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Intestinal Permeability in Physiological and Pathological Conditions: Major Determinants and Assessment Modalities

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Intestinal Permeability in Physiological and Pathological Conditions: Major Determinants and Assessment Modalities European Review for Medical and Pharmacological Sciences 2019; 23: 795-810 Intestinal permeability in physiological and pathological conditions: major determinants and assessment modalities C. GRAZIANI1, C. TALOCCO2, R. DE SIRE2, V. PETITO2, L.R. LOPETUSO2, J. GERVASONI3, S. PERSICHILLI3, F. FRANCESCHI4, V. OJETTI, A. GASBARRINI1,2, F. SCALDAFERRI1,2 1Area Gastroenterologia ed Oncologia Medica, Dipartimento di Scienze Gastroenterologiche, Endocrino- Metaboliche e Nefro-Urologiche, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy 2Istituto di Patologia Speciale Medica, Università Cattolica del Sacro Cuore, Rome, Italy 3Area Diagnostica di Laboratorio, Dipartimento di Scienze di Laboratorio e Infettivologiche, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy 4Area Medicina dell’Urgenza e Pronto Soccorso, Dipartimento Scienze dell’Emergenza, Anestesiologiche e della Rianimazione, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy 5Istituto di Medicina Interna e Geriatria, Università Cattolica del Sacro Cuore, Rome, Italy Cristina Graziani and Claudia Talocco are equal contributors; Antonio Gasbarrini and F. Scaldaferri are equal contributors Abstract: Intestinal permeability is the proper- ganisms1. This condition requires a complex defen- ty that allows solute and fluid exchange between sive system that separates intestinal content from intestinal lumen and intestinal mucosa. Many fac- the host tissues, and regulates nutrients adsorption, tors could have major impact on its regulation, in- allowing interactions between the resident micro- cluding gut microbiota, mucus layer, epithelial cell integrity, epithelial junction, immune responses, biota and intestinal immune system, ruling intes- intestinal vasculature, and intestinal motility. Any tinal translocation of bacterial compounds from change among these factors could have an impact external to the internal world: this is the functional on intestinal homeostasis and gut permeability. unit called “Gut Barrier”, which is composed by Healthy condition is associated to normal intes- the epithelial/intestinal mucosal barrier, the Gut tinal permeability whereas several intestinal and Microbiota, the intestinal mucus layers, the innate extra intestinal disease, like inflammatory bowel disease, irritable bowel syndrome, non-alcoholic and adaptive immune system associated to gut fatty liver disease among others, are associated mucosa, the intestinal vascular/lymphatic system, to increased intestinal permeability. the intestinal endocrine and neuroenteric system, This review aims to synthesize determinants the enzymatic system2 (Figure 1). on intestinal permeability and to report method- The outer layer is composed by gut microbiota ologies useful to the measurement of intestinal that competes with pathogens for space and resourc- permeability in clinical practice as well as in re- es, elaborates molecules required for mucosal in- search settings. tegrity, and modulates the immunological patterns Key Words of lower barrier. Intestinal microbiota refers to the Intestinal permeability, Microbiota, Gut barrier, Mu- entire population of microorganisms colonizing the cosal immunology, Barrier protector, Ibd, Lactulose/ 3 mannitol ratio, Cr51edta, Leaky gut. gastrointestinal tract , displaying great biodiver- sity4. It includes not just bacteria, but also fungi, archaea, yeast and viruses, that have a mutualistic relationship with bacteria, within themselves and Introduction with their host, co-habiting with enterocytes in a symbiotic relationship3. Bacteria up to know are The gastrointestinal (GI) tract accounts for a the most studied and characterized: the majority global surface of more than 200-meter square, be- of them belongs to two main phyla, Bacteroidetes ing perhaps the most exposed system to the outside and Firmicutes followed by Proteobacteria, Acti- world of our body, comprehending thousands of nobacteria and Fusobacteria4. Its qualitative and compounds from foods and associated microor- quantitative composition varies according to the Corresponding Author: Franco Scaldaferri, MD; e-mail: [email protected] 795 C. Graziani, C. Talocco, R. De Sire, V. Petito, L.R. Lopetuso et al. Figure 1. Components of the gut barrier, A functional unit composed by the epithelial/intes- tinal mucosal barrier, the Gut Microbiota, the intestinal mucus layers, the innate and adaptive immune system associated to gut mucosa, the intestinal vascular/lymphatic system, the intesti- nal endocrin and neuroenteric system, the enzymatic system. age, host genetics, diet and the local environment, Gut microbiota is in close contact with another like pH and oxygen content3,4. simple mechanism of antimicrobial protection: Gut microbiota displays different functions, the intestinal mucus, the first physical barrier that including metabolic, immunological and gut bacteria meet in the intestinal tract. It separates protection in the regulation of barrier function, the endoluminal contents from inner layer of the metabolism of nutrients, trophic function of the gut barrier and contains antimicrobial products mucosa, drug metabolism, and toxin metabolism. and secretory IgA. The goblet cells produce fac- It assists in the digestion of energy substrates, in tors like trefoil-factor and the resistin-like mol- producing vitamins and hormones and in pro- ecule-β that can stabilize mucin polymers and tecting the host from pathogen species2. Gut thereby maintain barrier integrity3. The mucus microbiota is a key element in balancing innate is composed of two layers: an inner layer firmly and adaptive immune systems within the gut3. attached to the epithelial cells, which is imper- 796 Intestinal permeability in physiological and pathological conditions vious to bacteria and functions as a protective zonula occludens proteins, which in turn anchor barrier for the epithelial cell surface, and an outer the transmembrane proteins to the actin cyto- layer that is less sticky. Both layers are organized skeleton. The interaction of Tight Junction pro- around the highly glycosylated mucin MUC2, teins with the actin cytoskeleton contributes to which forms an amorphous polymer-like cover barrier integrity8. In this setting, gut microbiota and is secreted by goblet cells5. plays a crucial role in physiologic conditions3,4, The inner layer consists of a complex network being a positive stimulus. Nutrients also play of other human cells. The epithelial/intestinal mu- an important role. Dietary components, such as cosa barrier is composed by epithelial cells (en- omega-6 polyunsaturated fatty acids (v6-PUFAs), terocytes), covering the entire intestinal surface long-chain saturated fatty acids, protein, and organized in villi and circular folds2. Enterocytes digestible carbohydrates, are associated to in- display on the apical surface microvilli or brush testinal inflammation and increased intestinal border, site of several intestinal enzymes. The permeability. In contrast, omega-3 polyunsatu- junction among enterocytes is ruled by adherens rated fatty acids (v3-PUFAs), vitamin D, medium junctions (AJs) and tight junctions (TJs), includ- chain triglycerides, bioactive food-derived pep- ing cadherins, claudins, occludin, and junctional tides, some probiotics and prebiotics and non-di- adhesion molecules (JAM) proteins, intercellular gestible carbohydrates were described to reduce proteins making bridges among cells and which intestinal permeability and improve intestinal seal adjacent cells together, making them a phisi- health. SCFAs produced from butyrate fermenta- cal barrier not permeable to bacteria or other tion, when administered orally to animal models substances. TJ is dynamic gates, whose function of IBD, protect against mucus layer alterations9. is regulated by several factors, including alcohol, Other factors are also associated to a physiologic food components, bacterial products, inflamma- modification of gut barrier, however they are not tory molecules and drugs2. considered in the present review. Immune cells of the intestinal mucosa are organized in a specialized and compartmental- Pathological Regulators ized system known as “gut-associated lymphoid of Intestinal Permeability tissue” or GALT. It is one of the largest lymphoid Intestinal permeability can be altered by cyto- organs, which determine the immune responses to kine-mediated dysfunction, resulting in immune pathogenic microorganisms and immune tolerance activation and tissue inflammation. In particular, to commensal bacteria. This ability is mediated IFN-γ, increases paracellular permeability in in- by dendritic cells and M-cells in Peyer’s patches. testinal epithelial cells through the redistribution These cells are able to internalize microorganisms and expression of Tight Junction proteins and the and macromolecules, presenting the antigens to rearrangement of the actin cytoskeleton. Other naive T lymphocytes, which differentiate and are powerful and pro-inflammatory cytokines were responsible for immune responses, including the associated to Tight Junction impairment through production of several types of cytokines2,6. several mechanisms: TNF-α, by inducing apop- tosis of intestinal epithelial cells, IL-1β, among Physiological Regulators others. Interleukin-10 (IL-10), a well-defined an- of Intestinal Permeability ti-inflammatory cytokine, has, on the other hand, The homeostasis of the intestinal epitheli- protective effect on Tigh Junction in vitro as well um and the regulation of intestinal
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