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• W1992600007 abstract "The role of gut microflora and their interaction with host immune response in the development of Crohn's disease (CD) is an area of intense research interest. D'Haens et al1D'Haens G.R. Geboes K. Peeters M. et al.Early lesions of recurrent Crohn's disease caused by infusion of intestinal contents in excluded ileum.Gastroenterology. 1998; 114: 262-267Abstract Full Text Full Text PDF PubMed Scopus (723) Google Scholar have characterized the importance of the fecal stream in the development of recurrence after resection in patients with CD. Prior studies had already demonstrated that metronidazole reduced both endoscopic and clinical recurrence after ileocecal resection in CD, suggesting that bacteria were the primary factor in the fecal stream driving CD in this setting.2Rutgeerts P. Hiele M. Geboes K. et al.Controlled trial of metronidazole treatment for prevention of Crohn's recurrence after ileal resection.Gastroenterology. 1995; 108: 1617-1621Abstract Full Text PDF PubMed Scopus (700) Google Scholar Furthermore, several serologic markers highlighting host immune responses to gut microflora have been identified in patients with CD as well as in specific CD phenotypes. Anti–Saccharomyces cerevisiae antibodies (immunoglobulin A and immunoglobulin G), antibodies to Escherichia coli outer membrane porin-C (Omp-C) and to clostridial flagellin (Cbir-1), and I2 antibody (novel homologue of the bacterial transcription-factor families) have been associated with small bowel disease location, fibrostenosis, perforating disease behavior, and small bowel surgery.3Targan S.R. Landers C.J. Yang H. et al.Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease.Gastroenterology. 2005; 128: 2020-2028Abstract Full Text Full Text PDF PubMed Scopus (386) Google Scholar, 4Mow W.S. Vasiliauskas E.A. Lin Y.C. et al.Association of antibody responses to microbial antigens and complications of small bowel Crohn's disease.Gastroenterology. 2004; 126: 414-424Abstract Full Text Full Text PDF PubMed Scopus (445) Google Scholar Higher titers to these serologic markers have been associated with higher odds of complicated disease behavior and need for surgery.5Dubinsky M.C. Kugathasan S. Mei L. et al.Increased immune reactivity predicts aggressive complicating Crohn's disease in children.Clin Gastroenterol Hepatol. 2008; 6: 1105-1111Abstract Full Text Full Text PDF PubMed Scopus (211) Google Scholar By using RNA ribosomal sequencing, fluorescence in situ hybridization, DNA microarrays, gene chips and metagenomic DNA analyses, unique qualitative and quantitative differences in gut microflora diversity have been identified in patients with CD.6Manichanh C. Rigottier-Gois L. Bonnaud E. et al.Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach.Gut. 2006; 55: 205-211Crossref PubMed Scopus (1557) Google Scholar, 7Kang S. Denman S.E. Morrison M. et al.Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray.Inflamm Bowel Dis. 2010; 16: 2034-2042Crossref PubMed Scopus (267) Google Scholar Further insight into the role of bacteria in CD can be expected as a result of the National Institutes of Health–sponsored Human Microbiome project. Because of the compelling evidence that the microbiota in patients with CD contributes to the pathogenesis of disease, it follows that strategic therapies aiming to restore a healthy balance of flora, such as antibiotics and probiotics, may offer an effective method of treating CD.8Shanahan F. Dinan T.G. Ross P. et al.Probiotics in transition.Clin Gastroenterol Hepatol. 2012; 10: 1220-1224Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar, 9Ciorba M.A. A gastroenterologist's guide to probiotics.Clin Gastroenterol Hepatol. 2012; 10: 960-968Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar Furthermore, use of probiotics is likely to be associated with a reduced side effect profile, potentially avoiding rare but serious side effects associated with immunosuppressant and biological therapies. In addition to their role in prevention of postoperative recurrence,2Rutgeerts P. Hiele M. Geboes K. et al.Controlled trial of metronidazole treatment for prevention of Crohn's recurrence after ileal resection.Gastroenterology. 1995; 108: 1617-1621Abstract Full Text PDF PubMed Scopus (700) Google Scholar antibiotics are an effective therapy for the treatment of perianal CD, active CD, and pouchitis.10Thia K.T. Mahadevan U. Feagan B.G. et al.Ciprofloxacin or metronidazole for the treatment of perianal fistulas in patients with Crohn's disease: a randomized, double-blind, placebo-controlled pilot study.Inflamm Bowel Dis. 2009; 15: 17-24Crossref PubMed Scopus (190) Google Scholar, 11Madden M.V. McIntyre A.S. Nicholls R.J. Double-blind crossover trial of metronidazole versus placebo in chronic unremitting pouchitis.Dig Dis Sci. 1994; 39: 1193-1196Crossref PubMed Scopus (255) Google Scholar, 12Prantera C. Lochs H. Grimaldi M. et al.Rifaximin-extended intestinal release induces remission in patients with moderately active Crohn's disease.Gastroenterology. 2012; 142: 473-481Abstract Full Text Full Text PDF PubMed Scopus (142) Google Scholar There has also been evidence to suggest that probiotics may be beneficial in the treatment of CD. A pilot study published in 1993 demonstrated that Saccharomyces boulardii treatment was associated with a reduction in bowel movement frequency compared with placebo in CD patients with mild residual symptoms.13Plein K. Hotz J. Therapeutic effects of Saccharomyces boulardii on mild residual symptoms in a stable phase of Crohn's disease with special respect to chronic diarrhea: a pilot study.Z Gastroenterol. 1993; 31: 129-134PubMed Google Scholar In 2000, Guslandi et al14Guslandi M. Mezzi G. Sorghi M. et al.Saccharomyces boulardii in maintenance treatment of Crohn's disease.Dig Dis Sci. 2000; 45: 1462-1464Crossref PubMed Scopus (597) Google Scholar assessed the effect of S boulardii in maintenance of remission in CD. Thirty-two patients with a confirmed diagnosis of CD in remission were randomized to receive either 3 g mesalamine daily or 1 g S boulardii daily in combination with 2 g mesalamine daily. At 6 months, 6 of 16 patients in the mesalamine group developed relapse, compared with 1 patient relapse in the S boulardii group (P = .004). However, several meta-analyses performed to assess the effectiveness of probiotics, including S boulardii, have failed to demonstrate a beneficial effect in maintenance of remission or prevention of postoperative recurrence in CD.15Rolfe V.E. Fortun P.J. Hawkey C.J. et al.Probiotics for maintenance of remission in Crohn's disease.Cochrane Database Syst Rev. 2006; 4 (CD004826)Google Scholar, 16Shen J. Ran H.Z. Yin M.H. et al.Meta-analysis: the effect and adverse events of lactobacilli versus placebo in maintenance therapy for Crohn disease.Intern Med J. 2009; 39: 103-109Crossref PubMed Scopus (54) Google Scholar, 17Doherty G.A. Bennett G.C. Cheifetz A.S. et al.Meta-analysis: targeting the intestinal microbiota in prophylaxis for post-operative Crohn's disease.Aliment Pharmacol Ther. 2010; 31: 802-809PubMed Google Scholar In this issue of Clinical Gastroenterology and Hepatology, Boureille and colleagues18Bourreille A. Cadiot G. Le Dreau G. et al.Saccharomyces boulardii does not prevent relapse of Crohn’s disease.Clin Gastroenterol Hepatol. 2013; 11: 982-987Abstract Full Text Full Text PDF PubMed Scopus (112) Google Scholar report the results of a prospective, 52-week double-blind, placebo-controlled, multicenter randomized trial to assess the effect of S boulardii on maintenance of remission in patients with CD. Patients with active CD who achieved remission with corticosteroids, budesonide, or aminosalicylates were eligible to participate. If remission was not achieved at week 4, investigators were able to modify the induction treatment strategy by switching to corticosteroids from aminosalicylates or vice versa. Participants were stratified on the basis of the type of induction agent used to induce remission (aminosalicylates vs steroids) and then randomized to 1 g daily S boulardii or placebo. The initial treatment strategy used to induce remission was tapered off. The primary outcome of the study was the percentage of patients in remission at 1 year. At the end of the study period, relapses were noted in 38 patients (47.5%) in the S boulardii group compared with 42 patients (53.2%) in the placebo group (P = .5). A large number of participants were excluded from the intention-to-treat population, resulting in a per-protocol population of 125 participants. No differences in relapse rates between groups were noted in the per-protocol analysis. There were also no differences in the median time to relapse, percentage of relapses during the weaning period of the initial induction treatment, percentage of relapses after treatment discontinuation, or in the median Crohn's disease activity index score between the 2 groups. A particularly interesting finding in this study was discovered when comparing outcomes by smoking history. Among nonsmokers, those given placebo were more than twice as likely to relapse compared with those who received S boulardii (72% vs 34.5%, P = .016). After adjusting for the stratification factor, the beneficial effect of S boulardii persisted among nonsmokers (odds ratio [OR], 0.18, 95% confidence interval [CI], 0.05–0.62); however, this effect was blunted when the former smoker and nonsmoker groups were combined (OR, 0.57; 95% CI, 0.25–1.33). The protective effect of S boulardii in nonsmokers was still evident in the final multivariate regression model that included extraintestinal manifestations and the stratification factor (OR, 0.22; 95% CI, 0.07–0.7; P = .01). How should these results be interpreted? As always, results of subgroup analyses should be interpreted with caution. Despite the limitations of subgroup analyses, are the results shown biologically plausible? Verschuere et al19Verschuere S. Bracke K.R. Demoor T. et al.Cigarette smoking alters epithelial apoptosis and immune composition in murine GALT.Lab Invest. 2011; 91: 1056-1067Crossref PubMed Scopus (50) Google Scholar, 20Verschuere S. Allais L. Bracke K.R. et al.Cigarette smoke and the terminal ileum: increased autophagy in murine follicle-associated epithelium and Peyer's patches.Histochem Cell Biol. 2012; 137: 293-301Crossref PubMed Scopus (17) Google Scholar have demonstrated in murine ileal follicle-associated epithelia that chronic exposure to cigarette smoke induces epithelial apoptosis, increased immune cell accumulation in Peyer patches, and increased autophagy-induced epithelial oxidative damage in ileal tissue, thereby increasing risk of CD. Tomoda et al21Tomoda K. Kubo K. Asahara T. et al.Cigarette smoke decreases organic acids levels and population of Bifidobacterium in the caecum of rats.J Toxicol Sci. 2011; 36: 261-266Crossref PubMed Scopus (33) Google Scholar found that cigarette smoke exposure was associated with decreased organic acid levels and Bifidobactrium levels in rat cecal contents. Taken together, these results suggest that cigarette smoke disrupts the integrity of the intestinal border, increases immune responses, decreases prebiotics, and decreases protective intestinal bacteria, thereby worsening outcomes in CD. Thus, smoking may result in a significant derangement in the gut microbiome and in host responses to the microbiome that are too great for probiotics alone to restore. This is purely speculative and needs to be confirmed in future studies. It is possible that probiotics may be efficacious to maintain remission in different subgroups of patients. Steroid-treated patients represent a group of patients with moderate to severe disease compared with patients treated with aminosalicylates. Thus, patients with milder disease may respond to probiotics. Stratified analyses in aminosalicylate-treated and steroid-treated patients did not show significant differences in relapse rates between S boulardii–treated and placebo-treated patients in either subgroup; however, the study was not powered to identify significant differences in each treatment stratum. We know from studies in biologics that early treatment is associated with improved outcomes. Is it possible that use of probiotics earlier in the disease course would result in better outcomes? The current study included patients with a short duration of disease. Therefore, one would have expected them to respond well to medical treatment. The earliest time to initiate treatment in clinical practice is in the postoperative setting. Again, probiotics disappoint when used in this setting. Is it possible that the authors selected the “wrong” probiotic to study? It seems certain that we will have different probiotics for use in the future, perhaps even genetically engineered probiotics to enhance treatment effect.22Zadeh M. Khan M.W. Goh Y.J. et al.Induction of intestinal pro-inflammatory immune responses by lipoteichoic acid.J Inflamm (Lond). 2012; 9: 7Crossref PubMed Scopus (19) Google Scholar, 23Mohamadzadeh M. Pfeiler E.A. Brown J.B. et al.Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid.Proc Natl Acad Sci U S A. 2011; 108: 4623-4630Crossref PubMed Scopus (192) Google Scholar, 24Khan M.W. Zadeh M. Bere P. et al.Modulating intestinal immune responses by lipoteichoic acid-deficient Lactobacillus acidophilus.Immunotherapy. 2012; 4: 151-161Crossref PubMed Scopus (19) Google Scholar, 25Saber R. Zadeh M. Pakanati K.C. et al.Lipoteichoic acid-deficient Lactobacillus acidophilus regulates downstream signals.Immunotherapy. 2011; 3: 337-347Crossref PubMed Scopus (27) Google Scholar However, analyses of existing studies with probiotics do not suggest that changing probiotics would have changed the outcome observed in this study. Similarly, some may argue that probiotics are not a “stand alone” treatment and should be used in combination with other therapies as adjunctive therapy. Although possible, this has not been confirmed previously. It should be noted that the eligibility and outcome measures were defined by symptom-based indexes (Harvey–Bradshaw index and Crohn's disease activity index).26Harvey R.F. Bradshaw J.M. A simple index of Crohn's-disease activity.Lancet. 1980; 1: 514Abstract PubMed Scopus (2050) Google Scholar, 27Best W.R. Becktel J.M. Singleton J.W. et al.Development of a Crohn's disease activity index: National Cooperative Crohn's Disease Study.Gastroenterology. 1976; 70: 439-444Abstract Full Text PDF PubMed Scopus (2946) Google Scholar The limitations of using symptom-based indexes have been well documented. The authors did include objective measures of disease activity, including sedimentation rate and quantitative C-reactive protein. No difference in these measures was noted between S boulardii–treated and placebo-treated patients. Including more objective data such as fecal calprotectin and/or endoscopic data on mucosal healing would have been helpful to examine the biological effect, if any, of S boulardii; however, during the time course of the study, symptom-based indices were the gold standard for assessment of disease activity in clinical trials. It would also have been interesting to include microbiome analyses before and after treatment, especially in the nonsmoker subgroup, to examine the effect of S boulardii on the microflora. In summary, use of probiotics to maintain remission in patients with CD cannot be advocated on the basis of the current study as well as prior meta-analyses. Use of probiotics in clinical practice should be limited to prevention of antibiotic-associated diarrhea,28Hempel S. Newberry S.J. Maher A.R. et al.Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis.JAMA. 2012; 307: 1959-1969Crossref PubMed Scopus (539) Google Scholar prevention of recurrent Clostridium difficile,29Johnston B.C. Ma S.S. Goldenberg J.Z. et al.Probiotics for the prevention of Clostridium difficile-associated diarrhea: a systematic review and meta-analysis.Ann Intern Med. 2012; 157: 878-888Crossref PubMed Scopus (305) Google Scholar and prevention and treatment of pouchitis.29Johnston B.C. Ma S.S. Goldenberg J.Z. et al.Probiotics for the prevention of Clostridium difficile-associated diarrhea: a systematic review and meta-analysis.Ann Intern Med. 2012; 157: 878-888Crossref PubMed Scopus (305) Google Scholar, 30Gionchetti P. Rizzello F. Helwig U. et al.Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial.Gastroenterology. 2003; 124: 1202-1209Abstract Full Text Full Text PDF PubMed Scopus (959) Google Scholar, 31Gionchetti P. Rizzello F. Venturi A. et al.Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial.Gastroenterology. 2000; 119: 305-309Abstract Full Text Full Text PDF PubMed Scopus (1292) Google Scholar Undoubtedly, patients will continue to use probiotics either as adjunctive therapy or as sole treatment for CD in a desire to find treatments with less side effects and as a way to empower themselves in the treatment process. Likewise, providers will still face questions from patients on which probiotic if any to use, what dose to select, and how to pay for these often costly treatments. Despite another negative study, more investigations in this area are needed, because other flora yet to be identified, combinations of flora, or genetically altered flora may prove to be beneficial. Saccharomyces boulardii Does Not Prevent Relapse of Crohn's DiseaseClinical Gastroenterology and HepatologyVol. 11Issue 8PreviewSaccharomyces boulardii is a probiotic yeast that has been shown to have beneficial effects on the intestinal epithelial barrier and digestive immune system. There is preliminary evidence that S boulardii could be used to treat patients with Crohn's disease (CD). We performed a randomized, placebo-controlled trial to evaluate the effects of S boulardii in patients with CD who underwent remission during therapy with steroids or aminosalicylates. Full-Text PDF" @default.
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• W1992600007 title "To Yeast or Not to Yeast: A Probiotic Question" @default.
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