Distinctive gut microbiomes of ankylosing spondylitis and inflammatory bowel disease patients suggest differing roles in pathogenesis and correlate with disease activity

P. R. Sternes; L. Brett; J. Phipps; F. Ciccia; T. Kenna; E. de Guzman; K. Zimmermann; M. Morrison; G. Holtmann; E. Klingberg; D. Mauro; C. McIvor; H. Forsblad-d’Elia; M. A. Brown

doi:10.1186/s13075-022-02853-3

Distinctive gut microbiomes of ankylosing spondylitis and inflammatory bowel disease patients suggest differing roles in pathogenesis and correlate with disease activity

P. R. Sternes^*, L. Brett, J. Phipps, F. Ciccia, T. Kenna, E. de Guzman, K. Zimmermann, M. Morrison, G. Holtmann, E. Klingberg, D. Mauro, C. McIvor, H. Forsblad-d’Elia, M. A. Brown

^*Corresponding author for this work

Medical & Molecular Genetics

Research output: Contribution to journal › Article › peer-review

16 Citations (Scopus)

Abstract

Background: Multiple studies have confirmed dysbiosis in ankylosing spondylitis (AS) and inflammatory bowel disease (IBD); however, due to methodological differences across studies, it has not been possible to determine if these diseases have similar or different gut microbiomes. Results: In this study, faecal and intestinal biopsies were obtained from 33 Australian AS patients (including 5 with concomitant IBD, ‘AS-IBD’), 59 IBD patients and 105 healthy controls. Stool samples were also obtained from 16 Italian AS patients and 136 Swedish AS patients. Focusing on the Australian cohort, AS, AS-IBD and IBD patients differed from one another and from healthy controls in both alpha and beta diversity. AS patients with and without clinical IBD could be distinguished from one another with moderate accuracy using stool microbiome (AUC=0.754). Stool microbiome also accurately distinguished IBD patients from healthy controls (AUC=0.757). Microbiome composition was correlated with disease activity measured by BASDAI and faecal calprotectin (FCP) levels. Enrichment of potentially pathogenic Streptococcus was noted in AS, AS-IBD and IBD patients. Furthermore, enrichment of another potentially pathogenic genus, Haemophilus, was observed in AS, AS-IBD, IBD, AS patients with increased BASDAI, and IBD patients with faecal calprotectin >100 μg/mg. Apart from these genera, no other taxa were shared between AS and IBD patients. Conclusions: In conclusion, the distinct gut microbiome of AS and AS-IBD patients compared to IBD patients and healthy controls is consistent with immunological and genetic evidence suggesting that the gut plays a different role in driving AS compared with IBD. However, enrichment of two potentially pathogenic genera in both diseases suggests that the presence of a shared/common microbial trigger of disease cannot be discounted.

Original language	English
Article number	163
Journal	Arthritis Research and Therapy
Volume	24
Issue number	1
DOIs	https://doi.org/10.1186/s13075-022-02853-3
Publication status	Published - Dec 2022

Keywords

Ankylosing spondylitis
Dysbiosis
Gut
Inflammatory Bowel disease

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10.1186/s13075-022-02853-3

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Sternes, P. R., Brett, L., Phipps, J., Ciccia, F., Kenna, T., de Guzman, E., Zimmermann, K., Morrison, M., Holtmann, G., Klingberg, E., Mauro, D., McIvor, C., Forsblad-d’Elia, H., & Brown, M. A. (2022). Distinctive gut microbiomes of ankylosing spondylitis and inflammatory bowel disease patients suggest differing roles in pathogenesis and correlate with disease activity. Arthritis Research and Therapy, 24(1), Article 163. https://doi.org/10.1186/s13075-022-02853-3

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title = "Distinctive gut microbiomes of ankylosing spondylitis and inflammatory bowel disease patients suggest differing roles in pathogenesis and correlate with disease activity",

abstract = "Background: Multiple studies have confirmed dysbiosis in ankylosing spondylitis (AS) and inflammatory bowel disease (IBD); however, due to methodological differences across studies, it has not been possible to determine if these diseases have similar or different gut microbiomes. Results: In this study, faecal and intestinal biopsies were obtained from 33 Australian AS patients (including 5 with concomitant IBD, {\textquoteleft}AS-IBD{\textquoteright}), 59 IBD patients and 105 healthy controls. Stool samples were also obtained from 16 Italian AS patients and 136 Swedish AS patients. Focusing on the Australian cohort, AS, AS-IBD and IBD patients differed from one another and from healthy controls in both alpha and beta diversity. AS patients with and without clinical IBD could be distinguished from one another with moderate accuracy using stool microbiome (AUC=0.754). Stool microbiome also accurately distinguished IBD patients from healthy controls (AUC=0.757). Microbiome composition was correlated with disease activity measured by BASDAI and faecal calprotectin (FCP) levels. Enrichment of potentially pathogenic Streptococcus was noted in AS, AS-IBD and IBD patients. Furthermore, enrichment of another potentially pathogenic genus, Haemophilus, was observed in AS, AS-IBD, IBD, AS patients with increased BASDAI, and IBD patients with faecal calprotectin >100 μg/mg. Apart from these genera, no other taxa were shared between AS and IBD patients. Conclusions: In conclusion, the distinct gut microbiome of AS and AS-IBD patients compared to IBD patients and healthy controls is consistent with immunological and genetic evidence suggesting that the gut plays a different role in driving AS compared with IBD. However, enrichment of two potentially pathogenic genera in both diseases suggests that the presence of a shared/common microbial trigger of disease cannot be discounted.",

keywords = "Ankylosing spondylitis, Dysbiosis, Gut, Inflammatory Bowel disease",

author = "Sternes, {P. R.} and L. Brett and J. Phipps and F. Ciccia and T. Kenna and {de Guzman}, E. and K. Zimmermann and M. Morrison and G. Holtmann and E. Klingberg and D. Mauro and C. McIvor and H. Forsblad-d{\textquoteright}Elia and Brown, {M. A.}",

note = "Funding Information: This study was supported the Australian government{\textquoteright}s National Health and Medical Research Council (NHMRC). The support did not include the design of the study, analysis, interpretation of data, and manuscript preparation. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1186/s13075-022-02853-3",

language = "English",

volume = "24",

journal = "Arthritis Research and Therapy",

issn = "1478-6354",

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number = "1",

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Sternes, PR, Brett, L, Phipps, J, Ciccia, F, Kenna, T, de Guzman, E, Zimmermann, K, Morrison, M, Holtmann, G, Klingberg, E, Mauro, D, McIvor, C, Forsblad-d’Elia, H & Brown, MA 2022, 'Distinctive gut microbiomes of ankylosing spondylitis and inflammatory bowel disease patients suggest differing roles in pathogenesis and correlate with disease activity', Arthritis Research and Therapy, vol. 24, no. 1, 163. https://doi.org/10.1186/s13075-022-02853-3

TY - JOUR

T1 - Distinctive gut microbiomes of ankylosing spondylitis and inflammatory bowel disease patients suggest differing roles in pathogenesis and correlate with disease activity

AU - Sternes, P. R.

AU - Brett, L.

AU - Phipps, J.

AU - Ciccia, F.

AU - Kenna, T.

AU - de Guzman, E.

AU - Zimmermann, K.

AU - Morrison, M.

AU - Holtmann, G.

AU - Klingberg, E.

AU - Mauro, D.

AU - McIvor, C.

AU - Forsblad-d’Elia, H.

AU - Brown, M. A.

N1 - Funding Information: This study was supported the Australian government’s National Health and Medical Research Council (NHMRC). The support did not include the design of the study, analysis, interpretation of data, and manuscript preparation. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - Background: Multiple studies have confirmed dysbiosis in ankylosing spondylitis (AS) and inflammatory bowel disease (IBD); however, due to methodological differences across studies, it has not been possible to determine if these diseases have similar or different gut microbiomes. Results: In this study, faecal and intestinal biopsies were obtained from 33 Australian AS patients (including 5 with concomitant IBD, ‘AS-IBD’), 59 IBD patients and 105 healthy controls. Stool samples were also obtained from 16 Italian AS patients and 136 Swedish AS patients. Focusing on the Australian cohort, AS, AS-IBD and IBD patients differed from one another and from healthy controls in both alpha and beta diversity. AS patients with and without clinical IBD could be distinguished from one another with moderate accuracy using stool microbiome (AUC=0.754). Stool microbiome also accurately distinguished IBD patients from healthy controls (AUC=0.757). Microbiome composition was correlated with disease activity measured by BASDAI and faecal calprotectin (FCP) levels. Enrichment of potentially pathogenic Streptococcus was noted in AS, AS-IBD and IBD patients. Furthermore, enrichment of another potentially pathogenic genus, Haemophilus, was observed in AS, AS-IBD, IBD, AS patients with increased BASDAI, and IBD patients with faecal calprotectin >100 μg/mg. Apart from these genera, no other taxa were shared between AS and IBD patients. Conclusions: In conclusion, the distinct gut microbiome of AS and AS-IBD patients compared to IBD patients and healthy controls is consistent with immunological and genetic evidence suggesting that the gut plays a different role in driving AS compared with IBD. However, enrichment of two potentially pathogenic genera in both diseases suggests that the presence of a shared/common microbial trigger of disease cannot be discounted.

AB - Background: Multiple studies have confirmed dysbiosis in ankylosing spondylitis (AS) and inflammatory bowel disease (IBD); however, due to methodological differences across studies, it has not been possible to determine if these diseases have similar or different gut microbiomes. Results: In this study, faecal and intestinal biopsies were obtained from 33 Australian AS patients (including 5 with concomitant IBD, ‘AS-IBD’), 59 IBD patients and 105 healthy controls. Stool samples were also obtained from 16 Italian AS patients and 136 Swedish AS patients. Focusing on the Australian cohort, AS, AS-IBD and IBD patients differed from one another and from healthy controls in both alpha and beta diversity. AS patients with and without clinical IBD could be distinguished from one another with moderate accuracy using stool microbiome (AUC=0.754). Stool microbiome also accurately distinguished IBD patients from healthy controls (AUC=0.757). Microbiome composition was correlated with disease activity measured by BASDAI and faecal calprotectin (FCP) levels. Enrichment of potentially pathogenic Streptococcus was noted in AS, AS-IBD and IBD patients. Furthermore, enrichment of another potentially pathogenic genus, Haemophilus, was observed in AS, AS-IBD, IBD, AS patients with increased BASDAI, and IBD patients with faecal calprotectin >100 μg/mg. Apart from these genera, no other taxa were shared between AS and IBD patients. Conclusions: In conclusion, the distinct gut microbiome of AS and AS-IBD patients compared to IBD patients and healthy controls is consistent with immunological and genetic evidence suggesting that the gut plays a different role in driving AS compared with IBD. However, enrichment of two potentially pathogenic genera in both diseases suggests that the presence of a shared/common microbial trigger of disease cannot be discounted.

KW - Ankylosing spondylitis

KW - Dysbiosis

KW - Gut

KW - Inflammatory Bowel disease

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U2 - 10.1186/s13075-022-02853-3

DO - 10.1186/s13075-022-02853-3

M3 - Article

AN - SCOPUS:85133517269

SN - 1478-6354

VL - 24

JO - Arthritis Research and Therapy

JF - Arthritis Research and Therapy

IS - 1

M1 - 163

ER -

Distinctive gut microbiomes of ankylosing spondylitis and inflammatory bowel disease patients suggest differing roles in pathogenesis and correlate with disease activity

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