Faecal microbiota study reveals specific dysbiosis in spondyloarthritis

Annals of the Rheumatic Diseases

Volumn 76, Issue 9, 2017, Pages 1614-1622

  Breban, Maxime ^a,b,c   Tap, Julien ^d   Leboime, Ariane ^c   Said Nahal, Roula ^c   Langella, Philippe ^d   Chiocchia, Gilles ^a,b,e   Furet, Jean Pierre ^d   Sokol, Harry ^c,d,f  

^a LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL AMBROISE PARÉ   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^f SORBONNE UNIVERSITÉ   (France)

Author keywords

ankylosing spondylitis; infection; inflammation; rheumatoid arthritis; spondyloarthritis

Indexed keywords

BIOLOGICAL PRODUCT; CORTICOSTEROID; DISEASE MODIFYING ANTIRHEUMATIC DRUG; HLA B27 ANTIGEN; METHOTREXATE; NONSTEROID ANTIINFLAMMATORY AGENT; PROTON PUMP INHIBITOR; RNA 16S; SALAZOSULFAPYRIDINE;

16S RIBOSOMAL RNA GENE; ADULT; AGED; ARTICLE; BIODIVERSITY; COHORT ANALYSIS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE COURSE; DNA ISOLATION; DYSBIOSIS; FECES ANALYSIS; FECES MICROFLORA; FEMALE; GENE SEQUENCE; HUMAN; INFLAMMATORY BOWEL DISEASE; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PATHOGENESIS; POPULATION ABUNDANCE; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; RUMINOCOCCUS; RUMINOCOCCUS GNAVUS; SIBLING; SPECIES COMPOSITION; SPONDYLARTHRITIS; VOLUNTEER; CASE CONTROL STUDY; FECES; GENETICS; IMMUNOLOGY; INTESTINE FLORA; MICROBIOLOGY; MIDDLE AGED; MULTIVARIATE ANALYSIS; SPONDYLOARTHROPATHY;

ADULT; AGED; ARTHRITIS, RHEUMATOID; CASE-CONTROL STUDIES; COHORT STUDIES; CROSS-SECTIONAL STUDIES; DYSBIOSIS; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HLA-B27 ANTIGEN; HUMANS; INFLAMMATORY BOWEL DISEASES; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; RNA, RIBOSOMAL, 16S; RUMINOCOCCUS; SIBLINGS; SPONDYLARTHROPATHIES;

EID: 85024839205     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2016-211064     Document Type: Article

References (45)

1. Baeten D, Breban M, Lories R, et al. Are spondylarthritides related but distinct conditions or a single disease with a heterogeneous phenotype? Arthritis Rheum 2013;65:12-20.
2. Breban M, Costantino F, André C, et al. Revisiting MHC genes in spondyloarthritis. Curr Rheumatol Rep 2015;17:516.
3. Brown MA, Kenna T, Wordsworth BP. Genetics of ankylosing spondylitis-insights into pathogenesis. Nat Rev Rheumatol 2016;12:81-91.
4. Ellinghaus D, Jostins L, Spain SL, et al. Analysis of five chronic inflammatory diseases identifies 27 new associations and highlights disease-specific patterns at shared loci. Nat Genet 2016;48:510-8.
5. Wlodarska M, Kostic AD, Xavier RJ. An integrative view of microbiome-host interactions in inflammatory bowel diseases. Cell Host Microbe 2015;17:577-91.
6. Breban M. Gut Microbiota and inflammatory joint diseases. Joint Bone Spine 2016;83:645-9.
7. T ito RY, Cypers H, Joossens M, et al. Brief report: Dialister as a microbial marker of disease activity in spondyloarthritis. Arthritis Rheumatol 2017;69:114-21.
8. Zhang X, Zhang D, Jia H, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med 2015;21:895-905.
9. Breban M. Gut Microbiota and inflammatory joint diseases. Joint Bone Spine 2016;83:645-9.
10. Said-Nahal R, Miceli-Richard C, Berthelot JM, et al. The familial form of spondylarthropathy: A clinical study of 115 multiplex families. Groupe Francąis D'etude Génétique Des Spondylarthropathies. Arthritis Rheum 2000;43:1356-65.
11. R udwaleit M, van der Heijde D, Landewé R, et al. The Assessment of SpondyloArthritis International Society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general. Ann Rheum Dis 2011;70:25-31.
12. Aletaha D, Neogi T, Silman AJ, et al. 2010 rheumatoid arthritis classification criteria: An American College of Rheumatology/European League against Rheumatism collaborative initiative. Ann Rheum Dis 2010:69:1580-8.
13. T ubach F, Pham T, Skomsvoll JF, et al. Stability of the patient acceptable symptomatic state over time in outcome criteria in ankylosing spondylitis. Arthritis Rheum 2006;55:960-3.
14. Furet JP, Firmesse O, Gourmelon M, et al. Comparative assessment of human and farm animal faecal Microbiota using real-time quantitative PCR. FEMS Microbiol Ecol 2009;68:351-62.
15. Lamas B, Richard ML, Leducq V, et al. CARD9 impacts colitis by altering gut Microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat Med 2016;22:598-605.
16. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of highthroughput community sequencing data. Nat Methods 2010;7:335-6.
17. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010;26:2460-1.
18. McDonald D, Price MN, Goodrich J, et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 2012;6:610-8.
19. Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12:R60.
20. Morgan XC, Tickle TL, Sokol H, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012;13:R79.
21. Cua DJ, Sherlock JP. Autoimmunity's collateral damage: Gut microbiota strikes ' back'. Nat Med 2011;17:1055-6.
22. Scher JU, Ubeda C, Artacho A, et al. Decreased bacterial diversity characterizes the altered gut Microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol 2015;67:128-39.
23. Goodrich JK, Waters JL, Poole AC, et al. Human genetics shape the gut microbiome. Cell 2014;159:789-99.
24. T urpin W, Espin-Garcia O, Xu W, et al. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat Genet 2016;48:1413-7.
25. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59-65.
26. T ailford LE, Crost EH, Kavanaugh D, et al. Mucin glycan foraging in the human gut microbiome. Front Genet 2015;6 http://www. frontiersin. org/Nutrigenomics
27. Beaud D, Tailliez P, Anba-Mondoloni J. Genetic characterization of the betaglucuronidase enzyme from a human intestinal bacterium, Ruminococcus gnavus. Microbiology 2005;151:2323-30.
28. D evlin AS, Fischbach MA. A biosynthetic pathway for a prominent class of microbiotaderived bile acids. Nat Chem Biol 2015;11:685-90.
29. P rindiville T, Cantrell M, Wilson KH. Ribosomal DNA sequence analysis of mucosaassociated bacteria in crohn's disease. Inflamm Bowel Dis 2004;10:824-33.
30. Mondot S, Lepage P, Seksik P, et al. Structural robustness of the gut mucosal microbiota is associated with crohn's disease remission after surgery. Gut 2016;65:954-62.
31. 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;139:1844-54.
32. Joossens M, Huys G, Cnockaert M, et al. Dysbiosis of the faecal Microbiota in patients with crohn's disease and their unaffected relatives. Gut 2011;60:631-7.
33. Machiels K, Sabino J, Vandermosten L, et al. Specific members of the predominant gut microbiota predict pouchitis following colectomy and IPAA in UC. Gut 2017;66:79-88.
34. P ng CW, Lindén SK, Gilshenan KS, et al. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 2010;105:2420-8.
35. T aurog JD, Maika SD, Satumtira N, et al. Inflammatory disease in HLA-B27 transgenic rats. Immunol Rev 1999;169:209-23.
36. Lin P, Bach M, Asquith M, et al. HLA-B27 and human ß2-microglobulin affect the gut Microbiota of transgenic rats. PLoS One 2014;9:e105684.
37. Asquith MJ, Stauffer P, Davin S, et al. Perturbed mucosal immunity and dysbiosis accompany clinical disease in a rat model of spondyloarthritis: Impact of HLA-B27 on mucosal immunity and Iintestinal microbiota. Arthritis Rheumatol 2016;68:2151-62.
38. Stoll ML. Gut microbes, immunity, and spondyloarthritis. Clin Immunol 2015;159:134-42.
39. Ciccia F, Guggino G, Rizzo A, et al. Dysbiosis and zonulin upregulation alter gut epithelial and vascular barriers in patients with ankylosing spondylitis. Ann Rheum Dis 2017;76:1123-32.
40. Costello M-E, Ciccia F, Willner D, et al. Brief Report: Intestinal dysbiosis in Ankylosing Spondylitis: Gut Microbiome and AS-Related genes. Arthritis Rheumatol 2015;67:686-91.
41. P apa E, Docktor M, Smillie C, et al. Non-invasive mapping of the gastrointestinal Microbiota identifies children with inflammatory bowel disease. PLoS One 2012;7:e39242.
42. Gevers D, Kugathasan S, Denson LA, et al. The treatment-naive microbiome in newonset crohn's disease. Cell Host Microbe 2014;15:382-92.
43. Gardiner BJ, Tai AY, Kotsanas D, et al. Clinical and microbiological characteristics of Eggerthella lenta bacteremia. J Clin Microbiol 2015;53:626-35.
44. Horz HP, Citron DM, Warren YA, et al. Synergistes group organisms of human origin. J Clin Microbiol 2006;44:2914-20.
45. Scher JU, Sczesnak A, Longman RS, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2013;2:e01202 http://elifesciences. org/lookup/doi/10.7554/eLife. 01202.