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Review

Inflammatory bowel diseases: interrelationships between dietary vitamin D, exposure to UV radiation and the fecal microbiome

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Pages 1039-1048 | Received 14 Jun 2019, Accepted 23 Oct 2019, Published online: 07 Nov 2019

References

  • Wallace KL, Zheng LB, Kanazawa Y, et al. Immunopathology of inflammatory bowel disease. World J Gastroenterol. 2014;20(1):6–21.
  • Khalili H, Huang ES, Ananthakrishnan AN, et al. Geographical variation and incidence of inflammatory bowel disease among US women. Gut. 2012;61(12):1686–1692.
  • Gearry RB, Richardson A, Frampton CM, et al. High incidence of Crohn’s disease in Canterbury, New Zealand: results of an epidemiologic study. Inflamm Bowel Dis. 2006;12(10):936–943.
  • Loftus EV. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology. 2004;126(6):1504–1517.
  • Shivananda S, Lennard-Jones J, Logan R, et al. Incidence of inflammatory bowel disease across Europe: is there a difference between north and south? Results of the European Collaborative Study on Inflammatory Bowel Disease (EC-IBD). Gut. 1996;39(5):690–697.
  • Gower-Rousseau C, Salomez JL, Dupas JL, et al. Incidence of inflammatory bowel disease in northern France (1988–1990). Gut. 1994;35(10):1433–1438.
  • Sonnenberg A. Demographic characteristics of hospitalized IBD patients. Dig Dis Sci. 2009;54(11):2449–2455.
  • Nerich V, Monnet E, Etienne A, et al. Geographical variations of inflammatory bowel disease in France: a study based on national health insurance data. Inflamm Bowel Dis. 2006;12(3):218–226.
  • Jantchou P, Clavel-Chapelon F, Racine A, et al. High residential sun exposure is associated with a low risk of incident Crohn’s disease in the prospective E3N Cohort. Inflamm Bowel Dis. 2013;20:75–81.
  • Nerich V, Jantchou P, Boutron-Ruault M-C, et al. Low exposure to sunlight is a risk factor for Crohn’s disease. Aliment Pharmacol Ther. 2011;33(8):940–945.
  • Ghaly S, Lawrance I. The role of vitamin D in gastrointestinal inflammation. Expert Rev Gastroenterol Hepatol. 2014;8:1–15.
  • Hart PH, Norval M, Byrne SN, et al. Exposure to ultraviolet radiation in the modulation of human diseases. Annu Rev Pathol. 2019;14:55–81.
  • Ananthakrishnan AN, Khalili H, Higuchi LM, et al. Higher predicted vitamin D status is associated with reduced risk of Crohn’s disease. Gastroenterology. 2012;142(3):482–489.
  • Jørgensen SP, Hvas CL, Agnholt J, et al. Active Crohn’s disease is associated with low vitamin D levels. J Crohns Colitis. 2013;7(10):e407–e413.
  • Ulitsky A, Ananthakrishnan AN, Naik A, et al. Vitamin D deficiency in patients with inflammatory bowel disease: association with disease activity and quality of life. JPEN J Parenter Enteral Nutr. 2011;35(3):308–316.
  • Harries AD, Brown R, Heatley RV, et al. Vitamin D status in Crohn’s disease: association with nutrition and disease activity. Gut. 1985;26(11):1197–1203.
  • Ananthakrishnan AN, Cagan A, Gainer VS, et al. Normalization of plasma 25-hydroxy vitamin D is associated with reduced risk of surgery in Crohn’s disease. Inflamm Bowel Dis. 2013;19:1.
  • Ananthakrishnan AN, Cheng S-C, Cai T, et al. Association between reduced plasma 25-hydroxy vitamin D and increased risk of cancer in patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol. 2013;12:821–827.
  • Ahuja V, Tandon RK. Inflammatory bowel disease in the Asia-Pacific area: a comparison with developed countries and regional differences. J Dig Dis. 2010;11(3):134–147.
  • Ng WK, Wong SH, Ng SC. Changing epidemiological trends of inflammatory bowel disease in Asia. Intest Res. 2016;14(2):111–119.
  • McIlroy J, Ianiro G, Mukhopadhya I, et al. Review article: the gut microbiome in inflammatory bowel disease-avenues for microbial management. Aliment Pharmacol Ther. 2018;47(1):26–42.
  • Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.
  • Murphy K, Travers P, Walport M, et al. Janeway’s immunobiology. New York (NY): Garland Science; 2012.
  • Kahrstrom CT, Pariente N, Weiss U. Intestinal microbiota in health and disease. Nature. 2016;535(7610):47.
  • Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. 2014;146:1489–1499.
  • Forbes JD, Van Domselaar G, Bernstein CN. Microbiome survey of the inflamed and noninflamed gut at different compartments within the gastrointestinal tract of inflammatory bowel disease patients. Inflamm Bowel Dis. 2016;22(4):817–825.
  • Khan KJ, Ullman TA, Ford AC, et al. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol. 2011;106(4):661–673.
  • Harper PH, Lee EC, Kettlewell MG, et al. Role of the faecal stream in the maintenance of Crohn’s colitis. Gut. 1985;26(3):279–284.
  • Rutgeerts P, Goboes K, Peeters M, et al. Effect of faecal stream diversion on recurrence of Crohn’s disease in the neoterminal ileum. Lancet. 1991;338(8770):771–774.
  • Janowitz HD, Croen EC, Sachar DB. The role of the fecal stream in Crohn’s disease: an historical and analytic review. Inflamm Bowel Dis. 1998;4(1):29–39.
  • Paramsothy S, Kamm MA, Kaakoush NO, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389(10075):1218–1228.
  • Moayyedi P, Surette MG, Kim PT, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149(1):102–109 e106.
  • Costello SP, Hughes PA, Waters O, et al. Effect of fecal microbiota transplantation on 8-week remission in patients with ulcerative colitis: a randomized clinical trial. JAMA. 2019;321(2):156–164.
  • Manichanh 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(2):205–211.
  • Walker AW, Sanderson JD, Churcher C, et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol. 2011;11:7.
  • Swidsinski A, Weber J, Loening-Baucke V, et al. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol. 2005;43(7):3380–3389.
  • Pascal V, Pozuelo M, Borruel N, et al. A microbial signature for Crohn’s disease. Gut. 2017;66(5):813–822.
  • Hansen R, Russell RK, Reiff C, 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(12):1913–1922.
  • Lopez-Siles M, Khan TM, Duncan SH, et al. Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl Environ Microbiol. 2012;78(2):420–428.
  • Barnich N, Denizot J, Darfeuille-Michaud AE. coli-mediated gut inflammation in genetically predisposed Crohn’s disease patients. Pathol Biol. 2013;61(5):e65–e69.
  • Shaw KA, Bertha M, Hofmekler T, et al. Dysbiosis, inflammation, and response to treatment: a longitudinal study of pediatric subjects with newly diagnosed inflammatory bowel disease. Genome Med. 2016;8(1):75.
  • Ghaly S, Kaakoush NO, Lloyd F, et al. High dose vitamin D supplementation alters faecal microbiome and predisposes mice to more severe colitis. Sci Rep. 2018;8(1):11511.
  • Schirmer M, Franzosa EA, Lloyd-Price J, et al. Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat Microbiol. 2018;3(3):337–346.
  • Gevers D, Kugathasan S, Knights D, et al. A microbiome foundation for the study of Crohn’s disease. Cell Host Microbe. 2017;21(3):301–304.
  • Suskind DL, Cohen SA, Brittnacher MJ, et al. Clinical and fecal microbial changes with diet therapy in active inflammatory bowel disease. J Clin Gastroenterol. 2018;52(2):155–163.
  • Ananthakrishnan AN, Luo C, Yajnik V, et al. Gut microbiome function predicts response to anti-integrin biologic therapy in inflammatory bowel diseases. Cell Host Microbe. 2017;21(5):603–610 e603.
  • Ghaly S, Lawrance I. The role of vitamin D in gastrointestinal inflammation. Expert Rev Gastroenterol Hepatol. 2014;8(8):909–923.
  • Zhang Y-G, Wu S, Sun J. Vitamin D, vitamin D receptor, and tissue barriers. Tissue Barriers. 2013;1(1):e23118.
  • Kong J, Zhang Z, Musch MW, et al. Novel role of the vitamin D receptor in maintaining the integrity of the intestinal mucosal barrier. Am J Physiol Gastrointest Liver Physiol. 2008;294(1):G208–G216.
  • Zaiou M, Gallo RL. Cathelicidins, essential gene-encoded mammalian antibiotics. J Mol Med (Berl). 2002;80(9):549–561.
  • Penna G, Adorini L. 1 Alpha,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J Iimmunol. 2000;164(5):2405–2411.
  • Hewison M, Freeman L, Hughes SV, et al. Differential regulation of vitamin D receptor and its ligand in human monocyte-derived dendritic cells. J Iimmunol. 2003;170(11):5382–5390.
  • Bhalla AK, Amento EP, Clemens TL, et al. Specific high-affinity receptors for 1,25-dihydroxyvitamin D3 in human peripheral blood mononuclear cells: presence in monocytes and induction in T lymphocytes following activation. J Clin Endocrinol Metab. 1983;57(6):1308–1310.
  • Provvedini DM, Manolagas SC. 1 Alpha,25-dihydroxyvitamin D3 receptor distribution and effects in subpopulations of normal human T lymphocytes. J Clin Endocrinol Metab. 1989;68(4):774–779.
  • Waterhouse M, Hope B, Krause L, et al. Vitamin D and the gut microbiome: a systematic review of in vivo studies. Eur J Nutr. 2018;58:2895–2910.
  • Lagishetty V, Misharin AV, Liu NQ, et al. Vitamin D deficiency in mice impairs colonic antibacterial activity and predisposes to colitis. Endocrinology. 2010;151(6):2423–2432.
  • Assa A, Vong L, Pinnell LJ, et al. Vitamin D deficiency promotes epithelial barrier dysfunction and intestinal inflammation. J Infect Dis. 2014;210(8):1296–1305.
  • Ooi JH, Li Y, Rogers CJ, et al. Vitamin D regulates the gut microbiome and protects mice from dextran sodium sulfate-induced colitis. J Nutr. 2013;143(10):1679–1686.
  • Wu S, Zhang YG, Lu R, et al. Intestinal epithelial vitamin D receptor deletion leads to defective autophagy in colitis. Gut. 2015;64(7):1082–1094.
  • Santoru ML, Piras C, Murgia A, et al. Cross sectional evaluation of the gut-microbiome metabolome axis in an Italian cohort of IBD patients. Sci Rep. 2017;7(1):9523.
  • Schaffler H, Herlemann DP, Klinitzke P, et al. Vitamin D administration leads to a shift of the intestinal bacterial composition in Crohn’s disease patients, but not in healthy controls. J Dig Dis. 2018;19(4):225–234.
  • Garg M, Hendy P, Ding JN, et al. The effect of vitamin D on intestinal inflammation and faecal microbiota in patients with ulcerative colitis. J Crohns Colitis. 2018;12(8):963–972.
  • Bashir M, Prietl B, Tauschmann M, et al. Effects of high doses of vitamin D3 on mucosa-associated gut microbiome vary between regions of the human gastrointestinal tract. Eur J Nutr. 2015;55:1479–1489.
  • Kanhere M, He J, Chassaing B, et al. Bolus weekly vitamin D3 supplementation impacts gut and airway microbiota in adults with cystic fibrosis: a double-blind, randomized, placebo-controlled clinical trial. J Clin Endocrinol Metab. 2018;103(2):564–574.
  • Hollams EM, Teo SM, Kusel M, et al. Vitamin D over the first decade and susceptibility to childhood allergy and asthma. J Allergy Clin Immunol. 2017;139(2):472–481 e479.
  • Roggenbuck M, Anderson D, Barfod KK, et al. Vitamin D and allergic airway disease shape the murine lung microbiome in a sex-specific manner. Respir Res. 2016;17(1):116.
  • Bodnar LM, Krohn MA, Simhan HN. Maternal vitamin D deficiency is associated with bacterial vaginosis in the first trimester of pregnancy. J Nutr. 2009;139(6):1157–1161.
  • Cahill KC, Conroy FJ, Brown A, et al. Tuberculous dactylitis in the setting of low serum vitamin D: a case report. J Plast Reconstr Aesthet Surg. 2011;64(12):e321–e324.
  • Jefferson KK, Parikh HI, Garcia EM, et al. Relationship between vitamin D status and the vaginal microbiome during pregnancy. J Perinatol. 2019;39(6):824–836.
  • Bora SA, Kennett MJ, Smith PB, et al. Regulation of vitamin D metabolism following disruption of the microbiota using broad spectrum antibiotics. J Nutr Biochem. 2018;56:65–73.
  • Bora SA, Kennett MJ, Smith PB, et al. The gut microbiota regulates endocrine vitamin D metabolism through fibroblast growth factor 23. Front Immunol. 2018;9:408.
  • Lin YD, Arora J, Diehl K, et al. Vitamin D is required for ILC3 derived IL-22 and protection from citrobacter rodentium infection. Front Immunol. 2019;10:1.
  • Jantchou P, Clavel-Chapelon F, Racine A, et al. High residential sun exposure is associated with a low risk of incident Crohn’s disease in the prospective E3N cohort. Inflamm Bowel Dis. 2014;20(1):75–81.
  • Limketkai BN, Bayless TM, Brant SR, et al. Lower regional and temporal ultraviolet exposure is associated with increased rates and severity of inflammatory bowel disease hospitalisation. Aliment Pharmacol Ther. 2014;40(5):508–517.
  • Gorman S, Scott NM, Tan DHW, et al. Acute erythemal ultraviolet radiation causes systemic immunosuppression in the absence of increased 25-hydroxyvitamin D3 levels in male mice. PLoS One. 2012;7(9):e46006.
  • Hart PH, Gorman S, Finlay-Jones JJ. Modulation of the immune system by UV radiation: more than just the effects of vitamin D? Nat Rev Immunol. 2011;11(9):584–596.
  • Bernard JJ, Cowing-Zitron C, Nakatsuji T, et al. Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med. 2012;18(8):1286–1290.
  • Hart PH, Norval M. Ultraviolet radiation-induced immunosuppression and its relevance for skin carcinogenesis. Photochem Photobiol Sci. 2018;17(12):1872–1884.
  • Suwanpradid J, Holcomb ZE, MacLeod AS. Emerging skin T-cell functions in response to environmental insults. J Invest Dermatol. 2017;137(2):288–294.
  • Holliman G, Lowe D, Cohen H, et al. Ultraviolet radiation-induced production of nitric oxide: amulti-cell and multi-donor analysis. Sci Rep. 2017;7(1):11105.
  • Soontrapa K, Honda T, Sakata D, et al. Prostaglandin E2-prostaglandin E receptor subtype 4 (EP4) signaling mediates UV irradiation-induced systemic immunosuppression. Proc Natl Acad Sci USA. 2011;108(16):6668–6673.
  • Sheibanie AF, Yen J-H, Khayrullina T, et al. The proinflammatory effect of prostaglandin E2 in experimental inflammatory bowel disease is mediated through the IL-23–>IL-17 axis. J Iimmunol. 2007;178(12):8138–8147.
  • Baird AC, Lloyd F, Lawrance IC. Prostaglandin E(2) and polyenylphosphatidylcholine protect against intestinal fibrosis and regulate myofibroblast function. Dig Dis Sci. 2015;60(6):1603–1616.
  • Romano M, Machnicki G, Rojas JI, et al. There is much to be learnt about the costs of multiple sclerosis in Latin America. Arq Neuropsiquiatr. 2013;71(8):549–555.
  • Veldhoen M, Duarte JH. The aryl hydrocarbon receptor: fine-tuning the immune-response. Curr Opin Immunol. 2010;22(6):747–752.
  • Hiratsuka T, Inomata M, Goto S, et al. Phototherapy with artificial light suppresses dextran sulfate sodium-induced colitis in a mouse model. J Gastroenterol Hepatol. 2014;29(4):749–756.
  • Breuer J, Schwab N, Schneider-Hohendorf T, et al. Ultraviolet B light attenuates the systemic immune response in central nervous system autoimmunity. Ann Neurol. 2014;75(5):739–758.
  • Hiramoto K, Yamate Y, Sato EF. The effects of ultraviolet eye irradiation on dextran sodium sulfate-induced ulcerative colitis in mice. Photochem Photobiol. 2016;92(5):728–734.
  • Ghaly S, Kaakoush NO, Lloyd F, et al. Ultraviolet irradiation of skin alters the faecal microbiome independently of vitamin D in mice. Nutrients. 2018;10(8):1069.
  • Jeevan A, Evans R, Brown EL, et al. Effect of local ultraviolet irradiation on infections of mice with Candida albicans, mycobacterium bovis BCG, and schistosoma mansoni. J Invest Dermatol. 1992;99(1):59–64.
  • Cestari TF, Kripke ML, Baptista PL, et al. Ultraviolet radiation decreases the granulomatous response to lepromin in humans. J Invest Dermatol. 1995;105(1):8–13.
  • Brown EL, Ullrich SE, Pride M, et al. The effect of UV irradiation on infection of mice with Borrelia burgdorferi. Photochem Photobiol. 2001;73(5):537–544.
  • Glaser R, Navid F, Schuller W, et al. UV-B radiation induces the expression of antimicrobial peptides in human keratinocytes in vitro and in vivo. J Allergy Clin Immunol. 2009;123(5):1117–1123.
  • Burns EM, Ahmed H, Isedeh PN, et al. Ultraviolet radiation, both UVA and UVB, influences the composition of the skin microbiome. Exp Dermatol. 2019;28(2):136–141.
  • Sanford JA, Gallo RL. Functions of the skin microbiota in health and disease. Semin Immunol. 2013;25(5):370–377.
  • Kabbani TA, Koutroubakis IE, Schoen RE, et al. Association of vitamin D level with clinical status in inflammatory bowel disease: a 5-year longitudinal study. Am J Gastroenterol. 2016;111(5):712–719.
  • Ananthakrishnan AN, Cagan A, Gainer VS, et al. Normalization of plasma 25-hydroxy vitamin D is associated with reduced risk of surgery in Crohn’s disease. Inflamm Bowel Dis. 2013;19(9):1921–1927.
  • Opstelten JL, Chan SSM, Hart AR, et al. Prediagnostic serum vitamin D levels and the risk of Crohn’s disease and ulcerative colitis in European populations: a nested case-control study. Inflamm Bowel Dis. 2018;24(3):633–640.
  • Gubatan J, Mitsuhashi S, Zenlea T, et al. Low serum vitamin D during remission increases risk of clinical relapse in patients with ulcerative colitis. Clin Gastroenterol Hepatol. 2017;15(2):240–246 e241.
  • Ghaly S, Murray K, Baird A, et al. High vitamin D-binding protein concentration, low albumin, and mode of remission predict relapse in Crohn’s disease. Inflamm Bowel Dis. 2016;22(10):2456–2464.
  • Hanauer SB. Vitamin D levels and outcomes in inflammatory bowel disease-which is the chicken and which is the egg? Clin Gastroenterol Hepatol. 2017;15(2):247–248.
  • Garg M. Serum vitamin D and risk of clinical relapse in patients with ulcerative colitis. Clin Gastroenterol Hepatol. 2017;15(7):1136.
  • Jorgensen SP, Agnholt J, Glerup H, et al. Clinical trial: vitamin D3 treatment in Crohn’s disease - a randomized double-blind placebo-controlled study. Aliment Pharmacol Ther. 2010;32(3):377–383.
  • Tan B, Li P, Lv H, et al. Treatment of vitamin D deficiency in Chinese inflammatory bowel disease patients: A prospective, randomized, open-label, pilot study. J Dig Dis. 2018;19(4):215–224.
  • Narula N, Cooray M, Anglin R, et al. Impact of high-dose vitamin D3 supplementation in patients with Crohn’s disease in remission: a pilot randomized double-blind controlled study. Dig Dis Sci. 2017;62(2):448–455.
  • Li J, Chen N, Wang D, et al. Efficacy of vitamin D in treatment of inflammatory bowel disease: A meta-analysis. Medicine (Baltimore). 2018;97(46):e12662.
  • Nielsen OH, Rejnmark L, Moss AC. Role of vitamin D in the natural history of inflammatory Bowel disease. J Crohns Colitis. 2018;12(6):742–752.
  • Melamed ML, Michos ED, Post W, et al. 25-hydroxyvitamin D levels and the risk of mortality in the general population. Arch Internal Med. 2008;168(15):1629–1637.
  • Jia X, Aucott LS, McNeill G. Nutritional status and subsequent all-cause mortality in men and women aged 75 years or over living in the community. Br J Nutr. 2007;98(3):593–599.
  • Crockett SD, Barry EL, Mott LA, et al. Calcium and vitamin D supplementation and increased risk of serrated polyps: results from a randomised clinical trial. Gut. 2018;68:475–486.

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