Distinct Microbiotas are Associated with Ileum-Restricted and Colon-Involving Crohn's Disease

Inflammatory Bowel Diseases

Volumn 22, Issue 2, 2016, Pages 293-302

  Naftali, Timna ^a   Reshef, Leah ^b   Kovacs, Amir ^b   Porat, Ron ^a   Amir, Itay ^b   Konikoff, Fred M ^a   Gophna, Uri ^b  

^a MEIR MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Crohn's disease; dysbiosis; MDI; microbiota

Indexed keywords

AMINO ACID TRANSPORTER; AMINOSALICYLIC ACID; ARGININE; AZATHIOPRINE; HISTIDINE; LYSINE; MERCAPTOPURINE; MESALAZINE; RNA 16S; STEROID;

ADULT; AMPLICON; ARTICLE; BACTERIAL COUNT; CLOSTRIDIALES; COLON; COLON BIOPSY; CONTROLLED STUDY; CROHN DISEASE; DIGESTIVE TRACT PARAMETERS; DISEASE ACTIVITY; DYSBIOSIS; ESCHERICHIA; FAECALIBACTERIUM; FEMALE; FUSOBACTERIUM; HUMAN; HUMAN TISSUE; ILEOCECAL VALVE; ILEUM; INTESTINE FLORA; MALE; MIDDLE AGED; PHENOTYPE; POPULATION ABUNDANCE; PRIORITY JOURNAL; PYROSEQUENCING; RELAPSE; REMISSION; RNA ANALYSIS; RUMINOCOCCACEAE; CASE CONTROL STUDY; COMPARATIVE STUDY; FOLLOW UP; GENETICS; ILEUM DISEASE; INFLAMMATION; MICROBIOLOGY; MICROFLORA; PATHOLOGY; PROGNOSIS;

ADULT; CASE-CONTROL STUDIES; COLON; CROHN DISEASE; FEMALE; FOLLOW-UP STUDIES; HUMANS; ILEAL DISEASES; ILEUM; INFLAMMATION; MALE; MICROBIOTA; MIDDLE AGED; PROGNOSIS; RNA, RIBOSOMAL, 16S;

EID: 84955604285     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000662     Document Type: Article

References (46)

1. Sellon RK, Tonkonogy S, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66: 5224-5231.
2. Taurog JD. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med. 1994; 180:2359-2364.
3. Franchimont D. Deficient host-bacteria interactions in inflammatory bowel disease? the toll-like receptor (TLR)-4 Asp299gly polymorphism is associated with Crohn's disease and ulcerative colitis. Gut. 2004;53: 987-992.
4. Bonen DK, Ogura Y, Nicolae DL, et al. Crohn's disease-associated NOD2 variants share a signaling defect in response to lipopolysaccharide and peptidoglycan. Gastroenterology. 2003;124:140-146.
5. Hampe J, Franke A, Rosenstiel P, et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet. 2007;39:207-211.
6. Yamazaki K, Onouchi Y, Takazoe M, et al. Association analysis of genetic variants in IL23R, ATG16L1 and 5p13.1 loci with Crohn's disease in Japanese patients. J Hum Genet. 2007;52:575-583.
7. Tamboli C, Neut C, Desreumaux P, et al. Dysbiosis as a prerequisite for IBD. Gut. 2004;53:1057-1057.
8. Gophna U, Sommerfeld K, Gophna S, et al. Differences between tissue-associated intestinal microfloras of patients with Crohn's disease and ulcerative colitis. J Clin Microbiol. 2006;44:4136-4141.
9. Frank DN, Robertson CE, Hamm CM, et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2011;17:179-184.
10. Martinez-Medina M. Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn's disease. Inflamm Bowel Dis. 2009;15:872-882.
11. Willing BP, Dicksved J, Halfvarson J, et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010;139:1844-1854.e1.
12. Morgan XC, Tickle TL, Sokol H, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13:R79.
13. Gevers D, Kugathasan S, Denson LA, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe. 2014; 15:382-392.
14. Ferrante M, Henckaerts L, Joossens M, et al. New serological markers in inflammatory bowel disease are associated with complicated disease behaviour. Gut. 2007;56:1394-1403.
15. Hancock L, Beckly J, Geremia A, et al. Clinical and molecular characteristics of isolated colonic Crohn's disease. Inflamm Bowel Dis. 2008;14:1667-1677.
16. Ahmad T, Armuzzi A, Bunce M, et al. The molecular classification of the clinical manifestations of Crohn's disease. Gastroenterology. 2002;122: 854-866.
17. Silverberg MS, Mirea L, Bull SB, et al. A population-and family-based study of Canadian families reveals association of HLA DRB1∗0103 with colonic involvement in inflammatory bowel disease. Inflamm Bowel Dis. 2003;9:1-9.
18. Fernandez L, Mendoza JL, Martinez A, et al. IBD1 and IBD3 determine location of Crohn's disease in the Spanish population. Inflamm Bowel Dis. 2004;10:715-722.
19. Arijs I, Quintens R, Van Lommel L, et al. Predictive value of epithelial gene expression profiles for response to infliximab in Crohn's disease. Inflamm Bowel Dis. 2010;16:2090-2098.
20. Baumgart M, Dogan B, Rishniw M, et al. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J. 2007;1:403-418.
21. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7: 335-336.
22. Hammer Ø, Harper DAT, Ryan PD. Paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001;4: 9-18.
23. Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
24. Langille MGI, Zaneveld J, Caporaso JG, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31:814-821.
25. Abubucker S, Segata N, Goll J, et al. Metabolic reconstruction for meta-genomic data and its application to the human microbiome. Plos Comput Biol. 2012;8.
26. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57:289-300.
27. Sepehri S, Kotlowski R. Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease. Inflamm Bowel Dis. 2007;13:675-683.
28. 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.
29. Arab HH, Salama SA, Eid AH, et al. Camel's milk ameliorates TNBS-induced colitis in rats via downregulation of inflammatory cytokines and oxidative stress. Food Chem Toxicol. 2014;69:294-302.
30. Willing B, Halfvarson J. Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn's disease. Inflamm Bowel Dis. 2009;15:653-660.
31. Tong M, Li X, Wegener Parfrey L, et al. A modular organization of the human intestinal mucosal microbiota and its association with inflammatory bowel disease. PLoS One. 2013;8:e80702.
32. Haberman Y, Tickle TL, Dexheimer PJ, et al. Pediatric Crohn disease patients exhibit specific ileal transcriptome and microbiome signature. J Clin Invest. 2014;124:3617-3633.
33. Abu Freha N, Schwartz D, Elkrinawi J, et al. Inflammatory bowel disease among Bedouin Arabs in southern Israel: urbanization and increasing prevalence rates. Eur J Gastroenterol Hepatol. 2015;27:230-234.
34. Fidder HH, Avidan B, Lahav M, et al. Clinical and demographic characterization of Jewish Crohn's disease patients in Israel. J Clin Gastroenter-ol. 2003;36:8-12.
35. Wills ES, Jonkers DMAE, Savelkoul PH, et al. Fecal microbial composition of ulcerative colitis and Crohn's disease patients in remission and subsequent exacerbation. PLoS One. 2014;9:e90981.
36. Cleynen I, González JR, Figueroa C, et al. Genetic factors conferring an increased susceptibility to develop Crohn's disease also influence disease phenotype: results from the IBDchip European Project. Gut. 2013;62: 1556-1565.
37. Juste C, Kreil DP, Beauvallet C, et al. Bacterial protein signals are associated with Crohn's disease. Gut. 2014;63:1566-1577.
38. Yamazaki K, Umeno J, Takahashi A, et al. A genome-wide association study identifies 2 susceptibility Loci for Crohn's disease in a Japanese population. Gastroenterology. 2013;144:781-788.
39. Julià A, Domènech E, Ricart E, et al. A genome-wide association study on a southern European population identifies a new Crohn's disease susceptibility locus at RBX1-EP300. Gut. 2013;62:1440-1445.
40. Ellinghaus D, Zhang H, Zeissig S, et al. Association between variants of PRDM1 and NDP52 and Crohn's disease, based on exome sequencing and functional studies. Gastroenterology. 2013;145:339-347.
41. Umeno J, Asano K, Matsushita T, et al. Meta-analysis of published studies identified eight additional common susceptibility loci for Crohn's disease and ulcerative colitis. Inflamm Bowel Dis. 2011;17:2407-2415.
42. Andoh A, Sakata S, Koizumi Y, et al. Terminal restriction fragment length polymorphism analysis of the diversity of fecal microbiota in patients with ulcerative colitis. Inflamm Bowel Dis. 2007;13:955-962.
43. Komanduri S, Gillevet PM, Sikaroodi M, et al. Dysbiosis in pouchitis: evidence of unique microfloral patterns in pouch inflammation. Clin Gas-troenterol Hepatol. 2007;5:352-360.
44. Reshef L, Kovacs A, Ofer A, et al. Pouch inflammation is associated with a decrease in specific bacterial taxa. Gastroenterol. 2015;149:718-727.
45. Tahara T, Yamamoto E, Suzuki H, et al. Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res. 2014;74:1311-1318.
46. Ohkusa T, Yoshida T, Sato N, et al. Commensal bacteria can enter colonic epithelial cells and induce proinflammatory cytokine secretion: a possible pathogenic mechanism of ulcerative colitis. J Med Microbiol. 2009;58: 535-545.