nach oben

Clinical Rheumatology

Erschienen in:

26.03.2020 | Original Article

Dynamic changes in gut microbiota under the influence of smoking and TNF-α-blocker in patients with ankylosing spondylitis

verfasst von: Fangze Zhang, Cuili Ma, Bin Zhang, Liqi Bi

Erschienen in: Clinical Rheumatology | Ausgabe 9/2020

Einloggen, um Zugang zu erhalten

Abstract

Objectives

This study aimed to investigate the relationship among smoking, TNF-α-blocker therapy, and the dynamic changes in gut microbiota in patients with ankylosing spondylitis (AS).

Methods

Using a 16S rRNA sequence, 98 fecal samples of 20 AS patients collected after 0, 1, 3 and 6 months of anti-TNF-α treatment and from 20 matched health controls were examined. The variation in composition, abundance, and diversity of gut microbiota was analyzed. The dynamic effects of smoking and treatment on gut microbiota and therapeutic efficacy in AS patients were studied.

Results

The increased relative abundance of microbiota in AS nonsmokers was g_Comamonas and g_Desulfovibrio, while that in AS smokers was g_Actinomyces, g_Collinsella, g_Lachnospiraceae_UCG-008, and g_Paraprevotella. The relative abundance of gut microbiota showed dynamic variation. The improvement rate of ASDAS in AS nonsmokers was higher than that in AS smokers (2.297 vs 1.736) after anti-TNF-α treatment. The β-diversity of gut microbiota in AS smokers was lower than that in AS nonsmokers and improved with treatment.

Conclusions

Both smoking and TNF-α-blocker had significant effects on the composition, relative abundance, and diversity of gut microbiota in AS patients. The AS smokers characteristically shared g_Collinsella and g_Dorea. The relative abundance of gut microbiota revealed high variability and was in dynamic fluctuation during treatment. The response of gut microbiota to anti-TNF-α treatment was found to be heterogeneous and selective. AS nonsmokers showed a greater improvement rate of ASDAS-CRP with treatment than AS smokers did. The AS smokers showed a lower β-diversity of gut microbiota, and improved after treatment.

Key Points

• Characterized the dynamic variation in gut microbiota in AS patients classified as smokers and nonsmokers during treatment with anti-TNF-α.

• Confirmed the interaction between smoking, anti-TNF-α therapy, and gut microbiota.

Shreiner AB, Kao JY, Young VB (2015) The gut microbiome in health and in disease. Curr Opin Gastroenterol 31:69–75. https://doi.org/10.1097/MOG.0000000000000139

Dulal S, Keku TO (2014) Gut microbiome and colorectal adenomas. Cancer J 20:225–231. https://doi.org/10.1097/PPO.0000000000000050CrossRefPubMedPubMedCentral

Kalinkovich A, Livshits G (2019) A cross talk between dysbiosis and gut-associated immune system governs the development of inflammatory arthropathies. Semin Arthritis Rheum 49:474–484. https://doi.org/10.1016/j.semarthrit.2019.05.007CrossRefPubMed

Zhong D, Wu C, Zeng X, Wang Q (2018) The role of gut microbiota in the pathogenesis of rheumatic diseases. Clin Rheumatol 37:25–34. https://doi.org/10.1007/s10067-017-3821-4CrossRefPubMed

Scher JU, Littman DR, Abramson SB (2016) Microbiome in inflammatory arthritis and human rheumatic diseases. Arthritis Rheum 68:35–45. https://doi.org/10.1002/art.39259CrossRef

Martinez A, Pacheco-Tena C, Vazquez-Mellado J, Burgos-Vargas R (2004) Relationship between disease activity and infection in patients with spondyloarthropathies. Ann Rheum Dis 63:1338–1340CrossRefPubMedPubMedCentral

Yang L, Wang L, Wang X, Xian CJ, Lu H (2016) A possible role of intestinal microbiota in the pathogenesis of ankylosing spondylitis. Int J Mol Sci 17(12):E2126. https://doi.org/10.3390/ijms17122126

Rath HC, Wilson KH, Sartor RB (1999) Differential induction of colitis and gastritis in HLA-B27 transgenic rats selectively colonized with Bacteroides vulgatus or Escherichia coli. Infect Immun 67:2969–2974CrossRefPubMedPubMedCentral

Mäki-Ikola O, Leirisalo-Repo M, Turunen U, Granfors K (1997) Association of gut inflammation with increased serum IgA class Klebsiella antibody concentrations in patients with axial ankylosing spondylitis (AS): implication for different aetiopathogenetic mechanisms for axial and peripheral AS? Ann Rheum Dis 56:180–183CrossRefPubMedPubMedCentral

10.

Martínez-González O, Cantero-Hinojosa J, Paule-Sastre P, Gómez-Magán JC, Salvatierra-Ríos D (1994) Intestinal permeability in patients with ankylosing spondylitis and their healthy relatives. Br J Rheumatol 33:644–647CrossRefPubMed

11.

Fragoulis GE, Siebert S, McInnes IB (2016) Therapeutic targeting of IL-17 and IL-23 cytokines in immune-mediated diseases. Annu Rev Med 67:337–353CrossRefPubMed

12.

Rashid T, Ebringer A (2012) Autoimmunity in rheumatic diseases is induced by microbial infections via crossreactivity or molecular mimicry. Autoimmune Dis 2012:539282. https://doi.org/10.1155/2012/539282CrossRefPubMedPubMedCentral

13.

Savin Z, Kivity S, Yonath H, Yehuda S (2018) Smoking and the intestinal microbiome. Arch Microbiol 200:677–684. https://doi.org/10.1007/s00203-018-1506-2CrossRefPubMed

14.

Ciurea A, Acherer A, Weber U, Exer P, Bernhard J, Tamborrini G, Riek M, Müller RB, Weiss B, Nissen MJ, Kissling R, Michel BA, Finckh A (2016) Impaired response to treatment with tumour necrosis factor α inhibitors in smokers with axial spondyloarthritis. Ann Rheum Dis 75:532–539. https://doi.org/10.1136/annrheumdis-2013-205133CrossRefPubMed

15.

Jones GT, Ratz T, Dean LE, Macfariane GJ, Atzeni F (2017) Disease severity in never smokers, ex-smokers, and current smokers with axial spondyloarthritis: results from the Scotland registry for ankylosing spondylitis. Arthritis Care Res 69:1407–1413. https://doi.org/10.1002/acr.23157CrossRef

16.

Van der LS, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 27:361–368CrossRef

17.

Garrett S, Jenkinson T, Kennedy LG, Whitelock H, Gaisford P, Calin A (1994) A new approach to defining disease status in ankylosing spondylitis the Bath Ankylosing Spondylitis Disease Activity Index. J Rheumatol 21:2286–2291PubMed

18.

Braun J, Pham T, Sieper J, Davis J, van der Linden S, Dougados M, van der Heijde D, ASAS Working Group (2003) International ASAS consensus statement for the use of anti-tumour necrosis factor agents in patients with ankylosing spondylitis. Ann Rheum Dis 62:817–824CrossRefPubMedPubMedCentral

19.

Machado P, Landewé R, Lie E, Kvien TK, Braun J, Baker D, van der Heijde D, Assessment of SpondyloArthritis international Society (2011) Ankylosing spondylitis disease activity score (ASDAS): defining cut-off values for disease activity states and improvement scores. Ann Rheum Dis 70:47–53. https://doi.org/10.1136/ard.2010.138594CrossRefPubMed

20.

Sieper J, Rudwaleit M, Baraliakos X, Braun J, Burgos-Vargas R, Dougados M, Hermann KG, Landewe R, Maksymoowych W, van der Heijde D (2009) The assessment of SpondyloArthritis international society (ASAS) hand book: a guide to assess spondyloarthritis. Ann Rheum Dis 68(Suppl 2):ii1–i44. https://doi.org/10.1136/ard.2008.104018CrossRefPubMed

21.

Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604CrossRefPubMed

22.

Laing B, Barnett MPG, Marlow G, Nasef NA, Ferguson LR (2018) An update on the role of gut microbiota in chronic inflammatory diseases, and potential therapeutic targets. Expert Rev Gastroenterol Hepatol 12:969–983. https://doi.org/10.1080/17474124.2018.1505497CrossRefPubMed

23.

Eeckhaut V, Machiels K, Perrier C, Romero C, Maes S, Flahou B, Steppe M, Haesebrouck F, Sas B, Ducatelle R, Vermeire S, Van Immerseel F (2013) Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut. 62:1745–1752. https://doi.org/10.1136/gutjnl-2012-303611CrossRefPubMed

24.

Garcia-Montoya L, Gul H, Emery P (2018) Recent advances in ankylosing spondylitis: understanding the disease and management. F1000Res 7:F1000 faculty Rev-1512. https://doi.org/10.12688/f1000research.14956.1 eCollection 2018CrossRefPubMedPubMedCentral

25.

De Vos M, Cuvelier C, Mielants H, Veys E, Barbier F, Elewaut A (1989) Ileocolonoscopy in seronegative spondylarthropathy. Gastroenterology 96:339–344CrossRefPubMed

26.

Costello ME, Ciccia F, Willner D, Warrington N, Robinson PC, Gardiner B, Marshall M, Kenna TJ, Triolo G, Brown MA (2015) Brief report: intestinal dysbiosis in ankylosing spondylitis. Arthritis Rheum 67:686–691. https://doi.org/10.1002/art.38967CrossRef

27.

Van Praet L, Jans L, Carron P, Jacques P, Glorieus E, Colman R (2014) Degree of bone marrow oedema in sacroiliac joints of patients with axial spondyloarthritis is linked to gut inflammation and male sex: results from the GIANT cohort. Ann Rheum Dis 73:1186–1189. https://doi.org/10.1136/annrheumdis-2013-203854

28.

Orchard TR, Thiyagaraja S, Welsh KI, Wordsworth BP, Hill Gaston JS, Jewell DP (2000) Clinical phenotype is related to HLA genotype in the peripheral arthropathies of inflammatory bowel disease. Gastroenterology 118:274–278CrossRefPubMed

29.

Asquith M, Elewaut D, Lin P, Rosenbaum JT (2014) The role of the gut and microbes in the pathogenesis of spondyloarthritis. Best Pract Res Clin Rheumatol 28:687–702. https://doi.org/10.1016/j.berh.2014.10.018

30.

Lee YW, Lee KM, Lee JM, Chung YY, Kim DB, Kim YJ, Chung WC, Paik CN (2019) The usefulness of fecal calprotectin in assessing inflammatory bowel disease activity. Korean J Intern Med 34(1):72–80. https://doi.org/10.3904/kjim.2016.324CrossRefPubMed

31.

Duran A, Kobak S, Sen N, Aktakka S, Atabay T, Orman M (2016) Fecal calprotectin is associated with disease activity in patients with ankylosing spondylitis. Bosn J Basic Med Sci 16:71–74. https://doi.org/10.17305/bjbms.2016.752CrossRefPubMedPubMedCentral

32.

Klingberg E, Olerod G, Hammarsten O, Forsblad-d'Elia H (2016) The vitamin D status in ankylosing spondylitis in relation to intestinal inflammation, disease activity, and bone health: a cross-sectional study. Osteoporos Int 27:2027–2033. https://doi.org/10.1007/s00198-016-3489-7CrossRefPubMed

33.

Gisbert JP, McNicholl AG, Gomollon F (2009) Questions and answers on the role of faecal calprotectin as a biological marker in inflammatory bowel disease. Inlamm Bowel Dis 15:1746–1754. https://doi.org/10.1002/ibd.20920CrossRef

34.

Wexler AG, Goodman AL (2017) An Insider's perspective: Bacteroides as a window into the microbiome. Nat Microbiol 2:17026. https://doi.org/10.1038/nmicrobiol.2017.26CrossRefPubMedPubMedCentral

35.

Li W, Wu X, Hu X, Wang T, Liang S, Duan Y, Jin F, Qin B (2017) Structural changes of gut microbiota in Parkinson's disease and its correlation with clinical features. Sci China Life Sci 60:1223–1233. https://doi.org/10.1007/s11427-016-9001-4CrossRefPubMed

36.

Quévrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, Miquel S, Carlier L, Bermúdez-Humarán LG, Pigneur B, Lequin O, Kharrat P, Thomas G, Rainteau D, Aubry C, Breyner N, Afonso C, Lavielle S, Grill JP, Chassaing G, Chatel JM, Trugnan G, Xavier R, Langella P, Sokol H, Seksik P (2016) Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn's disease. Gut 65:415–425. https://doi.org/10.1136/gutjnl-2014-307649CrossRefPubMed

37.

Wang CS, Li WB, Wang HY, Ma YM, Zhao XH, Yang H, Qian JM, Li JN (2018) VSL#3 can prevent ulcerative colitis-associated carcinogenesis in mice. World J Gastroenterol 24:4254–4262. https://doi.org/10.3748/wjg.v24.i37.4254CrossRefPubMedPubMedCentral

38.

Wu TR, Lin CS, Chang CJ, Lin TL, Martel J, Ko YF, Ojcius DM, Lu CC, Young JD, Lai HC (2019) Gut commensal Parabacteroides goldsteinii plays a predominant role in the anti-obesity effects of polysaccharides isolated from Hirsutella sinensis. Gut 68:248–262. https://doi.org/10.1136/gutjnl-2017-315458

39.

Jenq RR, Taur Y, Devlin SM, Ponce DM, Goldberg JD, Ahr KF, Littmann ER, Ling L, Gobourne AC, Miller LC, Docampo MD, Peled JU, Arpaia N, Cross JR, Peets TK, Lumish MA, Shono Y, Dudakov JA, Poeck H, Hanash AM, Barker JN, Perales MA, Giralt SA, Pamer EG, van den Brink MR (2015) Intestinal Blautia is associated with reduced death from graft-versus-host disease. Biol Blood Marrow Transplant 21(8):1373–1383. https://doi.org/10.1016/j.bbmt.2015.04.016CrossRefPubMedPubMedCentral

40.

Boesmans L, Valles-Colomer M, Wang J, Eeckhaut V, Falony G, Ducatelle R, Van Immerseel F, Raes J, Verbeke K (2018) Butyrate producers as potential next-generation probiotics: safety assessment of the administration of Butyricicoccus pullicaecorum to healthy volunteers. mSystems 3(6):e00094–e00018. https://doi.org/10.1128/mSystems.00094-18CrossRefPubMedPubMedCentral

41.

Kim D, Hofstaedter CE, Zhao C, Mattei L, Tanes C, Clarke E, Lauder A, Sherrill-Mix S, Chehoud C, Kelsen J, Conrad M, Collman RG, Baldassano R, Bushman FD, Bittinger K (2017) Optimizing methods and dodging pitfalls in microbiome research. Microbiome 5(1):52. https://doi.org/10.1186/s40168-017-0267-5

42.

Shanahan ER, Shah A, Koloski N, Walker MM, Talley NJ, Morrison M, Holtmann GJ (2018) Influence of cigarette smoking on the human duodenal mucosa-associated microbiota. Microbiome 6(1):150. https://doi.org/10.1186/s40168-018-0531-3CrossRefPubMedPubMedCentral

43.

Opstelten JL, Plassais J, van Mil SW, Achouri E, Pichaud M, Siersema PD, Oldenburg B, Cervino AC (2016) Gut microbial diversity is reduced in smokers with Crohn’s disease. Inflamm Bowel Dis 22(9):2070–2077. https://doi.org/10.1097/MIB.0000000000000875CrossRefPubMed

44.

de Paiva CS, Jones DB, Stern ME, Bian F, Moore QL, Corbiere S, Streckfus CF, Hutchinson DS, Ajami NJ, Petrosino JF, Pflugfelder SC (2016) Altered mucosal microbiome diversity and disease severity in Sjögren syndrome. Sci Rep 6:23561. https://doi.org/10.1038/srep23561CrossRefPubMedPubMedCentral

Titel: Dynamic changes in gut microbiota under the influence of smoking and TNF-α-blocker in patients with ankylosing spondylitis
verfasst von: Fangze Zhang
Cuili Ma
Bin Zhang
Liqi Bi
Publikationsdatum: 26.03.2020
Verlag: Springer International Publishing
Erschienen in: Clinical Rheumatology / Ausgabe 9/2020
Print ISSN: 0770-3198
Elektronische ISSN: 1434-9949
DOI: https://doi.org/10.1007/s10067-020-05032-4

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

24.04.2024 | DGIM 2024 | Kongressbericht | Nachrichten

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Dynamic changes in gut microbiota under the influence of smoking and TNF-α-blocker in patients with ankylosing spondylitis

Abstract

Objectives

Methods

Results

Conclusions

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Metformin rückt in den Hintergrund

Myokarditis nach Infekt – richtig schwierig wird es bei Profisportlern

Thrombophiliescreening – Wenn, dann richtig und nur bei therapeutischer Konsequenz

Bei Senioren mit Prostatakarzinom auf Anämie achten!

Update Innere Medizin

Springer Medizin

Abstract

Objectives

Methods

Results

Conclusions

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 9/2020

Retention rates and identification of factors associated with anti-TNFα, anti-IL17, and anti-IL12/23R agents discontinuation in psoriatic arthritis patients: results from a real-world clinical setting

Evaluation of cardiac autonomic nervous system in patients with ankylosing spondylitis using 12-lead electrocardiography and Holter monitoring

Evaluation of the immune response to hepatitis B vaccine in patients on biological therapy: results of the RIER cohort study

The changing profile of ankylosing spondylitis in the biologic era

A prospective cross-sectional study of serum IL-17A in antisynthetase syndrome

Risk of systemic autoimmune diseases in gastric disease patients with proton pump inhibitor use: a nationwide cohort study in Taiwan

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Metformin rückt in den Hintergrund

Myokarditis nach Infekt – richtig schwierig wird es bei Profisportlern

Thrombophiliescreening – Wenn, dann richtig und nur bei therapeutischer Konsequenz

Bei Senioren mit Prostatakarzinom auf Anämie achten!

Update Innere Medizin