Fecal microbiota transplantation for managing irritable bowel syndrome

References

• Canavan C, West J, Card T. The epidemiology of irritable bowel syndrome. Clin Epidemiol. 2014;6:71–80.
   PubMed Web of Science ®Google Scholar
• El-Salhy M. Recent developments in the pathophysiology of irritable bowel syndrome. World J Gastroenterol. 2015;21:7621–7636.
   PubMed Web of Science ®Google Scholar
• El-Salhy M, Hatlebakk JG, Gilja OH, et al. Irritable bowel syndrome: recent developments in diagnosis, pathophysiology, and treatment. Expert Rev Gastroenterol Hepatol. 2014;8:435–443.
   PubMed Web of Science ®Google Scholar
• Sperber AD, Dumitrascu D, Fukudo S, et al. The global prevalence of IBS in adults remains elusive due to the heterogeneity of studies: a Rome foundation working team literature review. Gut. 2017;66:1075–1082.
   PubMed Web of Science ®Google Scholar
• El-Salhy M. Irritable bowel syndrome: diagnosis and pathogenesis. World J Gastroenterol. 2012;18:5151–5163.
   PubMed Web of Science ®Google Scholar
• Lovell RM, Ford AC. Global prevalence of and risk factors for irritable bowel syndrome: a meta-analysis. Clin Gastroenterol Hepatol. 2012;10:712–721 e714.
   PubMed Web of Science ®Google Scholar
• El-Salhy M, Gundersen D, Hatlebakk JG, et al. Irritable bowel syndrome: diagnosis, pathogenesis and treatment options. New York: Nova Science Publishers, Inc; 2012.
   Google Scholar
• Schwille-Kiuntke J, Enck P, Zendler C, et al. Postinfectious irritable bowel syndrome: follow-up of a patient cohort of confirmed cases of bacterial infection with Salmonella or Campylobacter. Neurogastroenterol Motil. 2011;23:e479–488.
   PubMed Web of Science ®Google Scholar
• Spiller R, Garsed K. Infection, inflammation, and the irritable bowel syndrome. Dig Liver Dis. 2009;41:844–849.
   PubMedGoogle Scholar
• El-Salhy M. Recent advances in the diagnosis of irritable bowel syndrome. Expert Rev Gastroenterol Hepatol. 2015;9:1161–1174.
   PubMed Web of Science ®Google Scholar
• El-Salhy M, Gundersen D, Gilja OH, et al. Is irritable bowel syndrome an organic disorder? World J Gastroenterol. 2014;20:384–400.
   PubMed Web of Science ®Google Scholar
• Camilleri M, Halawi H, Oduyebo I. Biomarkers as a diagnostic tool for irritable bowel syndrome: where are we? Expert Rev Gastroenterol Hepatol. 2017;11:303–316.
   PubMed Web of Science ®Google Scholar
• El-Salhy M, Lomholt-Beck B, Hausken T. Chromogranin A as a possible tool in the diagnosis of irritable bowel syndrome. Scand J Gastroenterol. 2010;45:1435–1439.
   PubMed Web of Science ®Google Scholar
• Manning AP, Thompson WG, Heaton KW, et al. Towards positive diagnosis of the irritable bowel. Br Med J. 1978;2:653–654.
   PubMed Web of Science ®Google Scholar
• Palsson OS, Whitehead WE, Van Tilburg MA, et al. Rome IV diagnostic questionnaires and tables for investigators and clinicians. Gastroenterology. 2016 Feb 13. pili: s0016-5085 (16)00180-3.
   Google Scholar
• Malikowski T, Khanna S, Pardi DS. Fecal microbiota transplantation for gastrointestinal disorders. Curr Opin Gastroenterol. 2017;33:8–13.
   PubMed Web of Science ®Google Scholar
• Sundin J, Ohman L, Simren M. Understanding the gut microbiota in inflammatory and functional gastrointestinal diseases. Psychosom Med. 2017;79:857–867.
   PubMed Web of Science ®Google Scholar
• Sundin J, Rangel I, Fuentes S, et al. Altered faecal and mucosal microbial composition in post-infectious irritable bowel syndrome patients correlates with mucosal lymphocyte phenotypes and psychological distress. Aliment Pharmacol Ther. 2015;41:342–351.
   PubMed Web of Science ®Google Scholar
• Ohman L, Tornblom H, Simren M. Crosstalk at the mucosal border: importance of the gut microenvironment in IBS. Nat Rev Gastroenterol Hepatol. 2015;12:36–49.
   PubMed Web of Science ®Google Scholar
• Kassinen A, Krogius-Kurikka L, Makivuokko H, et al. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology. 2007;133:24–33.
   PubMed Web of Science ®Google Scholar
• Malinen E, Rinttila T, Kajander K, et al. Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol. 2005;100:373–382.
   PubMed Web of Science ®Google Scholar
• Matto J, Maunuksela L, Kajander K, et al. Composition and temporal stability of gastrointestinal microbiota in irritable bowel syndrome – a longitudinal study in IBS and control subjects. FEMS Immunol Med Microbiol. 2005;43:213–222.
   PubMed Web of Science ®Google Scholar
• Balsari A, Ceccarelli A, Dubini F, et al. The fecal microbial population in the irritable bowel syndrome. Microbiologica. 1982;5:185–194.
   PubMed Web of Science ®Google Scholar
• Si JM, Yu YC, Fan YJ, et al. Intestinal microecology and quality of life in irritable bowel syndrome patients. World J Gastroenterol. 2004;10:1802–1805.
   PubMed Web of Science ®Google Scholar
• Kerckhoffs AP, Samsom M, van der Rest ME, et al. Lower bifidobacteria counts in both duodenal mucosa-associated and fecal microbiota in irritable bowel syndrome patients. World J Gastroenterol. 2009;15:2887–2892.
   PubMed Web of Science ®Google Scholar
• Codling C, O’Mahony L, Shanahan F, et al. A molecular analysis of fecal and mucosal bacterial communities in irritable bowel syndrome. Dig Dis Sci. 2010;55:392–397.
   PubMed Web of Science ®Google Scholar
• Rajilic-Stojanovic M, Biagi E, Heilig HG, et al. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology. 2011;141:1792–1801.
   PubMed Web of Science ®Google Scholar
• Parkes GC, Rayment NB, Hudspith BN, et al. Distinct microbial populations exist in the mucosa-associated microbiota of sub-groups of irritable bowel syndrome. Neurogastroenterol Motil. 2012;24:31–39.
   PubMed Web of Science ®Google Scholar
• Parkes GC, Brostoff J, Whelan K, et al. Gastrointestinal microbiota in irritable bowel syndrome: their role in its pathogenesis and treatment. Am J Gastroenterol. 2008;103:1557–1567.
   PubMed Web of Science ®Google Scholar
• Rajilic-Stojanovic M, Jonkers DM, Salonen A, et al. Intestinal microbiota and diet in IBS: causes, consequences, or epiphenomena? Am J Gastroenterol. 2015;110:278–287.
   PubMed Web of Science ®Google Scholar
• Pinn DM, Aroniadis OC, Brandt LJ. Is fecal microbiota transplantation (FMT) an effective treatment for patients with functional gastrointestinal disorders (FGID)? Neurogastroenterol Motil. 2015;27:19–29.
   PubMed Web of Science ®Google Scholar
• Mazzawi T, Lied GA, El-Salhy M, et al. Effect of fecal microbiota transplantation on the symptoms and duodenal enteroendocrine cells in patients with irritable bowel syndrome. United European Gastroenterol J. 2016;4(Suppl.5):677.
   PubMed Web of Science ®Google Scholar
• Mazzawi T, Lied GA, El-Salhy M, et al. Kinetics of microbial community composition in patients with diarrhea-predominant irritable bowel syndrome following faecal microbiota transplantation. United European Gastroenterol J. 2016;4(Suppl.5):LB11–LB11.
   Google Scholar
• Borody T, Fischer M, Mitchell S, et al. Fecal microbiota transplantation in gastrointestinal disease: 2015 update and the road ahead. Expert Rev Gastroenterol Hepatol. 2015;9:1379–1391.
   PubMed Web of Science ®Google Scholar
• Borody TJ, Brandt LJ, Paramsothy S. Therapeutic faecal microbiota transplantation: current status and future developments. Curr Opin Gastroenterol. 2014;30:97–105.
   PubMed Web of Science ®Google Scholar
• Borody TJ, Campbell J. Fecal microbiota transplantation: techniques, applications, and issues. Gastroenterol Clin North Am. 2012;41:781–803.
   PubMed Web of Science ®Google Scholar
• Borody TJ, Connelly N, Mitchell SW. Fecal microbiota transplantation in gastrointestinal diseases: what practicing physicians should know. Pol Arch Med Wewn. 2015;125:852–858.
   PubMed Web of Science ®Google Scholar
• Borody TJ, George L, Andrews P, et al. Bowel-flora alteration: a potential cure for inflammatory bowel disease and irritable bowel syndrome? Med J Aust. 1989;150:604.
   PubMed Web of Science ®Google Scholar
• Borody TJ, Khoruts A. Fecal microbiota transplantation and emerging applications. Nat Rev Gastroenterol Hepatol. 2011;9:88–96.
   PubMed Web of Science ®Google Scholar
• Borody TJ, Paramsothy S, Agrawal G. Fecal microbiota transplantation: indications, methods, evidence, and future directions. Curr Gastroenterol Rep. 2013;15:337.
   PubMedGoogle Scholar
• Holvoet T, Joossens M, Wang J, et al. Assessment of faecal microbial transfer in irritable bowel syndrome with severe bloating. Gut. 2017;66:980–982.
   PubMed Web of Science ®Google Scholar
• Pinn DM, Aroniadis OC, Brandt LJ. Is fecal microbiota transplantation the answer for irritable bowel syndrome? A single-center experience. Am J Gastroenterol. 2014;109:1831–1832.
   PubMed Web of Science ®Google Scholar
• Mazzawi T, Lied GA, Sangnes DA, et al. The kinetics of gut microbial community composition in patients with irritable bowel syndrome following faecal microbiota transplantation. Submitted to Neurog Motil. 2017.
   Google Scholar
• Cammarota G, Ianiro G, Tilg H, et al. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017;66:569–580.
   PubMed Web of Science ®Google Scholar
• Lee CH, Steiner T, Petrof EO, et al. Frozen vs Fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent clostridium difficile infection: a randomized clinical trial. Jama. 2016;315:142–149.
   PubMed Web of Science ®Google Scholar
• Wise J. Frozen faecal matter works as well as fresh for transplantation in C difficile patients. Bmj. 2016;352:i138.
   PubMedGoogle Scholar
• Owens C, Broussard E, Surawicz C. Fecal microbiota transplantation and donor standardization. Trends Microbiol. 2013;21:443–445.
   PubMed Web of Science ®Google Scholar
• Kelly CR, Kunde SS, Khoruts A. Guidance on preparing an investigational new drug application for fecal microbiota transplantation studies. Clin Gastroenterol Hepatol. 2014;12:283–288.
   PubMed Web of Science ®Google Scholar
• Wang S, Xu M, Wang W, et al. Systematic review: adverse events of fecal microbiota transplantation. PloS One. 2016;11:e0161174.
   PubMed Web of Science ®Google Scholar
• Baxter M, Colville A. Adverse events in faecal microbiota transplant: a review of the literature. J Hosp Infect. 2016;92:117–127.
   PubMed Web of Science ®Google Scholar
• Hunter JC, Mu Y, Dumyati GK, et al. Burden of nursing home-onset clostridium difficile infection in the United States: estimates of incidence and patient outcomes. Open Forum Infect Dis. 2016;3:ofv196.
   PubMed Web of Science ®Google Scholar
• Lessa FC, Winston LG, McDonald LC. Burden of clostridium difficile infection in the United States. N Engl J Med. 2015;372:2369–2370.
   PubMed Web of Science ®Google Scholar
• Vancamelbeke M, Vermeire S. The intestinal barrier: a fundamental role in health and disease. Expert Rev Gastroenterol Hepatol. 2017;11:821–834.
   PubMed Web of Science ®Google Scholar
• Camilleri M, Madsen K, Spiller R, et al. Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterol Motil. 2012;24:503–512.
   PubMed Web of Science ®Google Scholar
• El-Salhy M, Hausken T, Gilja OH, et al. The possible role of gastrointestinal endocrine cells in the pathophysiology of irritable bowel syndrome. Expert Rev Gastroenterol Hepatol. 2017;11:139–148.
   PubMed Web of Science ®Google Scholar
• Holzer P, Farzi A. Neuropeptides and the microbiota-gut-brain axis. Adv Exp Med Biol. 2014;817:195–219.
   PubMed Web of Science ®Google Scholar
• Soret R, Chevalier J, De Coppet P, et al. Short-chain fatty acids regulate the enteric neurons and control gastrointestinal motility in rats. Gastroenterology. 2010;138:1772–1782.
   PubMed Web of Science ®Google Scholar
• Ohman L, Tornblom H, Simren M. Crosstalk at the mucosal border: importance of the gut microenvironment in IBS. Nat Rev Gastroenterol Hepatol. 2014;12:36–49.
   PubMed Web of Science ®Google Scholar
• Camilleri M. Management of the irritable bowel syndrome. Gastroenterology. 2001;120:652–668.
   PubMed Web of Science ®Google Scholar
• Camilleri M. Peripheral mechanisms in irritable bowel syndrome. N Engl J Med. 2012;367:1626–1635.
   PubMed Web of Science ®Google Scholar
• Camilleri M, Katzka DA. Irritable bowel syndrome: methods, mechanisms, and pathophysiology. Genetic epidemiology and pharmacogenetics in irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2012;302:G1075–1084.
   PubMed Web of Science ®Google Scholar
• Camilleri M, Heading RC, Thompson WG. Clinical perspectives, mechanisms, diagnosis and management of irritable bowel syndrome. Aliment Pharmacol Ther. 2002;16:1407–1430.
   PubMed Web of Science ®Google Scholar
• Hamer HM, Jonkers D, Venema K, et al. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008;27:104–119.
   PubMed Web of Science ®Google Scholar
• Hamer HM, Jonkers DM, Bast A, et al. Butyrate modulates oxidative stress in the colonic mucosa of healthy humans. Clin Nutr. 2009;28:88–93.
   PubMed Web of Science ®Google Scholar
• Hamer HM, Jonkers DM, Loof A, et al. Analyses of human colonic mucus obtained by an in vivo sampling technique. Dig Liver Dis. 2009;41:559–564.
   PubMedGoogle Scholar
• Hamer HM, Jonkers DM, Renes IB, et al. Butyrate enemas do not affect human colonic MUC2 and TFF3 expression. Eur J Gastroenterol Hepatol. 2010;22:1134–1140.
   PubMed Web of Science ®Google Scholar
• Hamer HM, Jonkers DM, Vanhoutvin SA, et al. Effect of butyrate enemas on inflammation and antioxidant status in the colonic mucosa of patients with ulcerative colitis in remission. Clin Nutr. 2010;29:738–744.
   PubMed Web of Science ®Google Scholar
• Keszthelyi D, Troost FJ, Jonkers DM, et al. Alterations in mucosal neuropeptides in patients with irritable bowel syndrome and ulcerative colitis in remission: a role in pain symptom generation? Eur J Pain. 2013;17:1299–1306.
   PubMed Web of Science ®Google Scholar
• Vanhoutvin SA, Troost FJ, Hamer HM, et al. Butyrate-induced transcriptional changes in human colonic mucosa. PloS One. 2009;4:e6759.
   PubMed Web of Science ®Google Scholar
• Vanhoutvin SA, Troost FJ, Kilkens TO, et al. The effects of butyrate enemas on visceral perception in healthy volunteers. Neurogastroenterol Motil. 2009;21:952–e976.
   PubMed Web of Science ®Google Scholar
• Stephen AM, Cummings JH. Mechanism of action of dietary fibre in the human colon. Nature. 1980;284:283–284.
   PubMed Web of Science ®Google Scholar
• Stephen AM, Cummings JH. Water holding by dietary fibre in vitro and its relationship to faecal bulking in man. Proc Nutr Soc. 1979;38:55a.
   PubMed Web of Science ®Google Scholar
• Eswaran S, Muir J, Chey WD. Fiber and functional gastrointestinal disorders. Am J Gastroenterol. 2013;108:718–727.
   PubMed Web of Science ®Google Scholar
• Chutkan R, Fahey G, Wright WL, et al. Viscous versus nonviscous soluble fiber supplements: mechanisms and evidence for fiber-specific health benefits. J Am Acad Nurse Pract. 2012;24:476–487.
   PubMedGoogle Scholar
• Zimmerman MA, Singh N, Martin PM, et al. Butyrate suppresses colonic inflammation through HDAC1-dependent Fas upregulation and Fas-mediated apoptosis of T cells. Am J Physiol Gastrointest Liver Physiol. 2012;302:G1405–1415.
   PubMed Web of Science ®Google Scholar
• Klampfer L, Huang J, Sasazuki T, et al. Inhibition of interferon gamma signaling by the short chain fatty acid butyrate. Mol Cancer Res. 2003;1:855–862.
   PubMed Web of Science ®Google Scholar
• Stempelj M, Kedinger M, Augenlicht L, et al. Essential role of the JAK/STAT1 signaling pathway in the expression of inducible nitric-oxide synthase in intestinal epithelial cells and its regulation by butyrate. J Biol Chem. 2007;282(13):9797–9804.
   PubMed Web of Science ®Google Scholar
• Mazzawi T, El-Sahy M, Lied GA, et al. Effect of faecal microbiota transplantation on the enteroendocrine cells of the colon in patients with Irritable Bowel Syndrome (IBS): double blinded-placebo controlled study. Neurogastroenterology Motil. 2017;29.Supl. 2.71.
   Web of Science ®Google Scholar
• El-Salhy M, Solomon T, Hausken T, et al. Gastrointestinal neuroendocrine peptides/amines in inflammatory bowel disease. World J Gasoenterol. 2017;23:5068–5086.
   PubMed Web of Science ®Google Scholar
• El-Salhy M, Gundersen D. Diet in irritable bowel syndrome. Nutr J. 2015;14:36.
   PubMed Web of Science ®Google Scholar
• El-Salhy M, Mazzawi T, Hausken T, et al. Interaction between diet and gastrointestinal endocrine cells. Biomed Reports. 2016;4:651–656.
   PubMed Web of Science ®Google Scholar
• Halmos EP. When the low FODMAP diet does not work. J Gastroenterol Hepatol. 2017;32 Suppl 1:69–72.
   PubMed Web of Science ®Google Scholar
• Staudacher HM, Whelan K, Irving PM, et al. Comparison of symptom response following advice for a diet low in fermentable carbohydrates (FODMAPs) versus standard dietary advice in patients with irritable bowel syndrome. J Hum Nutr Diet. 2011;24:487–495.
   PubMed Web of Science ®Google Scholar
• Bohn L, Storsrud S, Liljebo T, et al. Diet low in FODMAPs reduces symptoms of irritable bowel syndrome as well as traditional dietary advice: a randomized controlled trial. Gastroenterology. 2015;149:1399–1407.e1392.
   PubMed Web of Science ®Google Scholar
• Eswaran SL, Chey WD, Han-Markey T, et al. A randomized controlled trial comparing the low FODMAP diet vs. modified NICE guidelines in US adults with IBS-D. Am J Gastroenterol. 2016;111:1824–1832.
   PubMed Web of Science ®Google Scholar
• Bennet SMP, Bohn L, Storsrud S, et al. Multivariate modelling of faecal bacterial profiles of patients with IBS predicts responsiveness to a diet low in FODMAPs. Gut. 2017. pii: gutjnl-2016-313128. doi: 10.1136/gutjnl-2016-313128. [Epub ahead of print].
   PubMed Web of Science ®Google Scholar
• Halmos EP, Christophersen CT, Bird AR, et al. Diets that differ in their FODMAP content alter the colonic luminal microenvironment. Gut. 2015;64:93–100.
   PubMed Web of Science ®Google Scholar
• McIntosh K, Reed DE, Schneider T, et al. FODMAPs alter symptoms and the metabolome of patients with IBS: a randomised controlled trial. Gut. 2017;66(7):1241-1251. doi: 10.1136/gutjnl-2015-311339.
   Web of Science ®Google Scholar
• Catassi G, Lionetti E, Gatti S, et al. The low FODMAP diet: many question marks for a catchy acronym. Nutrients. 2017;9(3). pii: E292. doi: 10.3390/nu9030292.
   Web of Science ®Google Scholar
• McKenzie YA, Bowyer RK, Leach H, et al. British Dietetic Association systematic review and evidence-based practice guidelines for the dietary management of irritable bowel syndrome in adults (2016 update). J Hum Nutr Diet. 2016;29:549–575.
   PubMed Web of Science ®Google Scholar
• Ostgaard H, Hausken T, Gundersen D, et al. Diet and effects of diet management on quality of life and symptoms in patients with irritable bowel syndrome. Mol Med Report. 2012;5:1382–1390.
   PubMed Web of Science ®Google Scholar