Gut Microbiota and Celiac Disease

Digestive Diseases and Sciences

Volumn 61, Issue 6, 2016, Pages 1461-1472

  Marasco, Giovanni ^a   Di Biase, Anna Rita ^b   Schiumerini, Ramona ^a   Eusebi, Leonardo Henry ^a   Iughetti, Lorenzo ^b   Ravaioli, Federico ^a   Scaioli, Eleonora ^a   Colecchia, Antonio ^a   Festi, Davide ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Celiac disease; Dysbiosis; Gluten free diet; Gut microbiota; Probiotic

Indexed keywords

HLA DQ2 ANTIGEN; HLA DQ8 ANTIGEN; PROBIOTIC AGENT;

ADAPTIVE IMMUNITY; BACTERIAL STRAIN; BACTERIUM CULTURE; CELIAC DISEASE; DUODENUM MUCOSA; DYSBIOSIS; FECES MICROFLORA; GENETIC PREDISPOSITION; GLUTEN FREE DIET; HAPLOTYPE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; BACTERIUM; CLASSIFICATION; GASTROINTESTINAL TRACT; INFLAMMATION; METABOLISM; MICROBIOLOGY;

BACTERIA; CELIAC DISEASE; GASTROINTESTINAL TRACT; HUMANS; INFLAMMATION;

EID: 84952659994     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-015-4020-2     Document Type: Review

References (102)

1. Festi D, Schiumerini R, Eusebi LH, Marasco G, Taddia M, Colecchia A. Gut microbiota and metabolic syndrome. World J Gastroenterol. 2014;20:16079–16094.
2. Collado MC, Calabuig M, Sanz Y. Differences between the fecal microbiota of coeliac infants and healthy controls. Curr Issues Intest Microbiol. 2007;8:9–14.
3. Szebeni B, Veres G, Dezsofi A, et al. Increased mucosal expression of Toll-like receptor (TLR)2 and TLR4 in coeliac disease. J Pediatr Gastroenterol Nutr. 2007;45:187–193.
4. Husby S, Koletzko S, Korponay-Szabó IR, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guidelines for the diagnosis of coeliac disease. J Pediatr Gastroenterol Nutr. 2012;54:136–160.
5. Rubio-Tapia A, Hill ID, Kelly CP, Calderwood AH, Murray JA. ACG clinical guidelines: diagnosis and management of celiac disease. Am J Gastroenterol. 2013;108:656–676. (quiz 677).
6. Fasano A, Catassi C. Clinical practice. Celiac disease. N Engl J Med. 2012;367:2419–2426.
7. Guandalini S, Assiri A. Celiac disease: a review. JAMA Pediatr. 2014;168:272–278.
8. Harris LA, Park JY, Voltaggio L, Lam-Himlin D. Celiac disease: clinical, endoscopic, and histopathologic review. Gastrointest Endosc. 2012;76:625–640.
9. Schuppan D, Junker Y, Barisani D. Celiac disease: from pathogenesis to novel therapies. Gastroenterology. 2009;137:1912–1933.
10. Abadie V, Sollid LM, Barreiro LB, Jabri B. Integration of genetic and immunological insights into a model of celiac disease pathogenesis. Annu Rev Immunol. 2011;29:493–525.
11. Pender SL, Tickle SP, Docherty AJ, Howie D, Wathen NC, MacDonald TT. A major role for matrix metalloproteinases in T cell injury in the gut. J Immunol. 1997;158:1582–1590.
12. Daum S, Bauer U, Foss HD, et al. Increased expression of mRNA for matrix metalloproteinases-1 and -3 and tissue inhibitor of metalloproteinases-1 in intestinal biopsy specimens from patients with coeliac disease. Gut. 1999;44:17–25.
13. Ciccocioppo R, Di Sabatino A, Bauer M, et al. Matrix metalloproteinase pattern in celiac duodenal mucosa. Lab Invest. 2005;85:397–407.
14. Green PHR, Jabri B. Coeliac disease. Lancet. 2003;362:383–391.
15. Maiuri L, Ciacci C, Ricciardelli I, et al. Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. Lancet. 2003;362:30–37.
16. Londei M, Ciacci C, Ricciardelli I, Vacca L, Quaratino S, Maiuri L. Gliadin as a stimulator of innate responses in celiac disease. Mol Immunol. 2005;42:913–918.
17. Lammers KM, Lu R, Brownley J, et al. Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology. 2008;135:e3.
18. Thomas KE, Sapone A, Fasano A, Vogel SN. Gliadin stimulation of murine macrophage inflammatory gene expression and intestinal permeability are MyD88-dependent: role of the innate immune response in Celiac disease. J Immunol. 2006;176:2512–2521.
19. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9:313–323.
20. Meresse B, Cerf-Bensussan N. Innate T cell responses in human gut. Semin Immunol. 2009;21:121–129.
21. Palmer E. The generation of T cell tolerance. Swiss Med Wkly. 2007;137:99S–100S.
22. Sharma R, Young C, Neu J. Molecular modulation of intestinal epithelial barrier: contribution of microbiota. J Biomed Biotechnol. 2010;2010:305879.
23. Nagler-Anderson C. Man the barrier! Strategic defences in the intestinal mucosa. Nat Rev Immunol. 2001;1:59–67.
24. Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C. Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol. 2012;8:36–45.
25. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA. 2002;99:15451–15455.
26. Pace NR. A molecular view of microbial diversity and the biosphere. Science. 1997;276:734–740.
27. Rondon MR, August PR, Bettermann AD, et al. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol. 2000;66:2541–2547.
28. Hamady M, Knight R. Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res. 2009;19:1141–1152.
29. Greco L, Romino R, Coto I, et al. The first large population based twin study of coeliac disease. Gut. 2002;50:624–628.
30. Ivarsson A, Myléus A, Norström F, et al. Prevalence of childhood celiac disease and changes in infant feeding. Pediatrics. 2013;131:e687–e694.
31. Norris JM, Barriga K, Hoffenberg EJ, et al. Risk of celiac disease autoimmunity and timing of gluten introduction in the diet of infants at increased risk of disease. JAMA. 2005;293:2343–2351.
32. Lionetti E, Castellaneta S, Francavilla R, et al. Introduction of gluten, HLA status, and the risk of celiac disease in children. N Engl J Med. 2014;371:1295–1303.
33. Vriezinga SL, Auricchio R, Bravi E, et al. Randomized feeding intervention in infants at high risk for celiac disease. N Engl J Med. 2014;371:1304–1315.
34. Myléus A, Hernell O, Gothefors L, et al. Early infections are associated with increased risk for celiac disease: an incident case-referent study. BMC Pediatr. 2012;12:194.
35. Collado MC, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. J Clin Pathol. 2009;62:264–269.
36. De Palma G, Nadal I, Medina M, et al. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol. 2010;10:63.
37. Stene LC, Honeyman MC, Hoffenberg EJ, et al. Rotavirus infection frequency and risk of celiac disease autoimmunity in early childhood: a longitudinal study. Am J Gastroenterol. 2006;101:2333–2340.
38. Pavone P, Nicolini E, Taibi R, Ruggieri M. Rotavirus and celiac disease. Am J Gastroenterol. 1831;2007:102.
39. Decker E, Engelmann G, Findeisen A, et al. Cesarean delivery is associated with celiac disease but not inflammatory bowel disease in children. Pediatrics. 2010;125:e1433–e1440.
40. Mårild K, Stephansson O, Montgomery S, Murray JA, Ludvigsson JF. Pregnancy outcome and risk of celiac disease in offspring: a nationwide case-control study. Gastroenterology. 2012;142:e3.
41. Lasa J, Zubiaurre I, Dima G, Peralta D, Soifer L. Helicobacter pylori prevalence in patients with celiac disease: results from a cross-sectional study. Arq Gastroenterol. 2015;52:139–142.
42. Lebwohl B, Blaser MJ, Ludvigsson JF, et al. Decreased risk of celiac disease in patients with Helicobacter pylori colonization. Am J Epidemiol. 2013;178:1721–1730.
43. Simondi D, Ribaldone DG, Bonagura GA, et al. Helicobacter pylori in celiac disease and in duodenal intraepithelial lymphocytosis: active protagonist or innocent bystander? Clin Res Hepatol Gastroenterol. 2015;39:740–745.
44. Jozefczuk J, Bancerz B, Walkowiak M, et al. Prevalence of Helicobacter pylori infection in pediatric celiac disease. Eur Rev Med Pharmacol Sci. 2015;19:2031–2035.
45. Cinova J, De Palma G, Stepankova R, et al. Role of intestinal bacteria in gliadin-induced changes in intestinal mucosa: study in germ-free rats. PLoS One. 2011;6:e16169.
46. Laparra JM, Olivares M, Gallina O, Sanz Y. Bifidobacterium longum CECT 7347 modulates immune responses in a gliadin-induced enteropathy animal model. PLoS One. 2012;7:e30744.
47. Papista C, Gerakopoulos V, Kourelis A, et al. Gluten induces coeliac-like disease in sensitised mice involving IgA, CD71 and transglutaminase 2 interactions that are prevented by probiotics. Lab Invest. 2012;92:625–635.
48. D’Arienzo R, Stefanile R, Maurano F, et al. Immunomodulatory effects of Lactobacillus casei administration in a mouse model of gliadin-sensitive enteropathy. Scand J Immunol. 2011;74:335–341.
49. Sanz Y, Sánchez E, Marzotto M, Calabuig M, Torriani S, Dellaglio F. Differences in faecal bacterial communities in coeliac and healthy children as detected by PCR and denaturing gradient gel electrophoresis. FEMS Immunol Med Microbiol. 2007;51:562–568.
50. Nistal E, Caminero A, Vivas S, et al. Differences in faecal bacteria populations and faecal bacteria metabolism in healthy adults and celiac disease patients. Biochimie. 2012;94:1724–1729.
51. Tjellström B, Stenhammar L, Högberg L, et al. Gut microflora associated characteristics in children with celiac disease. Am J Gastroenterol. 2005;100:2784–2788.
52. Sánchez E, Ribes-Koninckx C, Calabuig M, Sanz Y. Intestinal Staphylococcus spp. and virulent features associated with coeliac disease. J Clin Pathol. 2012;65:830–834.
53. Chiba M, Hoshina S, Kono M, et al. Staphylococcus aureus in inflammatory bowel disease. Scand J Gastroenterol. 2001;36:615–620.
54. Nguyen GC, Patel H, Chong RY. Increased prevalence of and associated mortality with methicillin-resistant Staphylococcus aureus among hospitalized IBD patients. Am J Gastroenterol. 2010;105:371–377.
55. Ong PY, Patel M, Ferdman RM, Dunaway T, Church JA. Association of staphylococcal superantigen-specific immunoglobulin e with mild and moderate atopic dermatitis. J Pediatr. 2008;153:803–806.
56. Garza-González E, Morfín-Otero R, Llaca-Díaz JM, Rodriguez-Noriega E. Staphylococcal cassette chromosome mec (SCC mec) in methicillin-resistant coagulase-negative staphylococci. A review and the experience in a tertiary-care setting. Epidemiol Infect. 2010;138:645–654.
57. Olivares M, Neef A, Castillejo G, et al. The HLA-DQ2 genotype selects for early intestinal microbiota composition in infants at high risk of developing coeliac disease. Gut. 2015;64:406–417.
58. Nadal I, Donat E, Donant E, Ribes-Koninckx C, Calabuig M, Sanz Y. Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J Med Microbiol. 2007;56:1669–1674.
59. Sánchez E, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Intestinal Bacteroides species associated with coeliac disease. J Clin Pathol. 2010;63:1105–1111.
60. Nistal E, Caminero A, Herrán AR, et al. Differences of small intestinal bacteria populations in adults and children with/without celiac disease: effect of age, gluten diet, and disease. Inflamm Bowel Dis. 2012;18:649–656.
61. Sánchez E, Donat E, Ribes-Koninckx C, Fernández-Murga ML, Sanz Y. Duodenal-mucosal bacteria associated with celiac disease in children. Appl Environ Microbiol. 2013;79:5472–5479.
62. Ou G, Hedberg M, Hörstedt P, et al. Proximal small intestinal microbiota and identification of rod-shaped bacteria associated with childhood celiac disease. Am J Gastroenterol. 2009;104:3058–3067.
63. Forsberg G, Fahlgren A, Hörstedt P, Hammarström S, Hernell O, Hammarström M-L. Presence of bacteria and innate immunity of intestinal epithelium in childhood celiac disease. Am J Gastroenterol. 2004;99:894–904.
64. Wacklin P, Kaukinen K, Tuovinen E, et al. The duodenal microbiota composition of adult celiac disease patients is associated with the clinical manifestation of the disease. Inflamm Bowel Dis. 2013;19:934–941.
65. Kalliomäki M, Satokari R, Lähteenoja H, et al. Expression of microbiota, Toll-like receptors, and their regulators in the small intestinal mucosa in celiac disease. J Pediatr Gastroenterol Nutr. 2012;54:727–732.
66. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012;489:231–241.
67. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol. 2010;10:131–144.
68. Collado MC, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Imbalances in faecal and duodenal Bifidobacterium species composition in active and non-active coeliac disease. BMC Microbiol. 2008;8:232.
69. Di Cagno R, De Angelis M, De Pasquale I, et al. Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization. BMC Microbiol. 2011;11:219.
70. Golfetto L, de Senna FD, Hermes J, Beserra BTS, França FDS, Martinello F. Lower bifidobacteria counts in adult patients with celiac disease on a gluten-free diet. Arq Gastroenterol. 2014;51:139–143.
71. De Meij TGJ, Budding AE, Grasman ME, Kneepkens CMF, Savelkoul PHM, Mearin ML. Composition and diversity of the duodenal mucosa-associated microbiome in children with untreated coeliac disease. Scand J Gastroenterol. 2013;48:530–536.
72. De Palma G, Nadal I, Collado MC, Sanz Y. Effects of a gluten-free diet on gut microbiota and immune function in healthy adult human subjects. Br J Nutr. 2009;102:1154–1160.
73. Jackson FW. Effects of a gluten-free diet on gut microbiota and immune function in healthy adult human subjects—comment by Jackson. Br J Nutr. 2010;104:773.
74. Moshfegh AJ, Friday JE, Goldman JP, Ahuja JK. Presence of inulin and oligofructose in the diets of Americans. J Nutr. 1999;129:1407S–1411S.
75. Van Loo J, Coussement P, de Leenheer L, Hoebregs H, Smits G. On the presence of inulin and oligofructose as natural ingredients in the western diet. Crit Rev Food Sci Nutr. 1995;35:525–552.
76. Di Cagno R, Rizzello CG, Gagliardi F, et al. Different fecal microbiotas and volatile organic compounds in treated and untreated children with celiac disease. Appl Environ Microbiol. 2009;75:3963–3971.
77. Schippa S, Iebba V, Barbato M, et al. A distinctive “microbial signature” in celiac pediatric patients. BMC Microbiol. 2010;10:175.
78. Wacklin P, Laurikka P, Lindfors K, et al. Altered duodenal microbiota composition in celiac disease patients suffering from persistent symptoms on a long-term gluten-free diet. Am J Gastroenterol. 2014;109:1933–1941.
79. Marasco G, Colecchia A, Festi D. Dysbiosis in Celiac disease patients with persistent symptoms on gluten-free diet: a condition similar to that present in irritable bowel syndrome patients? Am J Gastroenterol. 2015;110:598.
80. Roma E, Roubani A, Kolia E, Panayiotou J, Zellos A, Syriopoulou VP. Dietary compliance and life style of children with coeliac disease. J Hum Nutr Diet. 2010;23:176–182.
81. Sonti R, Green PHR. Celiac disease: obesity in celiac disease. Nat Rev Gastroenterol Hepatol. 2012;9:247–248.
82. Kabbani TA, Goldberg A, Kelly CP, et al. Body mass index and the risk of obesity in coeliac disease treated with the gluten-free diet. Aliment Pharmacol Ther. 2012;35:723–729.
83. Mariani P, Viti MG, Montuori M, et al. The gluten-free diet: a nutritional risk factor for adolescents with celiac disease? J Pediatr Gastroenterol Nutr. 1998;27:519–523.
84. Scaramuzza AE, Mantegazza C, Bosetti A, Zuccotti GV. Type 1 diabetes and celiac disease: the effects of gluten free diet on metabolic control. World J Diabetes. 2013;4:130–134.
85. Kaukinen K, Lindfors K, Mäki M. Advances in the treatment of coeliac disease: an immunopathogenic perspective. Nat Rev Gastroenterol Hepatol. 2014;11:36–44.
86. Vanderpool C, Yan F, Polk DB. Mechanisms of probiotic action: implications for therapeutic applications in inflammatory bowel diseases. Inflamm Bowel Dis. 2008;14:1585–1596.
87. Zeng J, Li Y-Q, Zuo X-L, Zhen Y-B, Yang J, Liu C-H. Clinical trial: effect of active lactic acid bacteria on mucosal barrier function in patients with diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther. 2008;28:994–1002.
88. Seth A, Yan F, Polk DB, Rao RK. Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol. 2008;294:G1060–G1069.
89. Lindfors K, Blomqvist T, Juuti-Uusitalo K, et al. Live probiotic Bifidobacterium lactis bacteria inhibit the toxic effects induced by wheat gliadin in epithelial cell culture. Clin Exp Immunol. 2008;152:552–558.
90. Medina M, Izquierdo E, Ennahar S, Sanz Y. Differential immunomodulatory properties of Bifidobacterium logum strains: relevance to probiotic selection and clinical applications. Clin Exp Immunol. 2007;150:531–538.
91. Baba N, Samson S, Bourdet-Sicard R, Rubio M, Sarfati M. Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T cells. J Leukoc Biol. 2008;84:468–476.
92. Medina M, De Palma G, Ribes-Koninckx C, Calabuig M, Sanz Y. Bifidobacterium strains suppress in vitro the pro-inflammatory milieu triggered by the large intestinal microbiota of coeliac patients. J Inflamm (Lond). 2008;5:19.
93. Laparra JM, Sanz Y. Bifidobacteria inhibit the inflammatory response induced by gliadins in intestinal epithelial cells via modifications of toxic peptide generation during digestion. J Cell Biochem. 2010;109:801–807.
94. Laparra JM, Olivares M, Sanz Y. Oral administration of Bifidobacterium longum CECT 7347 ameliorates gliadin-induced alterations in liver iron mobilisation. Br J Nutr. 2013;110:1828–1836.
95. De Palma G, Cinova J, Stepankova R, Tuckova L, Sanz Y. Pivotal advance: bifidobacteria and gram-negative bacteria differentially influence immune responses in the proinflammatory milieu of celiac disease. J Leukoc Biol. 2010;87:765–778.
96. D’Arienzo R, Maurano F, Lavermicocca P, Ricca E, Rossi M. Modulation of the immune response by probiotic strains in a mouse model of gluten sensitivity. Cytokine. 2009;48:254–259.
97. De Angelis M, Rizzello CG, Fasano A, et al. VSL#3 probiotic preparation has the capacity to hydrolyze gliadin polypeptides responsible for Celiac Sprue. Biochim Biophys Acta. 2006;1762:80–93.
98. Smecuol E, Hwang HJ, Sugai E, Corso L, et al. Exploratory, randomized, double-blind, placebo-controlled study on the effects of Bifidobacterium infantis natren life start strain super strain in active celiac disease. J Clin Gastroenterol. 2013;47:139–147.
99. Olivares M, Castillejo G, Varea V, Sanz Y. Double-blind, randomised, placebo-controlled intervention trial to evaluate the effects of Bifidobacterium longum CECT 7347 in children with newly diagnosed coeliac disease. Br J Nutr. 2014;112:30–40.
100. Lorenzo Pisarello MJ, Vintiñi EO, González SN, Pagani F, Medina MS. Decrease in lactobacilli in the intestinal microbiota of celiac children with a gluten-free diet, and selection of potentially probiotic strains. Can J Microbiol. 2015;61:32–37.
101. Capriles VD, Arêas JAG. Effects of prebiotic inulin-type fructans on structure, quality, sensory acceptance and glycemic response of gluten-free breads. Food Funct. 2013;4:104–110.
102. Cheng J, Kalliomäki M, Heilig HGHJ, et al. Duodenal microbiota composition and mucosal homeostasis in pediatric celiac disease. BMC Gastroenterol. 2013;13:113.