Advertisement

Use of Probiotics to Prevent Celiac Disease and IBD in Pediatrics

  • Gloria SerenaEmail author
  • Alessio Fasano
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1125)

Abstract

The incidence of chronic inflammatory diseases (CIDs) is increasing worldwide. Their dramatic rise associated with limited effective strategies to slow down these epidemics calls for a better understanding of their pathophysiology in order to decrease the burdens on childhood. Several cross-sectional studies have demonstrated the association between intestinal dysbiosis and active diseases. Although informative, these studies do not mechanistically link alterations of the microflora with disease pathogenesis and, therefore, with potential therapeutic targets. More prospective studies are needed to determine whether intestinal dysbiosis plays a causative role in the onset and development of CIDs. Furthermore, given the complexity of the microflora interaction with the host, it is necessary to design a systems-level model of interactions between the host and the development of disease by integrating microbiome, metagenomics, metatranscriptomics, and metabolomics with either clinical either environmental data.

In this chapter we will discuss the current knowledge regarding the microbiome’s contribution to celiac disease and inflammatory bowel disease with a particular focus on how probiotics may be used as potential preventive therapy for CIDs.

Keywords

Celiac disease Inflammatory bowel diseases Microbiome Microbiota Probiotics 

References

  1. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J (2014) The placenta harbors a unique microbiome. Sci Transl Med 6:237ra65PubMedPubMedCentralGoogle Scholar
  2. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL, Investigators CS (2013) Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 185:385–394PubMedPubMedCentralGoogle Scholar
  3. Bach JF (2002) The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 347:911–920PubMedGoogle Scholar
  4. Barclay AR, Morrison DJ, Weaver LT (2008) What is the role of the metabolic activity of the gut microbiota in inflammatory bowel disease? Probing for answers with stable isotopes. J Pediatr Gastroenterol Nutr 46:486–495PubMedGoogle Scholar
  5. Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, De Simone C, Sartor RB (2005) VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100:1539–1546PubMedGoogle Scholar
  6. Butterworth AD, Thomas AG, Akobeng AK (2008) Probiotics for induction of remission in Crohn’s disease. Cochrane Database Syst Rev 3:CD006634Google Scholar
  7. Chassaing B, Darfeuille-Michaud A (2011) The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology 140:1720–1728PubMedGoogle Scholar
  8. Corridoni D, Arseneau KO, Cifone MG, Cominelli F (2014) The dual role of nod-like receptors in mucosal innate immunity and chronic intestinal inflammation. Front Immunol 5:317PubMedPubMedCentralGoogle Scholar
  9. Costeloe K, Hardy P, Juszczak E, Wilks M, Millar MR, Probiotics in Preterm Infants Study Collaborative, G (2016) Bifidobacterium breve BBG-001 in very preterm infants: a randomised controlled phase 3 trial. Lancet 387:649–660PubMedGoogle Scholar
  10. De Angelis M, Rizzello CG, Fasano A, Clemente MG, De Simone C, Silano M, De Vincenzi M, Losito I, Gobbetti M (2006) VSL#3 probiotic preparation has the capacity to hydrolyze gliadin polypeptides responsible for Celiac Sprue. Biochim Biophys Acta 1762:80–93PubMedGoogle Scholar
  11. Di Cagno R, De Angelis M, De Pasquale I, Ndagijimana M, Vernocchi P, Ricciuti P, Gagliardi F, Laghi L, Crecchio C, Guerzoni ME, Gobbetti M, Francavilla R (2011) Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization. BMC Microbiol 11:219PubMedPubMedCentralGoogle Scholar
  12. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 107:11971–11975PubMedPubMedCentralGoogle Scholar
  13. Drago S, El Asmar R, Di Pierro M, Grazia Clemente M, Tripathi A, Sapone A, Thakar M, Iacono G, Carroccio A, D’agate C, Not T, Zampini L, Catassi C, Fasano A (2006) Gliadin, zonulin and gut permeability: effects on celiac and non-celiac intestinal mucosa and intestinal cell lines. Scand J Gastroenterol 41:408–419PubMedGoogle Scholar
  14. Eastaff-Leung N, Mabarrack N, Barbour A, Cummins A, Barry S (2010) Foxp3+ regulatory T cells, Th17 effector cells, and cytokine environment in inflammatory bowel disease. J Clin Immunol 30:80–89PubMedGoogle Scholar
  15. Escudero-Hernandez C, Plaza-Izurieta L, Garrote JA, Bilbao JR, CEGEC, Arranz E (2017) Association of the IL-15 and IL-15Ralpha genes with celiac disease. Cytokine 99:73–79PubMedGoogle Scholar
  16. Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder MJ, Valles-Colomer M, Vandeputte D, Tito RY, Chaffron S, Rymenans L, Verspecht C, De Sutter L, Lima-Mendez G, D’hoe K, Jonckheere K, Homola D, Garcia R, Tigchelaar EF, Eeckhaudt L, Fu J, Henckaerts L, Zhernakova A, Wijmenga C, Raes J (2016) Population-level analysis of gut microbiome variation. Science 352:560–564PubMedGoogle Scholar
  17. Fasano A (2011) Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer. Physiol Rev 91:151–175PubMedGoogle Scholar
  18. Fiorucci S, Distrutti E, Mencarelli A, Barbanti M, Palazzini E, Morelli A (2002) Inhibition of intestinal bacterial translocation with rifaximin modulates lamina propria monocytic cells reactivity and protects against inflammation in a rodent model of colitis. Digestion 66:246–256PubMedGoogle Scholar
  19. Francavilla R, De Angelis M, Rizzello CG, Cavallo N, Dal Bello F, Gobbetti M (2017) Selected probiotic lactobacilli have the capacity to hydrolyze gluten peptides during simulated gastrointestinal digestion. Appl Environ Microbiol 83(14):e00376–e00317PubMedPubMedCentralGoogle Scholar
  20. Fujimori S, Tatsuguchi A, Gudis K, Kishida T, Mitsui K, Ehara A, Kobayashi T, Sekita Y, Seo T, Sakamoto C (2007) High dose probiotic and prebiotic cotherapy for remission induction of active Crohn’s disease. J Gastroenterol Hepatol 22:1199–1204PubMedGoogle Scholar
  21. Furrie E, Macfarlane S, Kennedy A, Cummings JH, Walsh SV, O’Neil DA, Macfarlane GT (2005) Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial. Gut 54:242–249PubMedPubMedCentralGoogle Scholar
  22. Garrote JA, Gomez-Gonzalez E, Bernardo D, Arranz E, Chirdo F (2008) Celiac disease pathogenesis: the proinflammatory cytokine network. J Pediatr Gastroenterol Nutr 47(Suppl 1):S27–S32PubMedGoogle Scholar
  23. Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van Treuren W, Ren B, Schwager E, Knights D, Song SJ, Yassour M, Morgan XC, Kostic AD, Luo C, Gonzalez A, Mcdonald D, Haberman Y, Walters T, Baker S, Rosh J, Stephens M, Heyman M, Markowitz J, Baldassano R, Griffiths A, Sylvester F, Mack D, Kim S, Crandall W, Hyams J, Huttenhower C, Knight R, Xavier RJ (2014) The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe 15:382–392PubMedPubMedCentralGoogle Scholar
  24. Granzotto M, Dal Bo S, Quaglia S, Tommasini A, Piscianz E, Valencic E, Ferrara F, Martelossi S, Ventura A, Not T (2009) Regulatory T-cell function is impaired in celiac disease. Dig Dis Sci 54:1513–1519PubMedGoogle Scholar
  25. Greenwood BM (1968) Autoimmune disease and parasitic infections in Nigerians. Lancet 2:380–382PubMedGoogle Scholar
  26. Gupta P, Andrew H, Kirschner BS, Guandalini S (2000) Is lactobacillus GG helpful in children with Crohn’s disease? Results of a preliminary, open-label study. J Pediatr Gastroenterol Nutr 31:453–457PubMedGoogle Scholar
  27. Ishikawa H, Akedo I, Umesaki Y, Tanaka R, Imaoka A, Otani T (2003) Randomized controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis. J Am Coll Nutr 22:56–63PubMedGoogle Scholar
  28. Jeon SG, Kayama H, Ueda Y, Takahashi T, Asahara T, Tsuji H, Tsuji NM, Kiyono H, Ma JS, Kusu T, Okumura R, Hara H, Yoshida H, Yamamoto M, Nomoto K, Takeda K (2012) Probiotic Bifidobacterium breve induces IL-10-producing Tr1 cells in the colon. PLoS Pathog 8:e1002714PubMedPubMedCentralGoogle Scholar
  29. Kaplan GG (2015) The global burden of IBD: from 2015 to 2025. Nat Rev Gastroenterol Hepatol 12:720–727PubMedGoogle Scholar
  30. Kato K, Mizuno S, Umesaki Y, Ishii Y, Sugitani M, Imaoka A, Otsuka M, Hasunuma O, Kurihara R, Iwasaki A, Arakawa Y (2004) Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis. Aliment Pharmacol Ther 20:1133–1141PubMedGoogle Scholar
  31. Khor B, Gardet A, Xavier RJ (2011) Genetics and pathogenesis of inflammatory bowel disease. Nature 474:307–317PubMedPubMedCentralGoogle Scholar
  32. Lammers KM, Lu R, Brownley J, Lu B, Gerard C, Thomas K, Rallabhandi P, Shea-Donohue T, Tamiz A, Alkan S, Netzel-Arnett S, Antalis T, Vogel SN, Fasano A (2008) Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology 135:194–204 e3PubMedPubMedCentralGoogle Scholar
  33. Lammers KM, Khandelwal S, Chaudhry F, Kryszak D, Puppa EL, Casolaro V, Fasano A (2011) Identification of a novel immunomodulatory gliadin peptide that causes interleukin-8 release in a chemokine receptor CXCR3-dependent manner only in patients with coeliac disease. Immunology 132:432–440PubMedPubMedCentralGoogle Scholar
  34. Lammers KM, Chieppa M, Liu L, Liu S, Omatsu T, Janka-Junttila M, Casolaro V, Reinecker HC, Parent CA, Fasano A (2015) Gliadin induces neutrophil migration via engagement of the formyl peptide receptor, FPR1. PLoS One 10:e0138338PubMedPubMedCentralGoogle Scholar
  35. Laparra JM, Sanz Y (2010) Bifidobacteria inhibit the inflammatory response induced by gliadins in intestinal epithelial cells via modifications of toxic peptide generation during digestion. J Cell Biochem 109:801–807PubMedGoogle Scholar
  36. Lees CW, Satsangi J (2009) Genetics of inflammatory bowel disease: implications for disease pathogenesis and natural history. Expert Rev Gastroenterol Hepatol 3:513–534PubMedGoogle Scholar
  37. Leonard MM, Camhi S, Huedo-Medina TB, Fasano A (2015a) Celiac disease genomic, environmental, microbiome, and metabolomic (CDGEMM) study design: approach to the future of personalized prevention of celiac disease. Nutrients 7:9325–9336PubMedPubMedCentralGoogle Scholar
  38. Leonard MM, Serena G, Sturgeon C, Fasano A (2015b) Genetics and celiac disease: the importance of screening. Expert Rev Gastroenterol Hepatol 9:209–215PubMedGoogle Scholar
  39. Lindfors K, Blomqvist T, Juuti-Uusitalo K, Stenman S, Venalainen J, Maki M, Kaukinen K (2008) Live probiotic Bifidobacterium lactis bacteria inhibit the toxic effects induced by wheat gliadin in epithelial cell culture. Clin Exp Immunol 152:552–558PubMedPubMedCentralGoogle Scholar
  40. Lionetti E, Castellaneta S, Francavilla R, Pulvirenti A, Tonutti E, Amarri S, Barbato M, Barbera C, Barera G, Bellantoni A, Castellano E, Guariso G, Limongelli MG, Pellegrino S, Polloni C, Ughi C, Zuin G, Fasano A, Catassi C, Weaning SWGO, Risk CD (2014) Introduction of gluten, HLA status, and the risk of celiac disease in children. N Engl J Med 371:1295–1303PubMedGoogle Scholar
  41. Madsen K, Cornish A, Soper P, Mckaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121:580–591PubMedGoogle Scholar
  42. Maiuri L, Ciacci C, Auricchio S, Brown V, Quaratino S, Londei M (2000) Interleukin 15 mediates epithelial changes in celiac disease. Gastroenterology 119:996–1006PubMedGoogle Scholar
  43. Malamut G, El Machhour R, Montcuquet N, Martin-Lanneree S, Dusanter-Fourt I, Verkarre V, Mention JJ, Rahmi G, Kiyono H, Butz EA, Brousse N, Cellier C, Cerf-Bensussan N, Meresse B (2010) IL-15 triggers an antiapoptotic pathway in human intraepithelial lymphocytes that is a potential new target in celiac disease-associated inflammation and lymphomagenesis. J Clin Invest 120:2131–2143PubMedPubMedCentralGoogle Scholar
  44. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55:205–211PubMedPubMedCentralGoogle Scholar
  45. Manichanh C, Borruel N, Casellas F, Guarner F (2012) The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol 9:599–608PubMedGoogle Scholar
  46. Michail S, Durbin M, Turner D, Griffiths AM, Mack DR, Hyams J, Leleiko N, Kenche H, Stolfi A, Wine E (2012) Alterations in the gut microbiome of children with severe ulcerative colitis. Inflamm Bowel Dis 18:1799–1808PubMedGoogle Scholar
  47. Miele E, Pascarella F, Giannetti E, Quaglietta L, Baldassano RN, Staiano A (2009) Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am J Gastroenterol 104:437–443PubMedGoogle Scholar
  48. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, Leleiko N, Snapper SB, Bousvaros A, Korzenik J, Sands BE, Xavier RJ, Huttenhower C (2012) Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 13:R79PubMedPubMedCentralGoogle Scholar
  49. Negroni A, Costanzo M, Vitali R, Superti F, Bertuccini L, Tinari A, Minelli F, Di Nardo G, Nuti F, Pierdomenico M, Cucchiara S, Stronati L (2012) Characterization of adherent-invasive Escherichia coli isolated from pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis 18:913–924PubMedGoogle Scholar
  50. Oliva S, Di Nardo G, Ferrari F, Mallardo S, Rossi P, Patrizi G, Cucchiara S, Stronati L (2012) Randomised clinical trial: the effectiveness of Lactobacillus reuteri ATCC 55730 rectal enema in children with active distal ulcerative colitis. Aliment Pharmacol Ther 35:327–334PubMedGoogle Scholar
  51. Olivares M, Neef A, Castillejo G, Palma GD, Varea V, Capilla A, Palau F, Nova E, Marcos A, Polanco I, Ribes-Koninckx C, Ortigosa L, Izquierdo L, Sanz Y (2015) The HLA-DQ2 genotype selects for early intestinal microbiota composition in infants at high risk of developing coeliac disease. Gut 64:406–417PubMedGoogle Scholar
  52. Olivares M, Benitez-Paez A, De Palma G, Capilla A, Nova E, Castillejo G, Varea V, Marcos A, Garrote JA, Polanco I, Donat E, Ribes-Koninckx C, Calvo C, Ortigosa L, Palau F, Sanz Y (2018) Increased prevalence of pathogenic bacteria in the gut microbiota of infants at risk of developing celiac disease: the PROFICEL study. Gut Microbes 9(6):551–558PubMedPubMedCentralGoogle Scholar
  53. Orel R, Kamhi Trop T (2014) Intestinal microbiota, probiotics and prebiotics in inflammatory bowel disease. World J Gastroenterol 20:11505–11524PubMedPubMedCentralGoogle Scholar
  54. Orholm M, Binder V, Sorensen TI, Rasmussen LP, Kyvik KO (2000) Concordance of inflammatory bowel disease among Danish twins. Results of a nationwide study. Scand J Gastroenterol 35:1075–1081PubMedGoogle Scholar
  55. Orlando A, Linsalata M, Notarnicola M, Tutino V, Russo F (2014) Lactobacillus GG restoration of the gliadin induced epithelial barrier disruption: the role of cellular polyamines. BMC Microbiol 14:19PubMedPubMedCentralGoogle Scholar
  56. Palmer C, Bik EM, Digiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177PubMedPubMedCentralGoogle Scholar
  57. Primec M, Micetic-Turk D, Langerholc T (2017) Analysis of short-chain fatty acids in human feces: a scoping review. Anal Biochem 526:9–21PubMedGoogle Scholar
  58. Reilly NR, Fasano A, Green PH (2012) Presentation of celiac disease. Gastrointest Endosc Clin N Am 22:613–621PubMedGoogle Scholar
  59. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl JP, Ricciardi-Castagnoli P (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2:361–367PubMedGoogle Scholar
  60. Rizzello CG, De Angelis M, Di Cagno R, Camarca A, Silano M, Losito I, De Vincenzi M, De Bari MD, Palmisano F, Maurano F, Gianfrani C, Gobbetti M (2007) Highly efficient gluten degradation by lactobacilli and fungal proteases during food processing: new perspectives for celiac disease. Appl Environ Microbiol 73:4499–4507PubMedPubMedCentralGoogle Scholar
  61. Rosenstiel P, Sina C, End C, Renner M, Lyer S, Till A, Hellmig S, Nikolaus S, Folsch UR, Helmke B, Autschbach F, Schirmacher P, Kioschis P, Hafner M, Poustka A, Mollenhauer J, Schreiber S (2007) Regulation of DMBT1 via NOD2 and TLR4 in intestinal epithelial cells modulates bacterial recognition and invasion. J Immunol 178:8203–8211PubMedGoogle Scholar
  62. Sarno M, Lania G, Cuomo M, Nigro F, Passannanti F, Budelli A, Fasano F, Troncone R, Auricchio S, Barone MV, Nigro R, Nanayakkara M (2014) Lactobacillus paracasei CBA L74 interferes with gliadin peptides entrance in Caco-2 cells. Int J Food Sci Nutr 65:953–959PubMedGoogle Scholar
  63. Schultz M, Timmer A, Herfarth HH, Sartor RB, Vanderhoof JA, Rath HC (2004) Lactobacillus GG in inducing and maintaining remission of Crohn’s disease. BMC Gastroenterol 4:5PubMedPubMedCentralGoogle Scholar
  64. Schuppan D (2000) Current concepts of celiac disease pathogenesis. Gastroenterology 119:234–242PubMedGoogle Scholar
  65. Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P, Jian R, Dore J (2003) Alterations of the dominant faecal bacterial groups in patients with Crohn’s disease of the colon. Gut 52:237–242PubMedPubMedCentralGoogle Scholar
  66. Sellitto M, Bai G, Serena G, Fricke WF, Sturgeon C, Gajer P, White JR, Koenig SS, Sakamoto J, Boothe D, Gicquelais R, Kryszak D, Puppa E, Catassi C, Ravel J, Fasano A (2012) Proof of concept of microbiome-metabolome analysis and delayed gluten exposure on celiac disease autoimmunity in genetically at-risk infants. PLoS One 7:e33387PubMedPubMedCentralGoogle Scholar
  67. Serena G, Yan S, Camhi S, Patel S, Lima RS, Sapone A, Leonard MM, Mukherjee R, Nath BJ, Lammers KM, Fasano A (2017) Proinflammatory cytokine interferon-gamma and microbiome-derived metabolites dictate epigenetic switch between forkhead box protein 3 isoforms in coeliac disease. Clin Exp Immunol 187:490–506PubMedPubMedCentralGoogle Scholar
  68. Steed H, Macfarlane GT, Blackett KL, Bahrami B, Reynolds N, Walsh SV, Cummings JH, Macfarlane S (2010) Clinical trial: the microbiological and immunological effects of synbiotic consumption – a randomized double-blind placebo-controlled study in active Crohn’s disease. Aliment Pharmacol Ther 32:872–883PubMedGoogle Scholar
  69. Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299:1259–1260PubMedPubMedCentralGoogle Scholar
  70. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening-Baucke V, Ortner M, Weber J, Hoffmann U, Schreiber S, Dietel M, Lochs H (2002) Mucosal flora in inflammatory bowel disease. Gastroenterology 122:44–54PubMedGoogle Scholar
  71. Thompson NP, Driscoll R, Pounder RE, Wakefield AJ (1996) Genetics versus environment in inflammatory bowel disease: results of a British twin study. BMJ 312:95–96PubMedPubMedCentralGoogle Scholar
  72. Tjellstrom B, Hogberg L, Stenhammar L, Falth-Magnusson K, Magnusson KE, Norin E, Sundqvist T, Midtvedt T (2013) Faecal short-chain fatty acid pattern in childhood coeliac disease is normalised after more than one year’s gluten-free diet. Microb Ecol Health Dis 24:1–5Google Scholar
  73. Tripathi A, Lammers KM, Goldblum S, Shea-Donohue T, Netzel-Arnett S, Buzza MS, Antalis TM, Vogel SN, Zhao A, Yang S, Arrietta MC, Meddings JB, Fasano A (2009) Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proc Natl Acad Sci U S A 106:16799–16804PubMedPubMedCentralGoogle Scholar
  74. Tursi A, Brandimarte G, Papa A, Giglio A, Elisei W, Giorgetti GM, Forti G, Morini S, Hassan C, Pistoia MA, Modeo ME, Rodino S, D’amico T, Sebkova L, Sacca N, Di Giulio E, Luzza F, Imeneo M, Larussa T, Di Rosa S, Annese V, Danese S, Gasbarrini A (2010) Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: a double-blind, randomized, placebo-controlled study. Am J Gastroenterol 105:2218–2227PubMedPubMedCentralGoogle Scholar
  75. Versini M, Jeandel PY, Bashi T, Bizzaro G, Blank M, Shoenfeld Y (2015) Unraveling the hygiene hypothesis of helminthes and autoimmunity: origins, pathophysiology, and clinical applications. BMC Med 13:81PubMedPubMedCentralGoogle Scholar
  76. Vicario M, Blanchard C, Stringer KF, Collins MH, Mingler MK, Ahrens A, Putnam PE, Abonia JP, Santos J, Rothenberg ME (2010) Local B cells and IgE production in the oesophageal mucosa in eosinophilic oesophagitis. Gut 59:12–20PubMedGoogle Scholar
  77. Vriezinga SL, Auricchio R, Bravi E, Castillejo G, Chmielewska A, Crespo Escobar P, Kolacek S, Koletzko S, Korponay-Szabo IR, Mummert E, Polanco I, Putter H, Ribes-Koninckx C, Shamir R, Szajewska H, Werkstetter K, Greco L, Gyimesi J, Hartman C, Hogen Esch C, Hopman E, Ivarsson A, Koltai T, Koning F, Martinez-Ojinaga E, Te Marvelde C, Pavic A, Romanos J, Stoopman E, Villanacci V, Wijmenga C, Troncone R, Mearin ML (2014) Randomized feeding intervention in infants at high risk for celiac disease. N Engl J Med 371:1304–1315PubMedGoogle Scholar
  78. Wacklin P, Kaukinen K, Tuovinen E, Collin P, Lindfors K, Partanen J, Maki M, Matto J (2013) The duodenal microbiota composition of adult celiac disease patients is associated with the clinical manifestation of the disease. Inflamm Bowel Dis 19:934–941PubMedGoogle Scholar
  79. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Jarnerot G, Tysk C, Jansson JK, Engstrand L (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139(1844–1854):e1Google Scholar
  80. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227PubMedPubMedCentralGoogle Scholar
  81. Zheng B, Van Bergenhenegouwen J, Overbeek S, Van De Kant HJ, Garssen J, Folkerts G, Vos P, Morgan ME, Kraneveld AD (2014) Bifidobacterium breve attenuates murine dextran sodium sulfate-induced colitis and increases regulatory T cell responses. PLoS One 9:e95441PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Mucosal Immunology and Biology Research Center and Division of Pediatric Gastroenterology and NutritionMassachusetts General Hospital for Children – Harvard Medical SchoolBostonUSA

Personalised recommendations