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Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease

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A special issue of Nutrients (ISSN 2072-6643). This special issue belongs to the section "Prebiotics and Probiotics".

Deadline for manuscript submissions: closed (25 May 2022) | Viewed by 50641

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Dr. Giulia Roda

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Guest Editor

IBD Center, Department of Gastroenterology, Humanitas Clinical and Research Center – IRCCS –, Rozzano, Italy
Interests: inflammatory bowel disease; bile acids; malabsorption; Crohn's disease; immune cells; diet; barrier function

Dr. Stefania Vetrano

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Guest Editor

IBD Center, Laboratory of Gastrointestinal Immunopathology, Humanitas Clinical and Research Center-IRCCS, Rozzano, 20089 Milan, Italy
Interests: inflammatory bowel disease; intestinal epithelial; cancer

Special Issue Information

Dear Colleagues,

Inflammatory bowel diseases (IBD), ulcerative colitis (UC), and Crohn's disease (CD), are progressive systematic chronic conditions which result from an overactive response of mucosal immune system to the food, environmental or infectious antigens in a genetically susceptible host. They are characterized by a deficient intestinal absorption and various symptoms, among which diarrhea represents an important target for treatment. Moreover, both the innate and cell‐mediated immunities are activated by the commensal enteric bacteria which play a crucial role in the progression and maintenance of IBD. Bile Acids (BAs) are endogenous acidic steroids synthetized in the liver from cholesterol with a pivotal role in lipid transport through enterohepatic circulation and as agonists of Farnesoid X receptor and TGR5. BAs are mainly reabsorbed in the terminal ileum through an active transport mechanism selective for their conjugates with glycine and taurine and inefficient for unconjugated BAs. The unabsorbed fraction undergoes deconjugation and 7-α-dihydroxylation in the colon by gut microbiota, allowing partial passive absorption and maintenance of the physiological pool size. Several studies have reported that intestinal inflammation alters the physiological concentration of bile acids. As a consequence, we assist with a non-physiological concentration of bile acids in peripheral blood, bile, and intestinal content. The pathogenic role of BAs in chronic IBD has long been debated. Several studies have evaluated BA metabolism in relation to hepatobiliary and intestinal diseases; these studies, however, are often limited in accurate selection of patient population, sample size and analytical methods, which are critical and limiting factors. BA malabsorption plays a major role in diarrhea, because luminal BAs result in colonic secretion of water and electrolytes and the induction of propagated contractions. BAs have been proposed as diagnostic or prognostic tools in IBD, but large studies to prove their utility are needed. Of note, microbiome components interact with luminal bile acids and the resulting metabolites might play an important role in maintaining the integrity of the barrier function.

It is believed that probiotics and possibly diet can induce changes in the intestinal microbiota and stabilize the beneficial microbial population. Moreover, the immunomodulatory properties of probiotics may be due to the bioactive compounds and secondary metabolites produced during the fermentation process or from their interaction with bile acids. Interaction between microbiome, probiotics, and bile acids has been poorly investigated.

In this Special Issue of Nutrients, we aim to achieve a better understanding of the role of BAs in inflammation, their interaction with the microbiome and how their alterations are involved in IBD, how we could incorporate them into clinical practice as diagnostic or prognostic tools and how probiotics\diet could orchestrate the interaction between bile acids and the microbiome and restore inflammation. We hope to achieve this through a series of manuscripts addressing the role of Bas and probiotics in health and inflammation, as well their interaction with the microbiota, and to understand how to use BAs as diagnostic or prognostic tools.

Dr. Giulia Roda
Dr. Stefania Vetrano
Guest Editors

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Keywords

bile acids
probiotics
diet
inflammation
malabsorption
inflammatory bowel diseases
Crohn’s disease
diet
immune cells
barrier function
gut microbiome

Published Papers (10 papers)

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Research

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22 pages, 4804 KiB

Open AccessArticle

Pomegranate Extract Affects Gut Biofilm Forming Bacteria and Promotes Intestinal Mucosal Healing Regulating the Crosstalk between Epithelial Cells and Intestinal Fibroblasts

by Giulia Rizzo, Samuel Elias Pineda Chavez, Elisa Vandenkoornhuyse, Cindy Lorena Cárdenas Rincón, Valeria Cento, Valentina Garlatti, Marek Wozny, Giusy Sammarco, Alessia Di Claudio, Lisa Meanti, Sudharshan Elangovan, Andrea Romano, Giulia Roda, Laura Loy, Arianna Dal Buono, Roberto Gabbiadini, Sara Lovisa, Roberto Rusconi, Alessandro Repici, Alessandro Armuzzi and Stefania Vetrano Show full author list Hide full author list

Nutrients 2023, 15(7), 1771; https://doi.org/10.3390/nu15071771 - 05 Apr 2023

Cited by 1 | Viewed by 6188

Abstract

Background: Pomegranate (Punica granatum) can be used to prepare a bioactive extract exerting anti-inflammatory activities. Clinical studies demonstrated an improvement in clinical response in inflammatory bowel disease (IBD) patients when pomegranate extract (PG) was taken as a complement to standard medications. However, the molecular mechanisms underlying its beneficial effects are still scarcely investigated. This study investigates the effect of PG on bacterial biofilm formation and the promotion of mucosal wound healing. Methods: The acute colitis model was induced in C57BL/6N mice by 3% dextran sodium sulfate administration in drinking water for 5 days. During the recovery phase of colitis, mice received saline or PG (200 mg/kg body weight) by oral gavage for 11 days. Colitis was scored daily by evaluating body weight loss, bleeding, and stool consistency. In vivo intestinal permeability was evaluated by fluorescein isothiocyanate-conjugated dextran assay, bacterial translocation was assessed by fluorescence in situ hybridization on tissues, whereas epithelial and mucus integrity were monitored by immunostaining for JAM-A and MUC-2 markers. Bacterial biofilm formation was assessed using microfluidic devices for 24 or 48 h. Primary fibroblasts were isolated from healthy and inflamed areas of 8 IBD patients, and Caco-2 cells were stimulated with or without PG (5 μg/mL). Inflammatory mediators were measured at the mRNA and protein level by RT-PCR, WB, or Bio-plex multiplex immunoassay, respectively. Results: In vivo, PG boosted the recovery phase of colitis, promoting a complete restoration of the intestinal barrier with the regeneration of the mucus layer, as also demonstrated by the absence of bacterial spread into the mucosa and the enrichment of crypt-associated fibroblasts. Microfluidic experiments did not highlight a specific effect of PG on Enterobacterales biofilm formation, even though Citrobacter freundii biofilm was slightly impaired in the presence of PG. In vitro, inflamed fibroblasts responded to PG by downregulating the release of metalloproteinases, IL-6, and IL-8 and upregulating the levels of HGF. Caco-2 cells cultured in a medium supplemented with PG increased the expression of SOX-9 and CD44, whereas in the presence of HGF or plated with a fibroblast-conditioned medium, they displayed a decrease in SOX-9 and CD44 expression and an increase in AXIN2, a negative regulator of Wnt signaling. Conclusions: These data provide new insight into the manifold effects of PG on promoting mucosal homeostasis in IBD by affecting pathogen biofilm formation and favoring the regeneration of the intestinal barrier through the regulation of the crosstalk between epithelial and stromal cells. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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19 pages, 4004 KiB

Open AccessArticle

Akkermansia muciniphila Colonization Alleviating High Fructose and Restraint Stress-Induced Jejunal Mucosal Barrier Disruption

by Jiayu Yu, Tianlong Liu, Zihao Gao, Runbang Liu, Zixu Wang, Yaoxing Chen, Jing Cao and Yulan Dong

Nutrients 2022, 14(15), 3164; https://doi.org/10.3390/nu14153164 - 30 Jul 2022

Cited by 6 | Viewed by 2359

Abstract

Akkermansia muciniphila (A. muciniphila) is a mucin-degrading bacterium that resides in the mucus layer, but its potential in intestinal inflammatory diseases has sparked controversy. It is well known that both the consumption of fructose-containing beverages and psychological stress increase the risk of intestinal disease. Our results revealed that a high-fructose diet aggravated the damage to the jejunal mucosal barrier caused by restraint stress, reduced tight junction protein expression and the intestinal digestion and absorption capacity, disrupted the ability of Paneth cells to secrete antimicrobial peptides, and promoted the expression of inflammatory cytokines. A. muciniphila colonization enhanced the defense function of the mucosal barrier by enhancing the function of the NLRP6, promoting autophagy, maintaining the normal secretion of antimicrobial peptides in Paneth cells, promoting the expression of tight junction proteins, negatively regulating the NF-kB signaling pathway and inhibiting the expression of inflammatory cytokines. Our work indicates that A. muciniphila ameliorates the disruption of the intestinal mucosal barrier under high fructose and restraint stress. These results provided a rationale for the development of probiotic colonization for the prevention or treatment of intestinal diseases. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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16 pages, 4386 KiB

Open AccessArticle

Protective Effect of Probiotics Isolated from Traditional Fermented Tea Leaves (Miang) from Northern Thailand and Role of Synbiotics in Ameliorating Experimental Ulcerative Colitis in Mice

by Napapan Kangwan, Sarawut Kongkarnka, Nitsara Boonkerd, Kridsada Unban, Kalidas Shetty and Chartchai Khanongnuch

Nutrients 2022, 14(1), 227; https://doi.org/10.3390/nu14010227 - 05 Jan 2022

Cited by 11 | Viewed by 3247

Abstract

This study aimed to investigate the protective effect of probiotics and synbiotics from traditional Thai fermented tea leaves (Miang) on dextran sulfate sodium (DSS)-induced colitis in mice, in comparison to sulfasalazine. C57BL/6 mice were treated with probiotics L. pentosus A14-6, CMY46 and synbiotics, L. pentosus A14-6 combined with XOS, and L. pentosus CMY46 combined with GOS for 21 days. Colitis was induced with 2% DSS administration for seven days during the last seven days of the experimental period. The positive group was treated with sulfasalazine. At the end of the experiment, clinical symptoms, pathohistological changes, intestinal barrier integrity, and inflammatory markers were analyzed. The probiotics and synbiotics from Miang ameliorated DSS-induced colitis by protecting body weight loss, decreasing disease activity index, restoring the colon length, and reducing pathohistological damages. Furthermore, treatment with probiotics and synbiotics improved intestinal barrier integrity, accompanied by lowing colonic and systemic inflammation. In addition, synbiotics CMY46 combined with GOS remarkedly elevated the expression of IL-10. These results suggested that synbiotics isolated from Miang had more effectiveness than sulfasalazine. Thereby, they could represent a novel potential natural agent against colonic inflammation. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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Review

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20 pages, 793 KiB

Open AccessReview

Bile Salt Hydrolase-Competent Probiotics in the Management of IBD: Unlocking the “Bile Acid Code”

by Raffaella Maria Gadaleta, Marica Cariello, Lucilla Crudele and Antonio Moschetta

Nutrients 2022, 14(15), 3212; https://doi.org/10.3390/nu14153212 - 05 Aug 2022

Cited by 16 | Viewed by 3753

Abstract

Bile acid (BA) species and the gut microbiota (GM) contribute to intestinal mucosa homeostasis. BAs shape the GM and, conversely, intestinal bacteria with bile salt hydrolase (BSH) activity modulate the BA pool composition. The mutual interaction between BAs and intestinal microorganisms also influences mucosal barrier integrity, which is important for inflammatory bowel disease (IBD) pathogenesis, prevention and therapy. High levels of secondary BAs are detrimental for the intestinal barrier and increase the intestinal inflammatory response and dysbiosis. Additionally, a lack of BSH-active bacteria plays a role in intestinal inflammation and BA dysmetabolism. Thus, BSH-competent bacteria in probiotic formulations are being actively studied in IBD. At the same time, studies exploring the modulation of the master regulator of BA homeostasis, the Farnesoid X Receptor (FXR), in intestinal inflammation and how this impacts the GM are gaining significant momentum. Overall, the choice of probiotic supplementation should be a peculiar issue of personalized medicine, considering not only the disease but also the specific BA and metabolic signatures of a given patient. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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28 pages, 2113 KiB

Open AccessReview

New Insights into Bile Acids Related Signaling Pathways in the Onset of Colorectal Cancer

by Cristiana Caliceti, Angela Punzo, Alessia Silla, Patrizia Simoni, Giulia Roda and Silvana Hrelia

Nutrients 2022, 14(14), 2964; https://doi.org/10.3390/nu14142964 - 20 Jul 2022

Cited by 14 | Viewed by 2959

Abstract

Colorectal cancer (CRC) ranks as the second among the causes of tumor death worldwide, with an estimation of 1.9 million new cases in 2020 and more than 900,000 deaths. This rate might increase by 60% over the next 10 years. These data are unacceptable considering that CRC could be successfully treated if diagnosed in the early stages. A high-fat diet promotes the hepatic synthesis of bile acids (BAs) increasing their delivery to the colonic lumen and numerous scientific reports correlate BAs, especially secondary BAs, with CRC incidence. We reviewed the physicochemical and biological characteristics of BAs, focusing on the major pathways involved in CRC risk and progression. We specifically pointed out the role of BAs as signaling molecules and the tangled relationships among their nuclear and membrane receptors with the big bang of molecular and cellular events that trigger CRC occurrence. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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19 pages, 1144 KiB

Open AccessEditor’s ChoiceReview

by Federica Di Vincenzo, Pierluigi Puca, Loris Riccardo Lopetuso, Valentina Petito, Letizia Masi, Bianca Bartocci, Marco Murgiano, Margherita De Felice, Lorenzo Petronio, Antonio Gasbarrini and Franco Scaldaferri

Nutrients 2022, 14(13), 2664; https://doi.org/10.3390/nu14132664 - 27 Jun 2022

Cited by 16 | Viewed by 4223

Abstract

Inflammatory bowel diseases (IBD) and microscopic colitis are chronic immune-mediated inflammatory disorders that affect the gastroenterological tract and arise from a complex interaction between the host’s genetic risk factors, environmental factors, and gut microbiota dysbiosis. The precise mechanistic pathways interlinking the intestinal mucosa homeostasis, the immunological tolerance, and the gut microbiota are still crucial topics for research. We decided to deeply analyze the role of bile acids in these complex interactions and their metabolism in the modulation of gut microbiota, and thus intestinal mucosa inflammation. Recent metabolomics studies revealed a significant defect in bile acid metabolism in IBD patients, with an increase in primary bile acids and a reduction in secondary bile acids. In this review, we explore the evidence linking bile acid metabolites with the immunological pathways involved in IBD pathogenesis, including apoptosis and inflammasome activation. Furthermore, we summarize the principal etiopathogenetic mechanisms of different types of bile acid-induced diarrhea (BAD) and its main novel diagnostic approaches. Finally, we discuss the role of bile acid in current and possible future state-of-the-art therapeutic strategies for both IBD and BAD. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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15 pages, 583 KiB

Open AccessReview

Ileal Pouch–Anal Anastomosis and Pouchitis: The Role of the Microbiota in the Pathogenesis and Therapy

by Roberto Gabbiadini, Arianna Dal Buono, Carmen Correale, Antonino Spinelli, Alessandro Repici, Alessandro Armuzzi and Giulia Roda

Nutrients 2022, 14(13), 2610; https://doi.org/10.3390/nu14132610 - 24 Jun 2022

Cited by 4 | Viewed by 3552

Abstract

Inflammatory bowel diseases, Crohn’s disease and ulcerative colitis, are life-long disorders characterized by the chronic relapsing inflammation of the gastrointestinal tract with the intermittent need for escalation treatment and, eventually, even surgery. The total proctocolectomy with ileal pouch–anal anastomosis (IPAA) is the surgical intervention of choice in subjects affected by ulcerative colitis (UC). Although IPAA provides satisfactory functional outcomes, it can be susceptible to some complications, including pouchitis as the most common. Furthermore, 10–20% of the pouchitis may develop into chronic pouchitis. The etiology of pouchitis is mostly unclear. However, the efficacy of antibiotics in pouchitis suggests that the dysbiosis of the IPAA microbiota plays an important role in its pathogenesis. We aimed to review the role of the microbiota in the pathogenesis and as a target therapy in subjects who develop pouchitis after undergoing the surgical intervention of total proctocolectomy with IPAA reconstruction. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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15 pages, 447 KiB

Open AccessReview

Inflammatory Bowel Disease and Reproductive Health: From Fertility to Pregnancy—A Narrative Review

by Camilla Ronchetti, Federico Cirillo, Noemi Di Segni, Martina Cristodoro, Andrea Busnelli and Paolo Emanuele Levi-Setti

Nutrients 2022, 14(8), 1591; https://doi.org/10.3390/nu14081591 - 12 Apr 2022

Cited by 6 | Viewed by 4148

Abstract

Despite the fact that knowledge on obstetrical management of Inflammatory Bowel Diseases (IBDs) has greatly improved over the years, many patients still actively avoid pregnancy for fear of adverse maternal or neonatal outcomes, of adverse effects of pregnancy on the disease activity, of eventual IBD inheritance, or of an increased risk of congenital malformations. Indeed, though data prove that fertility is hardly affected by the disease, a reduced birth rate is nevertheless observed in patients with IBD. Misconceptions on the safety of drugs during gestation and breastfeeding may influence patient choice and negatively affect their serenity during pregnancy or lactation. Moreover, physicians often showed concerns about starting IBD medications before and during pregnancy and did not feel adequately trained on the safety of IBD therapies. IBD-expert gastroenterologists and gynecologists should discuss pregnancy and breastfeeding issues with patients when starting or changing medications in order to provide appropriate information; therefore, pre-conception counselling on an individualized basis should be mandatory for all patients of reproductive age to reassure them that maintaining disease remission and balancing the eventual obstetrical risks is possible. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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23 pages, 1301 KiB

Open AccessReview

Bile Acid–Gut Microbiota Axis in Inflammatory Bowel Disease: From Bench to Bedside

by Min Yang, Yu Gu, Lingfeng Li, Tianyu Liu, Xueli Song, Yue Sun, Xiaocang Cao, Bangmao Wang, Kui Jiang and Hailong Cao

Nutrients 2021, 13(9), 3143; https://doi.org/10.3390/nu13093143 - 09 Sep 2021

Cited by 66 | Viewed by 11866

Abstract

Inflammatory bowel disease (IBD) is a chronic, relapsing inflammatory disorder of the gastrointestinal tract, with increasing prevalence, and its pathogenesis remains unclear. Accumulating evidence suggested that gut microbiota and bile acids play pivotal roles in intestinal homeostasis and inflammation. Patients with IBD exhibit decreased microbial diversity and abnormal microbial composition marked by the depletion of phylum Firmicutes (including bacteria involved in bile acid metabolism) and the enrichment of phylum Proteobacteria. Dysbiosis leads to blocked bile acid transformation. Thus, the concentration of primary and conjugated bile acids is elevated at the expense of secondary bile acids in IBD. In turn, bile acids could modulate the microbial community. Gut dysbiosis and disturbed bile acids impair the gut barrier and immunity. Several therapies, such as diets, probiotics, prebiotics, engineered bacteria, fecal microbiota transplantation and ursodeoxycholic acid, may alleviate IBD by restoring gut microbiota and bile acids. Thus, the bile acid–gut microbiota axis is closely connected with IBD pathogenesis. Regulation of this axis may be a novel option for treating IBD. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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24 pages, 1169 KiB

Open AccessReview

Bariatric Surgery and Liver Disease: General Considerations and Role of the Gut–Liver Axis

by Maria Cerreto, Francesco Santopaolo, Antonio Gasbarrini, Maurizio Pompili and Francesca Romana Ponziani

Nutrients 2021, 13(8), 2649; https://doi.org/10.3390/nu13082649 - 30 Jul 2021

Cited by 23 | Viewed by 6773

Abstract

Weight loss is a therapeutic solution for many metabolic disorders, such as obesity and its complications. Bariatric surgery aims to achieve lasting weight loss in all patients who have failed after multiple dietary attempts. Among its many benefits, it has been associated with the regression of non-alcoholic fatty liver disease (NAFLD), which is often associated with obesity, with evidence of substantial improvement in tissue inflammation and fibrosis. These benefits are mediated not only by weight loss, but also by favorable changes in systemic inflammation and in the composition of the gut microbiota. Changes in microbial metabolites such as short-chain fatty acids (SCFAs), capable of acting as endocrine mediators, and bile acids (BAs) as well as modifications of the gut-brain axis, are among the involved mechanisms. However, not all bariatric surgeries show beneficial effects on the liver; those leading to malabsorption can cause liver failure or a marked worsening of fibrosis and the development of cirrhosis. Nevertheless, there are still many unclear aspects, including the extent of the benefits and the magnitude of the risks of bariatric surgery in cirrhotic patients. In addition, the usefulness and the safety of these procedures in patients who are candidates to or who have undergone liver transplant need solid supporting evidence. This paper aims to review literature data on the use of bariatric surgery in the setting of chronic liver disease. Full article

(This article belongs to the Special Issue Bile Acids and Probiotics in Regulation of Intestinal Function in Health and Inflammatory Bowel Disease)

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