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Microscopic Colitis—Microbiome, Barrier Function and Associated Diseases

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Microscopic Colitis—Microbiome, Barrier Function and Associated Diseases Review Article Page 1 of 10 Microscopic colitis—microbiome, barrier function and associated diseases Saskia van Hemert1, Karolina Skonieczna-Żydecka2, Igor Loniewski2,3, Piotr Szredzki4, Wojciech Marlicz5 1Winclove Probiotics, Amsterdam, the Netherlands; 2Department of Biochemistry and Human Nutrition, Pomeranian Medical University, Szczecin, Poland; 3Sanprobi Sp. z o.o. Sp. K., Szczecin, Poland; 4Endoscopy Unit, Department of Surgery, Hospital Sędziszów Małopolski, Sędziszów Małopolski, Poland; 5Department of Gastroenterology, Pomeranian Medical University, Szczecin, Poland Contributions: (I) Conception and design: S van Hemert, W Marlicz; (II) Administrative support: None; (III) Provision of study materials or patients: K Żydecka-Skonieczna, I Loniewski; (IV) Collection and assembly of data: S van Hemert, K Żydecka-Skonieczna, W Marlicz; (V) Data analysis and interpretation: All authors; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors. Correspondence to: Wojciech Marlicz, MD, PhD, FACG. Department of Gastroenterology, Pomeranian Medical University, Unii Lubelskiej 1, 71-252 Szczecin, Poland. Email: [email protected]. Abstract: Microscopic colitis (MC) is a chronic inflammatory bowel disease (IBD) with little in terms of endoscopic abnormalities and is frequently associated with other autoimmune diseases. The peak incidence of the disease is in middle aged or older populations, mostly females. The pathogenesis of MC is complex, multifactorial and poorly understood. Current concepts revolve around innate immunity or microbiome alterations as well as gut barrier dysfunction, all of which lead to the development of subtle inflammatory lesions in gut mucosa. The results of numerous basic and clinical studies involving molecular techniques as well as advanced endoscopic imaging revealed the important role of both intrinsic (e.g., hormonal) as well as extrinsic (e.g., NSAIDs and PPIs) factors in the modulation of gastrointestinal microbiome and MC pathogenesis. Capsule endoscopy as well confocal endomicroscopy imaging, alongside standard endoscopic techniques offer new tools in the evaluation of MC patients and allow their better stratification for novel treatment protocols based on modulation of gut microbiome and barrier function. Keywords: Autoimmune diseases; intestinal and gut barrier; microscopic colitis (MC); microbiome; probiotics; super magnifying endoscopy; high definition endoscopy Submitted Mar 06, 2017. Accepted for publication Mar 15, 2017. doi: 10.21037/atm.2017.03.83 View this article at: http://dx.doi.org/10.21037/atm.2017.03.83 Introduction incidence of other IBDs, such as ulcerative colitis (UC) or Crohn’s disease (CD) (7,8). Of note, MC has been regarded Microscopic colitis (MC) is a chronic inflammatory bowel as a subgroup within IBD (8). disease (IBD) with few or no endoscopic abnormalities The two main subtypes of MC are lymphocytic colitis (1-3). Patients with MC present chronic, non-bloody watery (LC) and collagenous colitis (CC) (9). Epithelial damage diarrhoea, however some may suffer from constipation, and inflammation in the lamina propria, mainly with abdominal pain or even remain symptom free (4,5). Patients mononuclear cells, are observed in both diseases. In LC, the with MC are more often middle aged or older women in intraepithelial lymphocyte (IEL) count is ≥20/100 epithelial their seventh decade of life. According to several reports (6) cells and the sub-epithelial collagen layer <10 μm thick. there is steady increase in MC incidence, currently around In CC, the IEL count may be increased, but a thickening 10 cases per 100,000 person years, almost comparable to the of the sub-epithelial collagen layer ≥10 μm is necessary © Annals of Translational Medicine. All rights reserved. atm.amegroups.com Ann Transl Med 2017 Page 2 of 10 van Hemert et al. Microscopic colitis and microbiome for the diagnosis. It has been suggested that both subtypes Etiopathology of MC could be considered as histological subtypes of the same The pathophysiological cause of MC is unknown, but disease, and that in clinical trials, all MC patients could be recent hypotheses revolve around mucosal inflammation, included (10). Most recently, the type of MC incomplete microbiome and gut barrier alterations. Several extrinsic (MCi) with histopathological changes that are not fulfilling (environmental) as well as intrinsic (endocrine) factors the classic MC criteria has also been described in patients might play a role in the pathogenesis of the disease. with chronic diarrhoea and normal or close to normal endoscopic findings (1,11). The differential diagnosis between the complete and incomplete MC types remains Epithelial stress and mucosal inflammation the pathologist’s challanege and impacts on decision making Multiple studies have investigated different mechanisms in clinical practice (12). that might be involved in the development of mucosal MC has significant impact on the health-related quality inflammation in MC. An increase in the number of T-IELs of life of the patients affected (13). The main aim of suggests a specific mucosal immune response to luminal medical therapy is to improve the quality of life and achieve factors in predisposed individuals. Infiltration of CD8+ clinical remission. In patients with recurrent disease, MC T lymphocytes has been found in the epithelium of both recurrence prevention is desirable. The recommended LC and CC patients, whereas the amount of CD4+ T cells primary treatment of MC is with the glucocorticoid seems to be reduced in the epithelium (19). In the lamina budesonide (9,14). Antidiarrhoeals or colestyramine only propria, most T lymphocytes seem to be CD4+ (20). Both can be considered in MC patients with milder symptoms. CD4 and CD8 T cells of MC patients seem to be less active In case of relapse, budesonide can be used again either as compared to controls (21). Eosinophils also play a role intermittent or as low-dose continuous therapy. In patients in MC. Increased levels of luminal levels of eosinophilic with mild symptoms who do not respond to budesonide, cationic protein (CP) and an increased number of activated alterative drugs are recommended, such as colestyramine, eosinophils in the colonic mucosa have been found in aminosalicylates or bismuth (9). In some patients MC could patients with CC (21,22). be triggered by the use of certain medications, in particular Biopsies of sigmoid colon from patients with CC, non-steroidal anti-inflammatory drugs (NSAIDs), aspirin, incubated for 48 h in Roswell Park Memorial Institute proton pump inhibitors (PPIs), anti-diabetic drugs, and/or (RPMI) medium, produced increased levels of IFN-γ, antidepressants (15-17). In these cases discontinuation of TNA-α and IL-1 compared to controls (23). Levels of IL-8 the medication is the easiest; however not always sufficient and IL-13 did not differ between the groups. Other studies solution to treat the MC. Although the primary response have confirmed the presence of a pro-inflammatory cytokine to budesonide is often good, with response rate of around profiles in biopsies of MC patients (Figure 1) (24-26). 80% (14), relapses occur often (60–80%) when the Although these studies give an idea of the different treatment is stopped (9,18). Besides the relapses, patients mechanisms that may be involved in the development of the in remission can still suffer from persisting symptoms such mucosal inflammation in MC, the pathophysiological role as abdominal pain, fatigue, arthralgia or myalgia several of these findings is still unclear. years after diagnosis (9). The use of anti-TNF-alpha monoclonal antibodies (MoAb) (infliximab, adalimumab) MC and barrier dysfunction or biosimilars is reserved for the induction of remission in severe cases of MC that fail to respond to corticosteroids or The gut barrier is a complex, multicomponent system in immunomodulators, as an alternative to colectomy (12). which different cell types in and around the gut wall work MC has been linked to mucosal inflammation, together to prevent unwanted translocation of components autoimmune diseases and gut microbiota composition, all of from the lumen of the gut into the body. Perturbations which are also linked to gut barrier function. In this review in the gut barrier function can be due to poor nutrition, we would like to summarize the current research to MC infection or other illnesses. This can lead to increased in these fields, and to explore the possible roles gut barrier intestinal permeability, the rate of flux of molecules across function or microbiota might play in the occurrence and/or the epithelium (27). Increased intestinal permeability is treatment of MC. associated with a variety of gastrointestinal (GI) disorders, © Annals of Translational Medicine. All rights reserved. atm.amegroups.com Ann Transl Med 2017 Annals of Translational Medicine, 2017 Page 3 of 10 Paneth cell Enterocyte Tight junctions Adherens junctions GAP junctions Mucosal inflammation Antigens Antimicrobial peptides Mucins Epithelium: ↑ IL-6, IL-1 TH1 cells: ↑ INF-γ Dendritic cells: ↑ IL-12, IL-23 T-bet+ innate lymphoid cells: ↑ INF-γ sIgA Macrophages: ↑ TNF-α, IL-12 TH17 cells: ↑ IL-17A Bacteria B cells: ↑ IgG specific to commensals Figure 1 Simplified scheme representing immune alterations during mucosal inflammation. including IBD, irritable bowel syndrome and celiac in anti-inflammatory and epithelial barrier-enhancing disease (28). Mucosal barrier dysfunction has also been properties in animal models
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