Nutrition in IBD

  • Zubin Grover
  • Peter Lewindon


Malnutrition in inflammatory bowel disease (IBD) is related to reduced oral intake, malabsorption and catabolic stress due to inflammatory burden ultimately leading to loss of body form, composition and function. Malnutrition persists even when disease is in remission, and it is associated with increase in mortality, prolonged hospitalisations, post-operative complications, poor quality of life and greater health-care burden. There are multiple proxies of malnutrition, ranging from a simple bedside anthropometry and biochemistry to a more detailed body composition analysis. Anthropometry and biochemistry are practical and low-cost pragmatic malnutrition screening tools; however they cannot discriminate key body composition changes such as loss of lean body mass (LBM) or fat-free mass (FFM) and mesenteric fat deposition (MFD). These key body composition changes contribute to the higher inflammatory burden, poor therapeutic response to anti-TNFs and increased risk for intestinal surgery.

Treatments targets for IBD have also evolved with increasing emphasis on using therapies capable of inducing mucosal healing. Exclusive enteral nutrition (EEN) is the most well-established therapeutic diet in CD capable of inducing mucosal healing rates compared to conventional steroids. Concomitant use of partial enteral nutrition is also associated with reduction in loss of response to infliximab. There is also growing interest in anti-inflammatory exclusion diets to maintain remission, but robust endpoints like endoscopic remission are missing. Multiple serum and faecal biomarker studies have demonstrated anti-inflammatory effects of enteral diet, but the exact mechanism of action remains elusive. Modulation of microbiota and metabolomic changes following dietary elimination studies, more specifically in Crohn’s disease, have been tested in many recent studies; however these shifts do not establish a cause and effect relationship and may simply reflect functional gut adaptations due to changes in dietary substrates. As our understanding of the relationship between diet, nutrition and gut health evolves, we expect to see major advances in the role of dietary patterns and constituents in the development, treatment, cure and finally prevention of IBD.


  1. 1.
    Ng S, Bernstein C, Vatn M, et al. Geographical variability and environmental risk factors in inflammatory bowel disease. Gut. 2013;62:630–49.PubMedCrossRefGoogle Scholar
  2. 2.
    Casanova M, Chaparro M, Molina B, et al. Prevalence of malnutrition and nutritional characteristics of patients with inflammatory bowel disease. J Crohns Colitis. 2017;11:1430–9.PubMedCrossRefGoogle Scholar
  3. 3.
    Ananthakrishnan A, Khalili H, Konijeti G. A prospective study of long-term intake of dietary fibre and risk of Crohn’s disease and ulcerative colitis. Gastroenterology. 2013;145:970–7.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Jantchou P, Morois S, Clavel-Chapelon F, et al. Animal protein intake and risk of inflammatory bowel disease: the E3N prospective study. Am J Gastroenterol. 2010;105:2195.PubMedCrossRefGoogle Scholar
  5. 5.
    Ananthakrishnan A, Khalili H, Konijeti G, et al. Long-term intake of dietary fat and risk of ulcerative colitis and Crohn’s disease. Gut. 2014;63:776–84.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Devakota S, Wang Y, Musch M, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature. 2012;487:104–8.CrossRefGoogle Scholar
  7. 7.
    Chassaing B, Koren O, Goodrich J, et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature. 2015;519:92–6.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Chassaing B, Van de Wiele T, De Bodt J, et al. Dietary emulsifiers directly alter human microbiota composition and gene expression ex vivo potentiating intestinal inflammation. Gut. 2017;66:1414–27.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Valentini L, Schulzke J. Mundane, yet challenging: the assessment of malnutrition in inflammatory bowel disease. Eur J Intern Med. 2011;22:13–5.PubMedCrossRefGoogle Scholar
  10. 10.
    Dietitians Association of Australia. Evidence-based practice guidelines for the nutritional management of malnutrition in adult patients across the continuum of care. Nutr Diet. 2009;66(3 Suppl):S1–4.Google Scholar
  11. 11.
    Vasseur F, Gower-Rousseau C, Vernier-Massouille G, et al. Nutritional status and growth in pediatric Crohn’s disease: a population-based study. Am J Gastroenterol. 2010;105:1893–900 10.PubMedCrossRefGoogle Scholar
  12. 12.
    Valentini L, Schaper L, Buning C, et al. Malnutrition and impaired muscle strength in patients with Crohn’s disease and ulcerative colitis in remission. Nutrition. 2008;24:694–702.PubMedCrossRefGoogle Scholar
  13. 13.
    Bryant R, Trott M, Bartholomesusz F, et al. Systematic review: body composition in adults with inflammatory bowel disease. Aliment Pharmacol Ther. 2013;38:213–25.PubMedCrossRefGoogle Scholar
  14. 14.
    Thayu M, Denson L, Shunlts J, et al. Determinants of changes in linear growth and body composition in incident pediatric Crohn’s disease. Gastroenterology. 2010;139(2):430–8.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Tinsley A, Ehrlich O, Hwang C, et al. Knowledge, attitudes, and beliefs regarding the role of nutrition in ibd among patients and providers. Inflamm Bowel Dis. 2016;22:2474.PubMedCrossRefGoogle Scholar
  16. 16.
    Nguyen G, Munsell M, Harris M, et al. Nationwide prevalence and prognostic significance of clinically diagnosable protein-calorie malnutrition in hospitalized inflammatory bowel disease patients. Inflamm Bowel Dis. 2008;14:1105–11.PubMedCrossRefGoogle Scholar
  17. 17.
    Fasanmade A, Adedokun O, Blank M, et al. Pharmacokinetic properties of infliximab in children and adults with Crohn’s disease: a retrospective analysis of data from 2 phase III clinical trials. Clin Ther. 2011;33:946–64.PubMedCrossRefGoogle Scholar
  18. 18.
    Fasanmade A, Adedokun O, Olson A, et al. Serum albumin concentration: a predictive factor of infliximab pharmacokinetics and clinical response in patients with ulcerative colitis. Int J Clin Pharmacol Ther. 2010;48:297–308.PubMedCrossRefGoogle Scholar
  19. 19.
    Arias M, Vande Casteele N, Vermeire S, et al. A panel to predict long term outcomes of infliximab therapy for patients with ulcerative colitis. Clin Gastroenterol Hepatol. 2015;13(3):531–8.PubMedCrossRefGoogle Scholar
  20. 20.
    Brandse J, van den Brink G, Wildenberg M, et al. Loss of infliximab into feces is associated with lack of response to therapy in patients with severe ulcerative colitis. Gastroenterology. 2015;149(2):350–5.PubMedCrossRefGoogle Scholar
  21. 21.
    Van Langenberg D, Delta Gatta P, Wamington S, et al. Objectively measured muscle fatigue in Crohn’s disease: correlation with self-reported fatigue and associated factors for clinical application. J Crohns Colitis. 2014;8:137–46.Google Scholar
  22. 22.
    Zhang T, Ding C, Xie T, et al. Skeletal muscle depletion correlates with disease activity in ulcerative colitis and reverses after colectomy. Clin Nutr. 2017;36:1586–92.PubMedCrossRefGoogle Scholar
  23. 23.
    Bamba S, Sasaki M, Takaoka K, et al. Sarcopenia is a predictive factor for intestinal resection in admitted patients with Crohn’s disease. PLoS One. 2017;12:e0180036.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Holt D, Varma P, Strauss B, et al. Low muscle mass at initiation of anti-TNF therapy for inflammatory bowel disease is associated with early treatment failure: a retrospective analysis. Eur J Clin Nutr. 2017;71:773–7.PubMedCrossRefGoogle Scholar
  25. 25.
    Ding N, Malietzis G, Lung P, et al. The body composition profile is associated with response to anti-TNF therapy in Crohn’s disease and may offer alternative dosing paradigm. Aliment Pharmacol Ther. 2017;46:883–91.PubMedCrossRefGoogle Scholar
  26. 26.
    Zulian A, Cancello R, Micheletto G, et al. Visceral adipocytes: old actors in obesity and new protagonists in Crohn’s disease? Gut. 2012;61:86–94.PubMedCrossRefGoogle Scholar
  27. 27.
    Peyrin-Biroulet L, Gonzalez F, Dubuquoy L, et al. Mesenteric fat as a source of C reactive protein and a target for bacterial translocation in Crohn’s disease. Gut. 2012;61:78–85.PubMedCrossRefGoogle Scholar
  28. 28.
    Connelly T, Juza R, Sangster W, et al. Volumetric fat ratio and not body mass index is predictive of ileocolectomy outcomes in Crohn’s disease patients. Dig Surg. 2014;31:219–24.PubMedCrossRefGoogle Scholar
  29. 29.
    Ding Z, Wu X, Remer E, et al. Association between high visceral fat area and postoperative complications in patients with Crohn’s disease following primary surgery. Color Dis. 2016;18:163–72.PubMedCrossRefGoogle Scholar
  30. 30.
    Erhayiem B, Dhingsa R, Hawkey C, et al. Ratio of visceral to subcutaneous fat area is a biomarker of complicated Crohn’s disease. Clin Gastroenterol Hepatol. 2011;9:684–7.PubMedCrossRefGoogle Scholar
  31. 31.
    Uko V, Vortia E, Achkar J, et al. Impact of abdominal visceral adipose tissue on disease outcome in pediatric Crohn’s disease. Inflamm Bowel Dis. 2014;20:2286–91.PubMedCrossRefGoogle Scholar
  32. 32.
    Van Der Sloot K, Joshi A, Bellavance D, et al. Visceral adiposity, genetic susceptibility, and risk of complications among individuals with Crohn’s disease. Inflamm Bowel Dis. 2017;23:82–8.Google Scholar
  33. 33.
    Voitk AJ, Echave V, Feller JH, et al. Experience with elemental diet in the treatment of inflammatory bowel disease. Is this primary therapy? Arch Surg. 1973;107:329–33.PubMedCrossRefGoogle Scholar
  34. 34.
    Bury D, Stephens V, Randall T, et al. Use of a chemically defined, liquid, elemental diet for nutritional management of fistulas of the alimentary tract. Am J Surg. 1971;121(2):174–83.PubMedCrossRefGoogle Scholar
  35. 35.
    Ludvigsson JF, Krantz M, Bodin L, et al. Elemental versus polymeric enteral nutrition in paediatric Crohn’s disease: a multicentre randomized controlled trial. Acta Paediatr. 2004;93:327–35.CrossRefGoogle Scholar
  36. 36.
    Rodrigues AF, Johnson T, Davies P, et al. Does polymeric formula improve adherence to liquid diet therapy in children with active Crohn’s disease? Arch Dis Child. 2007;92:767–70.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Akobeng AK, Miller V, Stanton J, et al. Double-blind randomized controlled trial of glutamine-enriched polymeric diet in the treatment of active Crohn’s disease. J Pediatr Gastroenterol Nutr. 2000;30:78–84.PubMedCrossRefGoogle Scholar
  38. 38.
    Gorard DA, Hunt JB, Payne-James JJ, et al. Initial response and subsequent course of Crohn’s disease treated with elemental diet or prednisolone. Gut. 1993;34:1198–202.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Zachos M, Tondeur M, Griffiths A. Enteral nutritional therapy for induction of remission in Crohn’s disease. Cochrane Database Syst Rev. 2007;1:CD000542.Google Scholar
  40. 40.
    Day AS, Whitten KE, Sidler M, Lemberg DA. Systematic review: nutritional therapy in paediatric Crohn’s disease. Aliment Pharmacol Ther. 2008;27:293–307.CrossRefGoogle Scholar
  41. 41.
    Dziechciarz P, Horvath A, Shamir R, Szajewska H. Meta-analysis: enteral nutrition in active Crohn’s disease in children. Aliment Pharmacol Ther. 2007;26:795–806.PubMedCrossRefGoogle Scholar
  42. 42.
    Swaminath A, Feathers A, Ananthakrishnan A, et al. Systematic review with meta-analysis: enteral nutrition therapy for the induction of remission in paediatric Crohn’s disease. Aliment Pharmacol Ther. 2017;46:645–56.CrossRefGoogle Scholar
  43. 43.
    Cohen-Dolev N, Sladek M, Hussey S, et al. Differences in outcomes over time with exclusive enteral nutrition compared to steroids in children with mild to moderate Crohn’s Disease: results from the GROWTH CD study. J Crohns Colitis. 2018;12(3):306–12.PubMedCrossRefGoogle Scholar
  44. 44.
    Borrelli O, Cordischi L, Cirulli M, et al. Polymeric diet alone versus corticosteroids in the treatment of active pediatric Crohn’s disease: a randomized controlled open label trial. Clin Gastroenterol Hepatol. 2006;4:744–53.PubMedCrossRefGoogle Scholar
  45. 45.
    Yamamoto T, Nakahigashi M, Umegae S, et al. Impact of elemental diet on mucosal inflammation in patients with active Crohn’s disease: cytokine production and endoscopic and histological findings. Inflamm Bowel Dis. 2005;11:580–8.PubMedCrossRefGoogle Scholar
  46. 46.
    Grover Z, Muir R, Lewindon P, et al. Exclusive enteral nutrition induced early clinical, mucosal and transmural remission in paediatric Crohn’s disease. J Gastroenterol. 2014;49(4):638–45.PubMedCrossRefGoogle Scholar
  47. 47.
    Grover Z, Burgess C, Muir R, et al. Early mucosal healing with Exclusive Enteral Nutrition is associated with improved outcomes in newly diagnosed children with luminal Crohn’s disease. J Crohns Colitis. 2016;10:1159–64.PubMedCrossRefGoogle Scholar
  48. 48.
    Heerasing N, Thompson B, Hendy P, et al. Exclusive enteral nutrition provides an effective bridge to safer interval elective surgery for adults with Crohn’s disease. Aliment Pharmacol Ther. 2017;45:660–9.CrossRefGoogle Scholar
  49. 49.
    Verma S, Kirkwood B, Brown S, et al. Oral nutritional supplementation is effective in the maintenance of remission in Crohn’s disease. Dig Liver Dis. 2000;32:769–74.PubMedCrossRefGoogle Scholar
  50. 50.
    Takagi S, Utsunomiya K, Kuriyama S, et al. Effectiveness of an ‘half elemental diet’ as maintenance therapy for Crohn’s disease: a randomized-controlled trial. Aliment Pharmacol Ther. 2006;24:1333–40.PubMedCrossRefGoogle Scholar
  51. 51.
    Yamamoto T, Nakahigashi M, Saniabadi A, et al. Impacts of long-term enteral nutrition on clinical and endoscopic disease activities and mucosal cytokines during remission in patients with Crohn’s disease: a prospective study. Inflamm Bowel Dis. 2007;13(12):1493–501.PubMedCrossRefGoogle Scholar
  52. 52.
    Ding N, Hart A, De Cruz P. Systematic review: predicting and optimising response to antiTNF therapy in Crohn’s disease – algorithm for practical management. Aliment Pharmacol Ther. 2016;43:30–51.CrossRefGoogle Scholar
  53. 53.
    Sazuka S, Katsuno T, Nakagawa T, et al. Concomitant use of enteral nutrition therapy is associated with sustained response to infliximab in patients with Crohn’s disease. Eur J Clin Nutr. 2012;66:1219–23.PubMedCrossRefGoogle Scholar
  54. 54.
    Hirai F, Ishihara H, Yada S, et al. Effectiveness of concomitant enteral nutrition therapy and infliximab for maintenance treatment of Crohn’s disease in adults. Dig Dis Sci. 2013;58:1329–34.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Nguyen D, Palmer L, Nguyen E, et al. Specialized enteral nutrition therapy in Crohn’s disease patients on maintenance infliximab therapy: a meta-analysis. Ther Adv Gastroenterol. 2015;8:168–75.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Yamamoto T, Shiraki M, Nakahigashi M, et al. Enteral nutrition to suppress postoperative Crohn’s disease recurrence: a five-year prospective cohort study. Int J Color Dis. 2013;28(3):335–40.PubMedCrossRefGoogle Scholar
  57. 57.
    Yamamoto T, Nakahigashi M, Umegae S, et al. Impact of long-term enteral nutrition on clinical and endoscopic recurrence after resection for Crohn’s disease: a prospective, non-randomized, parallel, controlled study. Aliment Pharmacol Ther. 2007;25(1):67–72.CrossRefGoogle Scholar
  58. 58.
    Gupta K, Noble A, Kachelries K, et al. A novel enteral nutrition protocol for the treatment of pediatric Crohn’s disease. Inflamm Bowel Dis. 2013;19:1374–8.PubMedCrossRefGoogle Scholar
  59. 59.
    Lee D, Baldassano R, Otley A, et al. Comparative effectiveness of nutritional and biological therapy in north american children with active Crohn’s disease. Inflamm Bowel Dis. 2015;21:1786–93.PubMedCrossRefGoogle Scholar
  60. 60.
    Svolos V, Hansen R, Nichols B, et al. Treatment of active Crohn’s disease with an ordinary food-based diet that replicates exclusive enteral nutrition. Gastroenterology. 2018; Scholar
  61. 61.
    Sigall-Boneh R, Pfeffer-Gik T, Segal I, et al. 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;20:1353–60.Google Scholar
  62. 62.
    Sigall-Boneh R, Sarbagili S, Yanai H, et al. Dietary therapy with the Crohn’s disease Exclusion diet is a successful strategy for induction of remission in Children and Adults failing biological therapy. J Crohns Colitis. 2017;11:1205–12.PubMedCrossRefGoogle Scholar
  63. 63.
    Cohen S, Gold B, Oliva S, et al. Clinical and mucosal improvement with specific carbohydrate diet in pediatric Crohn disease. J Pediatr Gastroenterol Nutr. 2014;59:516–21.PubMedCrossRefGoogle Scholar
  64. 64.
    Obih C, Wahbeh G, Lee D, et al. Specific carbohydrate diet for pediatric inflammatory bowel disease in clinical practice within an academic IBD center. Nutrition. 2016;32:418–25.PubMedCrossRefGoogle Scholar
  65. 65.
    Wahbeh G, Ward B, Lee D, et al. Lack of Mucosal Healing From Modified Specific Carbohydrate Diet in Pediatric Patients With Crohn Disease. J Pediatr Gastroenterol Nutr. 2017;65:289–92.PubMedCrossRefGoogle Scholar
  66. 66.
    Wang G, Ren J, Li G, et al. The utility of food antigen test in the diagnosis of Crohn’s disease and remission maintenance after exclusive enteral nutrition. Clin Res Hepatol Gastroenterol. 2018;42(2):145–52. pii: S2210–7401.PubMedCrossRefGoogle Scholar
  67. 67.
    Prince A, Myers C, Joyce T, et al. Fermentable carbohydrate restriction (low FODMAP diet) in clinical practice improves functional gastrointestinal symptoms in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2016;22(5):1129–36.PubMedCrossRefGoogle Scholar
  68. 68.
    Ruuska T, Savilahti E, Maki M, et al. Exclusive whole protein enteral diet versus prednisolone in the treatment of acute Crohn’s disease in children. J Pediatr Gastroenterol Nutr. 1994;19(2):175–80.PubMedCrossRefGoogle Scholar
  69. 69.
    Fell JM, Paintin M, Arnaud-Battandier F, et al. Mucosal healing and a fall in mucosal pro-inflammatory cytokine mRNA induced by a specific oral polymeric diet in paediatric Crohn’s disease. Aliment Pharmacol Ther. 2000;14(3):281–9.PubMedCrossRefGoogle Scholar
  70. 70.
    Knight C, El-Matary W, Spray C, et al. Long-term outcome of nutritional therapy in paediatric Crohn’s disease. Clin Nutr. 2005;24:775–9.PubMedCrossRefGoogle Scholar
  71. 71.
    Bannerjee K, Camacho-Hubner C, Babinska K, et al. Anti-inflammatory and growth stimulating effects precede nutritional restitution during enteral feeding in Crohn disease. J Pediatr Gastroenterol Nutr. 2004;38:270–5.PubMedCrossRefGoogle Scholar
  72. 72.
    Meister D, Bode J, Shand A, Ghosh S. Anti-inflammatory effects of enteral diet components on Crohn’s disease-affected tissues in vitro. Dig Liver Dis. 2002;34:430–8.PubMedCrossRefGoogle Scholar
  73. 73.
    De Jong N, Leach S, Day A. Polymeric formula has direct anti-inflammatory effects on enterocytes in an in vitro model of intestinal inflammation. Dig Dis Sci. 2007;52:2029–36.PubMedCrossRefGoogle Scholar
  74. 74.
    Schoepfer AM, Beglinger C, Straumann A, et al. Fecal calprotectin correlates more closely with the Simple Endoscopic Score for Crohn’s disease (SES-CD) than CRP, blood leukocytes, and the CDAI. Am J Gastroenterol. 2010;105(1):162–9.PubMedCrossRefGoogle Scholar
  75. 75.
    Roseth AG, Aadland E, Grzyb K. Normalization of faecal calprotectin: a predictor of mucosal healing in patients with inflammatory bowel disease. Scand J Gastroenterol. 2004;39(10):1017–20.PubMedCrossRefGoogle Scholar
  76. 76.
    D’Haens G, Ferrante M, Vermeire S, et al. Fecal calprotectin is a surrogate marker for endoscopic lesions in inflammatory bowel disease. Inflamm Bowel Dis. 2012;18:2218–24.CrossRefGoogle Scholar
  77. 77.
    Molander P, af Björkesten CG, et al. Fecal calprotectin concentration predicts outcome in inflammatory bowel disease after induction therapy with TNF[alpha] blocking agents. Inflamm Bowel Dis. 2012;18:2011–7.PubMedCrossRefGoogle Scholar
  78. 78.
    Gerasimidis K, Nikolaou C, Edwards C, et al. Serial fecal calprotectin changes in children with Crohn’s disease on treatment with exclusive enteral nutrition: associations with disease activity, treatment response, and prediction of a clinical relapse. J Clin Gastroenterol. 2011;45(3):234–9.Google Scholar
  79. 79.
    Frivolt K, Schwerd T, Werkstetter KJ, et al. Repeated exclusive enteral nutrition in the treatment of paediatric Crohn’s disease: predictors of efficacy and outcome. Aliment Pharmacol Ther. 2014;39:1398–407.PubMedCrossRefGoogle Scholar
  80. 80.
    Grogan JL, Casson DH, Terry A, et al. Enteral feeding therapy for newly diagnosed pediatric Crohn’s disease: a double-blind randomized controlled trial with two years follow-up. Inflamm Bowel Dis. 2012;18:246–53.PubMedCrossRefGoogle Scholar
  81. 81.
    Levine A, Turner D, Pfeffer Gik T, 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 out- comes with therapy” (GROWTH CD) study. Inflamm Bowel Dis. 2014;20:278–85.PubMedCrossRefGoogle Scholar
  82. 82.
    Zubin G, Peter L. Predicting endoscopic Crohn’s disease activity before and after induction therapy in children: a comprehensive assessment of PCDAI, CRP, and fecal calprotectin. Inflamm Bowel Dis. 2015;21:1386–91.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Matsuoka K, Kanai T. The gut microbiota and inflammatory bowel disease. Semin Immunopathol. 2015;37:47–55.PubMedCrossRefGoogle Scholar
  84. 84.
    Pascal V, Pozuelo M, Borruel N, et al. A microbial signatures for Crohn’s disease. Gut. 2017;66:813–22.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Gevers D, Kugathasan S, et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe. 2014;15(3):382–92.Google Scholar
  86. 86.
    Bornside G, Cohn I Jr. Stability of normal human fecal flora during a chemically defined, low residue liquid diet. Ann Surg. 1975;181(1):58–60.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Wensinck F, Custers-van Lieshout LMC, Poppelaars-Kustermans P, et al. Stability of normal human fecal flora during a chemically defined, low residue liquid diet The faecal flora of patients with Crohn’s disease. J Hyg (Lond). 1981;87(1):1–12.Google Scholar
  88. 88.
    Tannock GW. New perceptions of the gut microbiota: implications for future research. Gastroenterol Clin N Am. 2005;34(3):361–8.CrossRefGoogle Scholar
  89. 89.
    Kaakoush N, Day A, et al. Effect of exclusive enteral nutrition on the microbiota of children with newly diagnosed Crohn’s disease. Clin Transl Gastroenterol. 2015;15:e71.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Schwerd T, Frivolt K, Clavel T, et al. Exclusive Enteral Nutrition in active pediatric Crohn’s disease: effects on intestinal microbiota and immune regulation. J Allergy Clin Immunol. 2016;138:592–6.PubMedCrossRefGoogle Scholar
  91. 91.
    Lewis J, Chen E, Baldassano R, 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.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Dunn K, Moore-Connors J, MacIntyre B, et al. Early changes in microbial community structure are associated with sustained remission after nutritional treatment of pediatric Crohn’s disease. Inflamm Bowel Dis. 2016;22:2853–286.PubMedCrossRefGoogle Scholar
  93. 93.
    Jia W, Whitehead R, Griffiths L, et al. Is the abundance of Faecalibacterium prausnitzii relevant to Crohn’s disease? FEMS Microbiol Lett. 2010;310:138–44.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Gerasimidis K, Bertz M, 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;20:861–71.PubMedCrossRefGoogle Scholar
  95. 95.
    Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci. 2008;105(43):16731–6.PubMedCrossRefGoogle Scholar
  96. 96.
    D’Argenio V, Precone V, et al. An altered gut microbiome profile in a child affected by Crohn’s disease normalized after nutritional therapy. Am J Gastroenterol. 2013;108:851–2.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Grover Z, Kang A, Morrison M, Radford Smith GL, Fukuma NM, Simms LA, Lewindon PJ. The relative abundances of Dorea and Faecalibacterium spp. in the mucosa associated microbiome of newly diagnosed children with Crohn’s disease are differentially affected by exclusive enteral nutrition. Gastroenterology. 2016;150(4):S132–3.CrossRefGoogle Scholar
  98. 98.
    Lionetti P, Callegari ML, Ferrari S, et al. Enteral nutrition and microflora in pediatric Crohn’s disease. JPEN J Parenter Enteral Nutr. 2005;29:S173–5.PubMedCrossRefGoogle Scholar
  99. 99.
    Leach ST, Mitchell HM, Eng WR, et al. Sustained modulation of intestinal bacteria by exclusive enteral nutrition used to treat children with Crohn’s disease. Aliment Pharmacol Ther. 2008;28(6):724–33.CrossRefGoogle Scholar
  100. 100.
    Quince C, Ijaz U, et al. Extensive modulation of the fecal metagenome in children with Crohn’s disease during exclusive enteral nutrition. Am J Gastroenterol. 2015;110:1718–29.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Zoetendal EG, von Wright A, Vilpponen-Salmela T, et al. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol. 2002;68:3401–7.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Leung K, Sharp P. MicroRNA functions in stress responses. Mol Cell. 2010;22:205–15.CrossRefGoogle Scholar
  103. 103.
    Yang Y, Ma Y, Shi C, et al. Overexpression of miR-21 in patients with ulcerative colitis impairs intestinal epithelial barrier function through targeting the Rho GTPase RhoB. Biochem Biophys Res Commun. 2013;434:746–52.PubMedCrossRefGoogle Scholar
  104. 104.
    Shi C, Liang Y, Yang J, Xia Y, et al. MicroRNA-21 knockout improve the survival rate in DSS induced fatal colitis through protecting against inflammation and tissue injury. PLoS One. 2013;8:e66814.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Chen Y, Xiao Y, Ge W, et al. miR-200b inhibits TGF-β1-induced epithelial-mesenchymal transition and promotes growth of intestinal epithelial cells. Cell Death Dis. 2013;4:e541.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Zhai Z, Wu F, Chuang A, et al. miR-106b fine tunes ATG16L1 expression and autophagic activity in intestinal epithelial HCT116 cells. Inflamm Bowel Dis. 2013;19:2295–301.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Lu C, Chen J, Xu HG, Zhou X, et al. MIR106B and MIR93 prevent removal of bacteria from epithelial cells by disrupting ATG16L1-mediated autophagy. Gastroenterology. 2014;146:188–99.PubMedCrossRefGoogle Scholar
  108. 108.
    Nguyen HT, Dalmasso G, Müller S, et al. Crohn’s disease-associated adherent invasive Escherichia coli modulate levels of microRNAs in intestinal epithelial cells to reduce autophagy. Gastroenterology. 2014;146:508–19.PubMedCrossRefGoogle Scholar
  109. 109.
    Feng X, Wang H, Ye S, et al. Up-regulation of microRNA-126 may contribute to pathogenesis of ulcerative colitis via regulating NF-kappaB inhibitor IκBα. PLoS One. 2012;7:e52782.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Chuang AY, Chuang JC, Zhai Z, et al. NOD2 expression is regulated by microRNAs in colonic epithelial HCT116 cells. Inflamm Bowel Dis. 2014;20:126–35.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Slattery M, Herrick J, Mullany L, et al. Diet and lifestyle factors associated with miRNA expression in colorectal tissue. Pharmagenomics Pers Med. 2017;10:1–16.Google Scholar
  112. 112.
    Guo Z, Gong J, Li Y, et al. Mucosal microRNAs expression profiles before and after exclusive enteral nutrition therapy in adult patients with Crohn’s disease. Nutrients. 2016;22:8.Google Scholar
  113. 113.
    Sigall-Boneh R, Levine A, Lomer M, et al. Research gaps in diet and nutrition in inflammatory bowel disease. a topical review by D-ECCO working group [Dietitians of ECCO]. JCC. 2017;12:1407–19.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Zubin Grover
    • 1
  • Peter Lewindon
    • 2
  1. 1.Princess Margaret Hospital for ChildrenPerthAustralia
  2. 2.Lady Cilento Children’s HospitalSouth BrisbaneAustralia

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