secretion&#46; In addition&#44; the effects were associated with a decrease in proinflammatory colonic cytokine synthesis and with the induction of anti-inflammatory cytokine secretion <a class="elsevierStyleCrossRef" href="#bib0640">&#91;47&#93;</a>&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Recently&#44; our group demonstrated a decreased abundance of <span class="elsevierStyleItalic">Faecalibacterium</span> and <span class="elsevierStyleItalic">Ruminococcus</span> in lean NASH patients <a class="elsevierStyleCrossRef" href="#bib0645">&#91;48&#93;</a>&#46; <span class="elsevierStyleItalic">Ruminococcus</span> belongs to the family Ruminococcaceae&#44; which are also fermenting anaerobes that lead to the production of SCFAs&#44; promoting the development of NAFLD <a class="elsevierStyleCrossRef" href="#bib0650">&#91;49&#93;</a>&#46; Interestingly&#44; in the same study&#44; advanced fibrosis &#40;stage &#62;2&#41; was associated with an increase in <span class="elsevierStyleItalic">Lactobacillus</span> in obese NASH patients <a class="elsevierStyleCrossRef" href="#bib0645">&#91;48&#93;</a>&#46; The genus <span class="elsevierStyleItalic">Lactobacillus</span> comprises more than 180 species with important immunological functions and metabolic activities <a class="elsevierStyleCrossRef" href="#bib0655">&#91;50&#93;</a>&#46; Some of these bacteria produce lactic acid from the fermentation of carbohydrates in the diet and can produce acetate and ethanol <a class="elsevierStyleCrossRef" href="#bib0660">&#91;51&#93;</a>&#44; which can induce liver damage&#44; such as inflammation&#44; leading to the progression of NASH <a class="elsevierStyleCrossRef" href="#bib0665">&#91;52&#93;</a>&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Some studies have shown an association between <span class="elsevierStyleItalic">Bacteroides</span> and <span class="elsevierStyleItalic">Escherichia</span> and advanced fibrosis <a class="elsevierStyleCrossRefs" href="#bib0670">&#91;53&#44;54&#93;</a>&#59; <span class="elsevierStyleItalic">Bifidobacterium</span> spp&#46; and <span class="elsevierStyleItalic">Akkermansia muciniphila</span> were strongly associated with markers of lipid metabolism and negatively associated with inflammation in adipose tissue and circulating glucose&#44; leptin&#44; triglycerides and insulin <a class="elsevierStyleCrossRef" href="#bib0680">&#91;55&#93;</a>&#46; Despite the fact that the diet is directly connected to dysbiosis&#44; a study showed that the IM of a genetically obese human could promote the onset of liver steatosis independent of dietary factors <a class="elsevierStyleCrossRef" href="#bib0510">&#91;21&#93;</a>&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">A possible mechanism by which the MI contributes to the development of NAFLD may be related to the amount of ethanol produced by bacteria &#40;<span class="elsevierStyleItalic">Escherichia coli</span>&#41; <a class="elsevierStyleCrossRef" href="#bib0685">&#91;56&#93;</a>&#46; The ethanol produced by these bacteria contributes to physiological and morphological changes in the intestinal barrier associated with small intestine bacterial overgrowth by increasing intestinal permeability and thereby increasing the passage of endotoxins from the intestinal lumen to the portal blood&#44; leading to an increase in the production of reactive oxygen species&#44; which stimulates hepatic inflammation <a class="elsevierStyleCrossRef" href="#bib0690">&#91;57&#93;</a>&#46; Ethanol is constantly produced by the MI even in the absence of alcohol ingestion&#46; It has been found that a diet rich in refined sugar can lead to increased levels of alcohol in the blood and that ingested ethanol is eliminated via the enzyme alcohol dehydrogenase in the liver&#46; This enzyme converts the alcohol into acetaldehyde&#44; which&#44; even in small concentrations&#44; is toxic to the body <a class="elsevierStyleCrossRef" href="#bib0695">&#91;58&#93;</a>&#46; The production of ethanol by the MI in obese and eutrophic patients with NASH suggests that it may contribute to the development and progression of the disease <a class="elsevierStyleCrossRef" href="#bib0700">&#91;59&#93;</a>&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Another product of the metabolism of nutrients by bacteria that may be toxic to the liver is trimethylamine N-oxide&#46; The IM can promote the conversion of choline to trimethylamine&#44; which will then reach the liver by the circulation gate and will be converted into trimethylamine N-oxide <a class="elsevierStyleCrossRef" href="#bib0615">&#91;42&#93;</a>&#46; The increase in the production of this compound leads to a decrease in the exportation of hepatic very-low-density lipoprotein and the modulation of bile acid synthesis&#44; which has detrimental effects on the liver&#44; such as increased liver fat deposition and inflammatory and oxidative lesions and decreased glucose metabolism <a class="elsevierStyleCrossRef" href="#bib0705">&#91;60&#93;</a>&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">NAFLD patients are characterized by a significant increase in circulating levels of endotoxins&#44; which may represent an important early marker of potential liver abnormality <a class="elsevierStyleCrossRef" href="#bib0710">&#91;61&#93;</a>&#46; Furthermore&#44; gut dysbiosis may be associated with changes in the level of serum metabolites&#44; including branched-chain amino acids and aromatic amino acids&#46; Moreover&#44; BCAAs are increased in individuals with IR&#44; which is considered the major risk factor for hepatic steatosis <a class="elsevierStyleCrossRef" href="#bib0715">&#91;62&#93;</a>&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleLabel">5</span><span class="elsevierStyleSectionTitle" id="sect0035">Prebiotics and probiotics and the intestinal microbiota</span><p id="par0100" class="elsevierStylePara elsevierViewall">Current studies have shown that the use of prebiotics and probiotics can modulate the MI in several diseases&#44; including NAFLD <a class="elsevierStyleCrossRefs" href="#bib0720">&#91;63&#8211;65&#93;</a>&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">Probiotics improve the composition of the MI&#44; which is associated with a reduction in liver inflammation&#44; a decrease in LPS concentrations and an improvement in aminotransferase concentrations <a class="elsevierStyleCrossRefs" href="#bib0735">&#91;66&#44;67&#93;</a>&#46; Probiotic supplementation can improve inflammatory factors <a class="elsevierStyleCrossRefs" href="#bib0745">&#91;68&#44;69&#93;</a> and improve metabolic parameters of NAFLD&#44; such as visceral fat&#44; total cholesterol and IR <a class="elsevierStyleCrossRef" href="#bib0755">&#91;70&#93;</a>&#46; In addition&#44; the consumption of probiotics has been associated with a decrease in low-density lipoprotein levels in animals and in humans with hypercholesterolemia <a class="elsevierStyleCrossRefs" href="#bib0760">&#91;71&#44;72&#93;</a>&#46; Cano <span class="elsevierStyleItalic">et al&#46;</span> demonstrated that the consumption of the <span class="elsevierStyleItalic">Bifidobacterium pseudocatenulatum</span> probiotic bacteria improved glucose tolerance&#44; inflammatory status and hepatic steatosis <a class="elsevierStyleCrossRef" href="#bib0770">&#91;73&#93;</a>&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">Prebiotics can modulate the IM by increasing beneficial bacteria in the intestine&#44; particularly Bifidobacteria and Lactobacilli&#44; and inhibit bacterial activities that are detrimental to host health <a class="elsevierStyleCrossRef" href="#bib0775">&#91;74&#93;</a>&#46; In addition&#44; in the large intestine&#44; inulin-type fructan and resistant starches are completely catabolized by the microbiota and are transformed into SCFAs&#44; bacterial biomass and organic acids such as lactic acid and gases &#40;carbon dioxide&#44; hydrogen and methane&#41; <a class="elsevierStyleCrossRef" href="#bib0735">&#91;66&#93;</a>&#46; Data suggest that altering the microbiota through the use of prebiotics leads to decreased hepatic lipogenesis and blood TG levels and increases the concentration of SCFAs&#59; however&#44; the ability to modulate the intestinal microbiota and liver function in patients with NAFLD should be investigated <a class="elsevierStyleCrossRefs" href="#bib0780">&#91;75&#8211;77&#93;</a>&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">Recent studies have shown that the use of prebiotics and probiotics can be an alternative therapy in the treatment of NAFLD&#46; In an experimental model of NAFLD&#44; it was observed that the use of synbiotics can reduce hepatic aminotransferases and IL-6 expression&#46; However&#44; the histology showed that the synbiotic was not able to prevent the progression of the disease <a class="elsevierStyleCrossRef" href="#bib0795">&#91;78&#93;</a>&#46; A randomized clinical trial demonstrated that the use of multistrain probiotics was able to modulate the IM&#44; thereby significantly reducing fatty liver and aminotransferase activity and reducing the expression of TNF-&#945; and IL6 in NAFLD patients <a class="elsevierStyleCrossRef" href="#bib0800">&#91;79&#93;</a>&#46; Another randomized study showed that synbiotic supplementation improves hepatic steatosis&#44; aspartate aminotransferase levels&#44; lipid profile and homeostatic model assessment&#41; in NAFLD patients <a class="elsevierStyleCrossRef" href="#bib0725">&#91;64&#93;</a>&#46; A study in NASH patients also showed that the use of synbiotics &#40;<span class="elsevierStyleItalic">Bifidobacterium longum</span> and fructooligosaccharide&#41;&#44; in combination with lifestyle modification &#40;diet and exercise&#41;&#44; improved aspartate aminotransferase&#44; low-density lipoprotein&#44; and TNF-&#945;&#44; leading to decreased endotoxins&#44; IR and steatosis <a class="elsevierStyleCrossRef" href="#bib0805">&#91;80&#93;</a>&#46; In addition&#44; a study conducted by Eslamparast <span class="elsevierStyleItalic">et al&#46;</span> corroborated the conclusion that the use of synbiotics combined with physical exercise improves aminotransferase levels&#44; TNF-&#945; and NF-k&#946; <a class="elsevierStyleCrossRef" href="#bib0810">&#91;81&#93;</a>&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">In conclusion&#44; some evidence has demonstrated the role of the IM in the pathogenesis of NAFLD&#47;NASH&#59; however&#44; it is necessary to explore how the IM can be modulated to improve NAFLD&#47;NASH progression&#46; Future randomized studies involving diet and&#47;or probiotics should be performed&#46;<span class="elsevierStyleDefList"><span class="elsevierStyleSectionTitle" id="sect0040">Abbreviations</span><span class="elsevierStyleDefTerm">GI</span><span class="elsevierStyleDefDescription"><p id="par0125" class="elsevierStylePara elsevierViewall">gastrointestinal</p></span><span class="elsevierStyleDefTerm">IM</span><span class="elsevierStyleDefDescription"><p id="par0130" class="elsevierStylePara elsevierViewall">intestinal microbiota</p></span><span class="elsevierStyleDefTerm">LPS</span><span class="elsevierStyleDefDescription"><p id="par0135" class="elsevierStylePara elsevierViewall">lipopolysaccharides</p></span><span class="elsevierStyleDefTerm">NAFLD</span><span class="elsevierStyleDefDescription"><p id="par0140" class="elsevierStylePara elsevierViewall">nonalcoholic fatty liver disease</p></span><span class="elsevierStyleDefTerm">NASH</span><span class="elsevierStyleDefDescription"><p id="par0145" class="elsevierStylePara elsevierViewall">nonalcoholic steatohepatitis</p></span><span class="elsevierStyleDefTerm">NF-k&#946;</span><span class="elsevierStyleDefDescription"><p id="par0150" class="elsevierStylePara elsevierViewall">nuclear factor-kappa B</p></span><span class="elsevierStyleDefTerm">SCFA</span><span class="elsevierStyleDefDescription"><p id="par0155" class="elsevierStylePara elsevierViewall">short-chain fatty acid</p></span><span class="elsevierStyleDefTerm">TNF-&#945;</span><span class="elsevierStyleDefDescription"><p id="par0160" class="elsevierStylePara elsevierViewall">tumor necrosis factor-alpha</p></span></span></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Conflict of interest</span><p id="par0165" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare&#46;</p></span></span>"
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          "titulo" => "Intestinal microbiota and NAFLD&#47;NASH"
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          "identificador" => "sec0025"
          "titulo" => "Prebiotics and probiotics and the intestinal microbiota"
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            0 => "NAFLD"
            1 => "NASH"
            2 => "Intestinal microbiota"
            3 => "Dysbiosis"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Genetic predisposition&#44; the intestinal microbiota &#40;IM&#41; and environmental factors&#44; such as sedentary lifestyle and inadequate diet&#44; should be considered as critical factors for the development of nonalcoholic fatty liver disease &#40;NAFLD&#41;&#46; Recently&#44; some studies have demonstrated an association between dysbiosis and NAFLD&#59; however&#44; the exact mechanisms that lead to intestinal membrane damage&#44; bacterial translocation and inflammation are not well elucidated&#46; Due to the relevance of this theme&#44; the IM and its metabolites have received special attention in recent years in an attempt to better understand the mechanisms related to the prevention&#44; physiopathology&#44; and treatment of NAFLD&#46; In this paper&#44; we provide a review of the human IM and its role in diet&#44; obesity&#44; and the development&#47;progression of NAFLD&#47;NASH&#44; as well as the use of prebiotics and probiotics in the modulation of IM&#46;</p></span>"
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Possible mechanisms related to the intestinal microbiota that lead to energy imbalance and consequently obesity&#46;</p> <p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">FIAF&#44; fasting-induced adipose factor&#59; Gpr41&#47;43&#44; G-protein coupled receptor&#59; LPL&#44; lipoprotein lipase&#59; SCFAs&#44; short chain fatty acids&#59; AMPK&#44; AMP-activated protein kinase&#59; TRL5&#44; Toll-like receptor-5&#46;</p>"
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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">The role of the intestinal microbiota in the development of fatty liver&#46; Intestinal dysbiosis may be a determining factor for the development and progression of NAFLD&#47;NASH&#46; The increase in pathogenic bacteria and Gram-negative bacteria increases dietary energy extraction&#44; leading to increased intestinal permeability and bacterial translocation&#44; stimulating de novo fatty acid synthesis and increasing LPS expression&#44; as well as the expression of NF-k&#946; and TNF-&#945;&#46;</p> <p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">LPS&#44; lipopolysaccharides&#59; NF-k&#946;&#44; nuclear factor-kappa &#946;&#59; TNF-&#945;&#44; tumor necrosis factor-alpha&#46;</p>"
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Article information

ISSN: 16652681
Original language: English

DOI:10.1016/j.aohep.2019.04.006

The statistics are updated each day

Year/Month	Html	Pdf	Total

2024 November	18	1	19
2024 October	80	6	86
2024 September	118	7	125
2024 August	79	8	87
2024 July	115	17	132
2024 June	88	11	99
2024 May	83	9	92
2024 April	89	8	97
2024 March	94	15	109
2024 February	91	14	105
2024 January	139	29	168
2023 December	125	26	151
2023 November	150	22	172
2023 October	197	27	224
2023 September	79	10	89
2023 August	106	19	125
2023 July	97	15	112
2023 June	116	10	126
2023 May	177	23	200
2023 April	129	27	156
2023 March	115	13	128
2023 February	98	17	115
2023 January	79	13	92
2022 December	106	16	122
2022 November	76	19	95
2022 October	107	25	132
2022 September	115	29	144
2022 August	145	37	182
2022 July	100	13	113
2022 June	105	28	133
2022 May	180	39	219
2022 April	76	32	108
2022 March	93	26	119
2022 February	94	12	106
2022 January	92	19	111
2021 December	72	28	100
2021 November	73	17	90
2021 October	114	45	159
2021 September	70	22	92
2021 August	87	24	111
2021 July	62	25	87
2021 June	46	9	55
2021 May	83	19	102
2021 April	296	59	355
2021 March	209	57	266
2021 February	100	48	148
2021 January	114	41	155
2020 December	111	20	131
2020 November	97	31	128
2020 October	71	24	95
2020 September	71	34	105
2020 August	78	26	104
2020 July	43	21	64
2020 June	50	14	64
2020 May	125	28	153
2020 April	49	17	66
2020 March	55	35	90
2020 February	62	66	128
2020 January	47	13	60
2019 December	40	25	65
2019 November	47	33	80
2019 October	71	41	112
2019 September	58	21	79
2019 August	34	28	62
2019 July	31	34	65
2019 June	96	80	176
2019 May	112	107	219
2019 April	0	6	6

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