The Impact of Exclusive Enteral Nutrition (EEN) on the Gut Microbiome in Crohn's Disease: A Review

Amber MacLellan, Jessica Moore-Connors, Shannan Grant, Leah Cahill, Morgan G I Langille, Johan Van Limbergen, Amber MacLellan, Jessica Moore-Connors, Shannan Grant, Leah Cahill, Morgan G I Langille, Johan Van Limbergen

Abstract

Crohn's disease (CD), a form of inflammatory bowel disease (IBD), is thought to arise from a complex interaction of genetics, the gut microbiome, and environmental factors, such as diet. There is clear evidence that dietary intervention is successful in the treatment of CD-exclusive enteral nutrition (EEN) is able to induce remission in up to 80% of CD patients. While the mechanism of action of EEN is not clear, EEN is known to cause profound changes in the gut microbiome. Understanding how EEN modifies the gut microbiome to induce remission could provide insight into CD etiopathogenesis and aid the development of microbiome-targeted interventions to guide ongoing dietary therapy to sustain remission. This review includes current literature on changes in composition and function of the gut microbiome associated with EEN treatment in CD patients.

Keywords: Crohn’s disease; exclusive enteral nutrition; microbiome.

Conflict of interest statement

The authors declare no conflict of interest.

References

    1. Fiocchi C. Inflammatory bowel disease pathogenesis: Where are we? J. Gastroenterol. Hepatol. 2015;30:12–18. doi: 10.1111/jgh.12751.
    1. Sinagra E., Tomasello G., Cappello F., Leone A., Cottone M., Bellavia M., Rossi F., Facella T., Damiani P., Zeenny M., et al. Probiotics, prebiotics and symbiotics in inflammatory bowel diseases: State-of-the-art and new insights. J. Biol. Regul. Homeost. Agents. 2013;27:919–933.
    1. Levy M., Kolodziejczyk A.A., Thaiss C.A., Elinav E. Dysbiosis and the immune system. Nat. Rev. Immunol. 2017;17:219–232. doi: 10.1038/nri.2017.7.
    1. Ruemmele F.M. Role of diet in inflammatory bowel disease. Ann. Nutr. Metab. 2016;68:33–41. doi: 10.1159/000445392.
    1. Penagini F., Dilillo D., Borsani B., Cococcioni L., Galli E., Bedogni G., Zuin G., Zuccotti G.V. Nutrition in pediatric inflammatory bowel disease: From etiology to treatment. A systematic review. Nutrients. 2016;8:334. doi: 10.3390/nu8060334.
    1. Falony G., Joossens M., Vieira-Silva S., Wang J., Darzi Y., Faust K., Kurilshikov A., Bonder M.J., Valles-Colomer M., Vandeputte D., et al. Population-level analysis of gut microbiome variation. Science. 2016;352:560–564. doi: 10.1126/science.aad3503.
    1. Zhernakova A., Kurilshikov A., Bonder M.J., Tigchelaar E.F., Schirmer M., Vatanen T., Mujagic Z., Vila A.V., Falony G., Vieira-Silva S., et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 2016;352:565–569. doi: 10.1126/science.aad3369.
    1. D′Souza S., Levy E., Mack D., Israel D., Lambrette P., Ghadirian P., Deslandres C., Morgan K., Seidman E.G., Amre D.K. Dietary patterns and risk for Crohn's disease in children. Inflamm. Bowel Dis. 2008;14:367–373. doi: 10.1002/ibd.20333.
    1. Yamamoto T., Shimoyama T., Kuriyama M. Dietary and enteral interventions for Crohn’s disease. Curr. Opin. Biotechnol. 2017;44:69–73. doi: 10.1016/j.copbio.2016.11.011.
    1. Sigall-Boneh R., Pfeffer-Gik T., Segal I., Zangen T., Boaz M., Levine A. Partial Enteral Nutrition with a Crohn’s Disease Exclusion Diet Is Effective for Induction of Remission in Children and Young Adults with Crohn’s Disease. Inflamm. Bowel Dis. 2014;20:1353–1360. doi: 10.1097/MIB.0000000000000110.
    1. Otley A.R., Russell R.K., Day A.S. Nutritional therapy for the treatment of pediatric Crohn’s disease. Expert Rev. Clin. Immunol. 2010;6:667–676. doi: 10.1586/eci.10.37.
    1. Ruemmele F., Veres G., Kolho K.-L., Griffiths A., Levine A., Escher J., Dias J.A., Barabino A., Braegger C., Bronsky J., et al. Consensus guidelines of ECCO/ESPGHAN on the medical management of pediatric Crohn’s disease. J. Crohn’s Colitis. 2014;8:1179–1207. doi: 10.1016/j.crohns.2014.04.005.
    1. Day A., Whitten K., Sidler M., Lemberg D. Systematic review: Nutritional therapy in paediatric Crohn’s disease. Aliment. Pharmacol. Ther. 2008;27:293–307. doi: 10.1111/j.1365-2036.2007.03578.x.
    1. Borrelli O., Cordischi L., Cirulli M., Paganelli M., Labalestra V., Uccini S., Russo P.M., Cucchiara S. Polymeric diet alone versus corticosteroids in the treatment of active pediatric Crohn’s disease: A randomized controlled open-label trial. Clin. Gastroenterol. Hepatol. 2006;4:744–753. doi: 10.1016/j.cgh.2006.03.010.
    1. Levine A., Turner D., Gik T.P., Dias J.A., Veres G., Shaoul R., Staiano A., Escher J., Kolho K.L., Paerregaard A., et al. Comparison of outcomes parameters for induction of remission in New Onset Pediatric Crohn’s Disease: Evaluation of the Porto IBD Group “Growth Relapse and Outcomes with Therapy” (GROWTH CD) Study. Inflamm. Bowel Dis. 2014;20:278–285. doi: 10.1097/01.MIB.0000437735.11953.68.
    1. Zachos M., Tondeur M., Griffiths A.M. Enteral nutritional therapy for induction of remission in Crohn’s disease. Cochrane Database Syst. Rev. 2007;24:CD000542.
    1. Grover Z., Burgess C., Muir R., Reilly C., Lewindon P.J. Early Mucosal Healing with Exclusive Enteral Nutrition is Associated with Improved Outcomes in Newly Diagnosed Children with Luminal Crohn’s disease. J. Crohn’s Colitis. 2016;10:1159–1164. doi: 10.1093/ecco-jcc/jjw075.
    1. Grover Z., Muir R., Lewindon P. Exclusive enteral nutrition induces early clinical, mucosal and transmural remission in paediatric Crohn’s disease. J. Gastroenterol. 2014;49:638–645. doi: 10.1007/s00535-013-0815-0.
    1. Altomare R., Damiano G., Abruzzo A., Palumbo V.D., Tomasello G., Buscemi S., Lo Monte A.I. Enteral nutrition support to treat malnutrition in inflammatory bowel disease. Nutrients. 2015;7:2125–2133. doi: 10.3390/nu7042125.
    1. Van Limbergen J., Haskett J., Griffiths A.M., Critch J., Huynh H., Ahmed N., de Bruyn J.C., Issenman R., El-Matary W., Walters T.D., et al. Toward enteral nutrition in the treatment of pediatric Crohn disease in Canada: A workshop to identify barriers and enablers. Can. J. Gastroenterol. Hepatol. 2015;29:351–356. doi: 10.1155/2015/509497.
    1. Levine A., Milo T., Buller H., Markowitz J. Consensus and controversy in the management of pediatric Crohn disease: An international survey. J. Pediatr. Gastroenterol. Nutr. 2003;36:464–469. doi: 10.1097/00005176-200304000-00008.
    1. Brahmbhatt V., Montoliu I., Bosco N., Martin F., Guy P. Characterization of Selected Metabolic and Immunologic Markers Following Exclusive Enteral Nutrition of Pediatric Crohn’s Disease Patients. J. Gastrointest. Dig. 2016;6:2. doi: 10.4172/2161-069X.1000466.
    1. Levine A., Wine E. Effects of enteral nutrition on Crohn’s disease: Clues to the impact of diet on disease pathogenesis. Inflamm. Bowel Dis. 2013;19:1322–1329. doi: 10.1097/MIB.0b013e3182802acc.
    1. Day A.S., Lopez R.N. Exclusive enteral nutrition in children with Crohn’s disease. World J. Gastroenterol. 2015;21:6809–6816.
    1. Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009;9:313–323. doi: 10.1038/nri2515.
    1. Sartor R.B. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134:577–594. doi: 10.1053/j.gastro.2007.11.059.
    1. Alhagamhmad M.H., Day A.S., Lemberg D.A., Leach S.T. An overview of the bacterial contribution to Crohn disease pathogenesis. J. Med. Microbiol. 2016;65:1049–1059.
    1. Bernstein C.N. Treatment of IBD: Where we are and where we are going. Am. J. Gastroenterol. 2015;110:114–126. doi: 10.1038/ajg.2014.357.
    1. Joossens M., Huys G., Cnockaert M., de Preter V., Verbeke K., Rutgeerts P., Vandamme P., Vermeire S. Dysbiosis of the faecal microbiota in patients with Crohn’s disease and their unaffected relatives. Gut. 2011;60:631–637. doi: 10.1136/gut.2010.223263.
    1. Takahashi K., Nishida A., Fujimoto T., Fujii M., Shioya M., Imaeda H., Inatomi O., Bamba S., Andoh A., Sugimoto M. Reduced abundance of butyrate-producing bacteria species in the fecal microbial community in Crohn’s disease. Digestion. 2016;93:59–65. doi: 10.1159/000441768.
    1. Frank D.N., Robertson C.E., Hamm C.M., Kpadeh Z., Zhang T., Chen H., Zhu W., Sartor R.B., Boedeker E.C., Harpaz N., et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm. Bowel Dis. 2011;17:179–184. doi: 10.1002/ibd.21339.
    1. Gevers D., Kugathasan S., Denson L.A., Vázquez-Baeza Y., Van Treuren W., Ren B., Schwager E., Knights D., Song S.J., Yassour M., et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe. 2014;15:382–392. doi: 10.1016/j.chom.2014.02.005.
    1. Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermudez-Humaran L.G., Gratadoux J.J., Blugeon S., Bridonneau C., Furet J.P., Corthier G., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA. 2008;105:16731–16736. doi: 10.1073/pnas.0804812105.
    1. Fujimoto T., Imaeda H., Takahashi K., Kasumi E., Bamba S., Fujiyama Y., Andoh A. Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn’s disease. J. Gastroenterol. Hepatol. 2013;28:613–619. doi: 10.1111/jgh.12073.
    1. Quévrain E., Maubert M., Michon C., Chain F., Marquant R., Tailhades J., Miquel S., Carlier L., Bermúdez-Humarán L., Pigneur B., et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut. 2015;65:365–367.
    1. Zechner E.L. Inflammatory disease caused by intestinal pathobionts. Curr. Opin. Microbiol. 2017;35:64–69. doi: 10.1016/j.mib.2017.01.011.
    1. Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., Wei D., Goldfarb K.C., Santee C.A., Lynch S.V., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–498. doi: 10.1016/j.cell.2009.09.033.
    1. Bellavia M., Damiano G., Gioviale M.C., Palumbo V.D., Cacciabaudo F., Buscemi G., Monte A.I.L. Abnormal expansion of segmented filamentous bacteria in the gut: A role in pathogenesis of chronic inflammatory intestinal diseases? Rev. Med. Microbiol. 2011;22:45–47. doi: 10.1097/MRM.0b013e328348ce81.
    1. Ringel Y., Maharshak N., Ringel-Kulka T., Wolber E.A., Sartor R.B., Carroll I.M. High throughput sequencing reveals distinct microbial populations within the mucosal and luminal niches in healthy individuals. Gut Microbes. 2015;6:173–181. doi: 10.1080/19490976.2015.1044711.
    1. Rangel I., Sundin J., Fuentes S., Repsilber D., Vos W., Brummer R.J. The relationship between faecal-associated and mucosal-associated microbiota in irritable bowel syndrome patients and healthy subjects. Aliment. Pharmacol. Ther. 2015;42:1211–1221. doi: 10.1111/apt.13399.
    1. Ward D.M., Weller R., Bateson M.M. 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature. 1990;345:63–65. doi: 10.1038/345063a0.
    1. Chakravorty S., Helb D., Burday M., Connell N., Alland D. A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J. Microbiol. Methods. 2007;69:330–339. doi: 10.1016/j.mimet.2007.02.005.
    1. Fraher M.H., O′toole P.W., Quigley E.M. Techniques used to characterize the gut microbiota: A guide for the clinician. Nat. Rev. Gastroenterol. Hepatol. 2012;9:312–322. doi: 10.1038/nrgastro.2012.44.
    1. Moore-Connors J.M., Dunn K.A., Bielawski J.P., van Limbergen J. Novel strategies for applied metagenomics. Inflamm. Bowel Dis. 2016;22:709–718. doi: 10.1097/MIB.0000000000000717.
    1. Lionetti P., Callegari M.L., Ferrari S., Cavicchi M.C., Pozzi E., de Martino M., Morelli L. Enteral nutrition and microflora in pediatric Crohn’s disease. J. Parenter. Enter. Nutr. 2005;29:S173–S178. doi: 10.1177/01486071050290S4S173.
    1. Leach S., Mitchell H., Eng W., Zhang L., Day A. Sustained modulation of intestinal bacteria by exclusive enteral nutrition used to treat children with Crohn’s disease. Aliment. Pharmacol. Ther. 2008;28:724–733. doi: 10.1111/j.1365-2036.2008.03796.x.
    1. Shiga H., Kajiura T., Shinozaki J., Takagi S., Kinouchi Y., Takahashi S., Negoro K., Endo K., Kakuta Y., Suzuki M., et al. Changes of faecal microbiota in patients with Crohn’s disease treated with an elemental diet and total parenteral nutrition. Dig. Liver Dis. 2012;44:736–742. doi: 10.1016/j.dld.2012.04.014.
    1. Gerasimidis K., Bertz M., Hanske L., Junick J., Biskou O., Aguilera M., Garrick V., Russell R.K., Blaut M., McGrogan P., et al. Decline in Presumptively Protective Gut Bacterial Species and Metabolites Are Paradoxically Associated with Disease Improvement in Pediatric Crohn’s Disease During Enteral Nutrition. Inflamm. Bowel Dis. 2014;20:861–871. doi: 10.1097/MIB.0000000000000023.
    1. Sokol H., Seksik P., Furet J., Firmesse O., Nion-Larmurier I., Beaugerie L., Cosnes J., Corthier G., Marteau P., Dore J. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm. Bowel Dis. 2009;15:1183–1189. doi: 10.1002/ibd.20903.
    1. Jia W., Whitehead R.N., Griffiths L., Dawson C., Waring R.H., Ramsden D.B., Hunter J.O., Cole J.A. Is the abundance of Faecalibacterium prausnitzii relevant to Crohn’s disease? FEMS Microbiol. Lett. 2010;310:138–144. doi: 10.1111/j.1574-6968.2010.02057.x.
    1. Hansen R., Russell R.K., Reiff C., Louis P., McIntosh F., Berry S.H., Mukhopadhya I., Bisset W.M., Barclay A.R., Bishop J., et al. Microbiota of de-novo pediatric IBD: Increased Faecalibacterium prausnitzii and reduced bacterial diversity in Crohn’s but not in ulcerative colitis. Am. J. Gastroenterol. 2012;107:1913–1922. doi: 10.1038/ajg.2012.335.
    1. D′argenio V., Precone V., Casaburi G., Miele E., Martinelli M., Staiano A., Salvatore F., Sacchetti L. An altered gut microbiome profile in a child affected by Crohn’s disease normalized after nutritional therapy. Am. J. Gastroenterol. 2013;108:851–852. doi: 10.1038/ajg.2013.46.
    1. Kaakoush N.O., Day A.S., Leach S.T., Lemberg D.A., Nielsen S., Mitchell H.M. Effect of exclusive enteral nutrition on the microbiota of children with newly diagnosed Crohn’s disease. Clin. Transl. Gastroenterol. 2015;6:e71. doi: 10.1038/ctg.2014.21.
    1. Schwerd T., Frivolt K., Clavel T., Lagkouvardos I., Katona G., Mayr D., Uhlig H.H., Haller D., Koletzko S., Bufler P. Exclusive enteral nutrition in active pediatric Crohn disease: Effects on intestinal microbiota and immune regulation. J. Allergy Clin. Immunol. 2016;138:592–596. doi: 10.1016/j.jaci.2015.12.1331.
    1. Quince C., Ijaz U.Z., Loman N., Eren A.M., Saulnier D., Russell J., Haig S.J., Calus S.T., Quick J., Barclay A., et al. Extensive modulation of the fecal metagenome in children with Crohn’s disease during exclusive enteral nutrition. Am. J. Gastroenterol. 2015;110:1718–1729. doi: 10.1038/ajg.2015.357.
    1. Lewis J.D., Chen E.Z., Baldassano R.N., Otley A.R., Griffiths A.M., Lee D., Bittinger K., Bailey A., Friedman E.S., Hoffmann C., et al. Inflammation, antibiotics, and diet as environmental stressors of the gut microbiome in pediatric Crohn’s disease. Cell Host Microbe. 2015;18:489–500. doi: 10.1016/j.chom.2015.09.008.
    1. David L.A., Maurice C.F., Carmody R.N., Gootenberg D.B., Button J.E., Wolfe B.E., Ling A.V., Devlin A.S., Varma Y., Fischbach M.A., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563. doi: 10.1038/nature12820.
    1. Guinet-Charpentier C., Lepage P., Morali A., Chamaillard M., Peyrin-Biroulet L. Effects of enteral polymeric diet on gut microbiota in children with Crohn’s disease. Gut. 2016;66:194–195. doi: 10.1136/gutjnl-2015-311058.
    1. Dunn K.A., Moore-Connors J.M., MacIntyre B., Stadnyk A., Thomas N.A., Noble A., Madhi G., Rashid M., Otley A.R., Bielawski J.P., et al. Early changes in microbial community structure are associated with sustained remission following nutritional treatment of Pediatric Crohn’s Disease. Inflamm. Bowel Dis. 2016;22:2853–2862. doi: 10.1097/MIB.0000000000000956.
    1. Mukhopadhya I., Hansen R., El-Omar E.M., Hold G.L. IBD—What role do Proteobacteria play? Nat. Rev. Gastroenterol. Hepatol. 2012;9:219–230. doi: 10.1038/nrgastro.2012.14.
    1. Morgan X.C., Tickle T.L., Sokol H., Gevers D., Devaney K.L., Ward D.V., Reyes J.A., Shah S.A., LeLeiko N., Snapper S.B., et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13:R79. doi: 10.1186/gb-2012-13-9-r79.
    1. Hamer H.M., De Preter V., Windey K., Verbeke K. Functional analysis of colonic bacterial metabolism: Relevant to health? Am. J. Physiol. Gastrointest. Liver Physiol. 2012;302:G1–G9. doi: 10.1152/ajpgi.00048.2011.
    1. Macfarlane G.T., Macfarlane S. Fermentation in the human large intestine: Its physiologic consequences and the potential contribution of prebiotics. J. Clin. Gastroenterol. 2011;45:S120–S127. doi: 10.1097/MCG.0b013e31822fecfe.
    1. Shade A., Handelsman J. Beyond the Venn diagram: The hunt for a core microbiome. Environ. Microbiol. 2012;14:4–12. doi: 10.1111/j.1462-2920.2011.02585.x.
    1. Larsen P.E., Dai Y. Metabolome of human gut microbiome is predictive of host dysbiosis. Gigascience. 2015;4:42. doi: 10.1186/s13742-015-0084-3.
    1. Guinane C.M., Cotter P.D. Role of the gut microbiota in health and chronic gastrointestinal disease: Understanding a hidden metabolic organ. Ther. Adv. Gastroenterol. 2013;6:295–308. doi: 10.1177/1756283X13482996.
    1. Tremaroli V., Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242–249. doi: 10.1038/nature11552.
    1. Walton C., Montoya M., Fowler D., Turner C., Jia W., Whitehead R., Griffiths L., Waring R., Ramsden D., Cole J., et al. Enteral feeding reduces metabolic activity of the intestinal microbiome in Crohn’s disease: An observational study. Eur. J. Clin. Nutr. 2016;70:1052–1056. doi: 10.1038/ejcn.2016.74.
    1. Yao C., Muir J., Gibson P. Review article: Insights into colonic protein fermentation, its modulation and potential health implications. Aliment. Pharmacol. Ther. 2016;43:181–196. doi: 10.1111/apt.13456.
    1. Mottawea W., Chiang C.-K., Mühlbauer M., Starr A.E., Butcher J., Abujamel T., Deeke S.A., Brandel A., Zhou H., Shokralla S., et al. Altered intestinal microbiota–host mitochondria crosstalk in new onset Crohn’s disease. Nat. Commun. 2016;7:13419. doi: 10.1038/ncomms13419.
    1. Bellavia M., Tomasello G., Romeo M., Damiani P., Monte A.I.L., Lozio L., Campanella C., Gammazza A.M., Rappa F., Zummo G., et al. Gut microbiota imbalance and chaperoning system malfunction are central to ulcerative colitis pathogenesis and can be counteracted with specifically designed probiotics: A working hypothesis. Med. Microbiol. Immunol. 2013;202:393–406. doi: 10.1007/s00430-013-0305-2.
    1. Sanderson I.R., Udeen S., Davies P.S., Savage M.O., Walker-Smith J.A. Remission induced by an elemental diet in small bowel Crohn’s disease. Arch. Dis. Child. 1987;62:123–127. doi: 10.1136/adc.62.2.123.
    1. Griffiths A.M. Enteral feeding in inflammatory bowel disease. Curr. Opin. Clin. Nutr. Metab. Care. 2006;9:314–318. doi: 10.1097/01.mco.0000222117.76536.49.
    1. Wu G.D., Chen J., Hoffmann C., Bittinger K., Chen Y.-Y., Keilbaugh S.A., Bewtra M., Knights D., Walters W.A., Knight R., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334:105–108. doi: 10.1126/science.1208344.
    1. Martino J.V., Limbergen J.V., Cahil L. The role of carrageenan and carboxymethylcellulose in the development of intestinal inflammation. Front. Pediatr. 2017;5:96.
    1. Johnson T., Macdonald S., Hill S.M., Thomas A., Murphy M.S. Treatment of active Crohn’s disease in children using partial enteral nutrition with liquid formula: A randomised controlled trial. Gut. 2006;55:356–361. doi: 10.1136/gut.2004.062554.
    1. Dunn K.A., Moore-Connors J.M., MacIntyre B., Stadnyk A., Thomas N.A., Noble A., Madhi G., Rashid M., Otley A.R., Bielawski J.P., et al. The gut microbiome of pediatric Crohn’s disease patients differs from healthy controls in genes that can influence the balance between a healthy and dysregulated immune response. Inflamm. Bowel Dis. 2016;22:2607–2618. doi: 10.1097/MIB.0000000000000949.
    1. Kinsey L., Burden S. A survey of people with inflammatory bowel disease to investigate their views of food and nutritional issues. Eur. J. Clin. Nutr. 2016;70:852–854. doi: 10.1038/ejcn.2016.57.
    1. Svolos V., Gerasimidis K., Buchanan E., Curtis L., Garrick V., Hay J., Laird S., Munro J., Gaya D.R., Russell R.K., et al. Dietary treatment of Crohn’s disease: Perceptions of families with children treated by exclusive enteral nutrition, a questionnaire survey. BMC Gastroenterol. 2017;17:14. doi: 10.1186/s12876-016-0564-7.
    1. Brotherton C.S., Taylor A.G., Bourguignon C., Anderson J.G. A High Fiber Diet May Improve Bowel Function and Health-Related Quality of Life in Patients with Crohn’s Disease. Gastroenterol. Nurs. 2014;37:206–216. doi: 10.1097/SGA.0000000000000047.
    1. Olendzki B.C., Silverstein T.D., Persuitte G.M., Ma Y., Baldwin K.R., Cave D. An anti-inflammatory diet as treatment for inflammatory bowel disease: A case series report. Nutr. J. 2014;13:5. doi: 10.1186/1475-2891-13-5.
    1. Rajendran N., Kumar D. Food-specific IgG4-guided exclusion diets improve symptoms in Crohn’s disease: A pilot study. Colorectal Dis. 2011;13:1009–1013. doi: 10.1111/j.1463-1318.2010.02373.x.
    1. Obih C., Wahbeh G., Lee D., Braly K., Giefer M., Shaffer M.L., Nielson H., Suskind D.L. Specific carbohydrate diet for pediatric inflammatory bowel disease in clinical practice within an academic IBD center. Nutrition. 2016;32:418–425. doi: 10.1016/j.nut.2015.08.025.
    1. Prince A.C., Myers C.E., Joyce T., Irving P., Lomer M., Whelan K. Fermentable carbohydrate restriction (low FODMAP diet) in clinical practice improves functional gastrointestinal symptoms in patients with inflammatory bowel disease. Inflamm. Bowel Dis. 2016;22:1129–1136. doi: 10.1097/MIB.0000000000000708.
    1. Tóth C., Dabóczi A., Howard M., Miller N.J., Clemens Z. Crohn’s disease successfully treated with the paleolithic ketogenic diet. Int. J. Case Rep. Images. 2016;7:570–578. doi: 10.5348/ijcri-2016102-CR-10690.
    1. Berntson L., Agback P., Dicksved J. Changes in fecal microbiota and metabolomics in a child with juvenile idiopathic arthritis (JIA) responding to two treatment periods with exclusive enteral nutrition (EEN) Clin. Rheumatol. 2016;35:1501–1506. doi: 10.1007/s10067-016-3238-5.
    1. Berntson L., Hedlund-Treutiger I., Alving K. Anti-inflammatory effect of exclusive enteral nutrition in patients with juvenile idiopathic arthritis. Clin. Exp. Rheumatol. 2016;34:941–945.
    1. Suskind D.L., Cohen S.A., Brittnacher M.J., Wahbeh G., Lee D., Shaffer M.L., Braly K., Hayden H.S., Klein J., Gold B. Clinical and Fecal Microbial Changes with Diet Therapy in Active Inflammatory Bowel Disease. J. Clin. Gastroenterol. 2017 doi: 10.1097/MCG.0000000000000772.
    1. Barnes E.L., Nestor M., Onyewadume L., De Silva P., Korzenik J.R., Investigators D. High Dietary Intake of Specific Fatty Acids Increases Risk of Flares in Patients with Ulcerative Colitis in Remission During Treatment with Aminosalicylates. Clin. Gastroenterol. Hepatol. 2017;S1542–S3565:30051–30054. doi: 10.1016/j.cgh.2016.12.036.

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