Smokers with active Crohn's disease have a clinically relevant dysbiosis of the gastrointestinal microbiota

Inflammatory Bowel Diseases

Volumn 18, Issue 6, 2012, Pages 1092-1100

  Benjamin, Jane L ^a   Hedin, Charlotte R H ^a   Koutsoumpas, Andreas ^a   Ng, Siew C ^b,c   McCarthy, Neil E ^d   Prescott, Natalie J ^e   Pessoa Lopes, Pedro ^e   Mathew, Christopher G ^e   Sanderson, Jeremy ^a   Hart, Ailsa L ^b   Kamm, Michael A ^b,f   Knight, Stella C ^b   Forbes, Alastair ^g   Stagg, Andrew J ^d   Lindsay, James O ^d,h   Whelan, Kevin ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

^h BARTS HEALTH NHS TRUST   (United Kingdom)

Author keywords

Bacteroides; Crohn's disease; Faecalibacterium prausnitzii; microbiota; smoking

Indexed keywords

RNA 16S;

ADULT; ARTICLE; BACTEROIDES; BIFIDOBACTERIACEAE; CLINICAL STUDY; CLOSTRIDIUM; CONTROLLED STUDY; CROHN DISEASE; DEMOGRAPHY; DISEASE ACTIVITY; ESCHERICHIA COLI; EUBACTERIUM; FECES ANALYSIS; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; INTESTINE FLORA; MAJOR CLINICAL STUDY; MALE; MULTIVARIATE ANALYSIS; PREVOTELLA; PRIORITY JOURNAL; RECORDING; RNA PROBE; SAMPLE; SMOKING;

ADULT; CASE-CONTROL STUDIES; COLONY COUNT, MICROBIAL; CROHN DISEASE; DNA, BACTERIAL; FECES; FEMALE; GASTROINTESTINAL TRACT; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; METAGENOME; PROSPECTIVE STUDIES; SMOKING;

EID: 84861331645     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.21864     Document Type: Article

References (51)

1. Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001; 2: 361-367.
2. Stagg AJ, Hart AL, Knight SC, et al. The dendritic cell: its role in intestinal inflammation and relationship with gut bacteria. Gut. 2003; 52: 1522-1529.
3. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004; 118: 229-241.
4. Ivanov II, Frutos RL, Manel N, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008; 4: 337-349.
5. Sartor RB,. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008; 134: 577-594.
6. Hoentjen F, Tonkonogy SL, Qian BF, et al. CD4(+) T lymphocytes mediate colitis in HLA-B27 transgenic rats monoassociated with nonpathogenic Bacteroides vulgatus. Inflamm Bowel Dis. 2007; 13: 317-324.
7. Kim SC, Tonkonogy SL, Albright CA, et al. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology. 2005; 128: 891-906.
8. Hart AL, Lammers K, Brigidi P, et al. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut. 2004; 53: 1602-1609.
9. 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 U S A. 2008; 105: 16731-16736.
10. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010; 464: 59-65.
11. Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 2005; 308: 1635-1638.
12. Tamboli CP, Neut C, Desreumaux P, et al. Dysbiosis in inflammatory bowel disease. Gut. 2004; 53: 1-4.
13. Giaffer MH, Holdsworth CD, Duerden BI,. The assessment of faecal flora in patients with inflammatory bowel disease by a simplified bacteriological technique. J Med Microbiol. 1991; 35: 238-243.
14. Swidsinski A, Ladhoff A, Pernthaler A, et al. Mucosal flora in inflammatory bowel disease. Gastroenterology. 2002; 122: 44-54.
15. Mylonaki M, Rayment NB, Rampton DS, et al. Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm Bowel Dis. 2005; 11: 481-487.
16. Frank DN, St Amand AL, Feldman RA, et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007; 104: 13780-13785.
17. Sokol H, Seksik P, Furet JP, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009; 15: 1183-1189.
18. Cosnes J, Cattan S, Blain A, et al. Long-term evolution of disease behavior of Crohn's disease. Inflamm Bowel Dis. 2002; 8: 244-250.
19. 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.
20. Cosnes J, Carbonnel F, Beaugerie L, et al. Effects of cigarette smoking on the long-term course of Crohn's disease. Gastroenterology. 1996; 110: 424-431.
21. Cosnes J,. Tobacco and IBD: relevance in the understanding of disease mechanisms and clinical practice. Best Pract Res Clin Gastroenterol. 2004; 18: 481-496.
22. Kikuchi H, Itoh J, Fukuda S,. Chronic nicotine stimulation modulates the immune response of mucosal T cells to Th1-dominant pattern via nAChR by upregulation of Th1-specific transcriptional factor. Neurosci Lett. 2008; 432: 217-221.
23. Prescott NJ, Fisher SA, Franke A, et al. A nonsynonymous SNP in ATG16L1 predisposes to ileal Crohn's disease and is independent of CARD15 and IBD5. Gastroenterology. 2007; 132: 1665-1671.
24. Mahid SS, Minor KS, Soto RE, et al. Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc. 2006; 81: 1462-1471.
25. Sokol H, Seksik P, Rigottier-Gois L, et al. Specificities of the fecal microbiota in inflammatory bowel disease. Inflamm Bowel Dis. 2006; 12: 106-111.
26. Takaishi H, Matsuki T, Nakazawa A, et al. Imbalance in intestinal microflora constitution could be involved in the pathogenesis of inflammatory bowel disease. Int J Med Microbiol. 2008; 298: 463-472.
27. Swidsinski A, Ladhoff A, Pernthaler A, et al. Mucosal flora in inflammatory bowel disease. Gastroenterology. 2002; 122: 44-54.
28. Swidsinski A, Loening-Baucke V, Bengmark S, et al. Azathioprine and mesalazine-induced effects on the mucosal flora in patients with IBD colitis. Inflamm Bowel Dis. 2007; 13: 51-56.
29. Harmsen HJ, Gibson GR, Elfferich P, et al. Comparison of viable cell counts and fluorescence in situ hybridization using specific rRNA-based probes for the quantification of human fecal bacteria. FEMS Microbiol Lett. 2000; 183: 125-129.
30. Maddox PH, Jenkins D,. 3-Aminopropyltriethoxysilane (APES): a new advance in section adhesion. J Clin Pathol. 1987; 40: 1256-1257.
31. Kapuscinski J,. DAPI: a DNA-specific fluorescent probe. Biotech Histochem. 1995; 70: 220-233.
32. Langendijk PS, Schut F, Jansen GJ, et al. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol. 1995; 61: 3069-3075.
33. Manz W, Amann R, Ludwig W, et al. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology. 1996; 142 (Pt 5): 1097-1106.
34. Franks AH, Harmsen HJ, Raangs GC, et al. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol. 1998; 64: 3336-3345.
35. Poulsen LK, Lan F, Kristensen CS, et al. Spatial distribution of Escherichia coli in the mouse large intestine inferred from rRNA in situ hybridization. Infect Immun. 1994; 62: 5191-5194.
36. Suau A, Rochet V, Sghir A, et al. Fusobacterium prausnitzii and related species represent a dominant group within the human fecal flora. Syst Appl Microbiol. 2001; 24: 139-145.
37. Dallongeville J, Marecaux N, Fruchart JC, et al. Cigarette smoking is associated with unhealthy patterns of nutrient intake: a meta-analysis. J Nutr. 1998; 128: 1450-1457.
38. Mai V, McCrary QM, Sinha R, et al. Associations between dietary habits and body mass index with gut microbiota composition and fecal water genotoxicity: an observational study in African American and Caucasian American volunteers. Nutr J. 2009; 8: 49.
39. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009; 137: 1716-1724.
40. Wahed M, Goodhand JR, West O, et al. Tobacco dependence and awareness of health risks of smoking in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2011; 23: 90-94.
41. Robinson S, Bugler C,. General Lifestyle Survey 2008 (Smoking and drinking among adults). Office for National Statistics, Newport, UK.
42. Gorber SC, Schofield-Hurwitz S, Hardt J, et al. The accuracy of self-reported smoking: a systematic review of the relationship between self-reported and cotinine-assessed smoking status. Nicotine Tob Res. 2009; 11: 12-24.
43. van Winkelhoff AJ, Bosch-Tijhof CJ, Winkel EG, et al. Smoking affects the subgingival microflora in periodontitis. J Periodontol. 2001; 72: 666-671.
44. Mooney J, Hodge PJ, Kinane DF,. Humoral immune response in early-onset periodontitis: influence of smoking. J Periodontal Res. 2001; 36: 227-232.
45. Van KC, Belaiche J, Steeman C, et al. Negative association between smoking and anti-Saccharomyces cerevisiae antibodies in Crohn's disease. Acta Gastroenterol Belg. 2003; 66: 1-6.
46. Collado MC, Donat E, Ribes-Koninckx C, et al. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. J Clin Pathol. 2009; 62: 264-269.
47. Ng SC, Benjamin JL, McCarthy NE, et al. Relationship between human intestinal dendritic cells, gut microbiota, and disease activity in Crohn's disease. Inflamm Bowel Dis. 2010 [Epub ahead of print].
48. 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.
49. Mai V, Greenwald B, Morris JG Jr, et al. Effect of bowel preparation and colonoscopy on post-procedure intestinal microbiota composition. Gut. 2006; 55: 1822-1823.
50. Mondot S, Kang S, Furet JP, et al. Highlighting new phylogenetic specificities of Crohn's disease microbiota. Inflamm Bowel Dis. 2011; 17: 185-192.
51. Seksik P, Rigottier-Gois L, Gramet G, et al. Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon. Gut. 2003; 52: 237-242.