Interleukin-17 Inhibition in Spondyloarthritis Is Associated With Subclinical Gut Microbiome Perturbations and a Distinctive Interleukin-25-Driven Intestinal Inflammation

Arthritis Rheumatol. 2020 Apr;72(4):645-657. doi: 10.1002/art.41169. Epub 2020 Mar 12.

Abstract

Objective: To characterize the ecological effects of biologic therapies on the gut bacterial and fungal microbiome in psoriatic arthritis (PsA)/spondyloarthritis (SpA) patients.

Methods: Fecal samples from PsA/SpA patients pre- and posttreatment with tumor necrosis factor inhibitors (TNFi; n = 15) or an anti-interleukin-17A monoclonal antibody inhibitor (IL-17i; n = 14) underwent sequencing (16S ribosomal RNA, internal transcribed spacer and shotgun metagenomics) and computational microbiome analysis. Fecal levels of fatty acid metabolites and cytokines/proteins implicated in PsA/SpA pathogenesis or intestinal inflammation were correlated with sequence data. Additionally, ileal biopsies obtained from SpA patients who developed clinically overt Crohn's disease (CD) after treatment with IL-17i (n = 5) were analyzed for expression of IL-23/Th17-related cytokines, IL-25/IL-17E-producing cells, and type 2 innate lymphoid cells (ILC2s).

Results: There were significant shifts in abundance of specific taxa after treatment with IL-17i compared to TNFi, particularly Clostridiales (P = 0.016) and Candida albicans (P = 0.041). These subclinical alterations correlated with changes in bacterial community co-occurrence, metabolic pathways, IL-23/Th17-related cytokines, and various fatty acids. Ileal biopsies showed that clinically overt CD was associated with expansion of IL-25/IL-17E-producing tuft cells and ILC2s (P < 0.05), compared to pre-IL-17i treatment levels.

Conclusion: In a subgroup of SpA patients, the initiation of IL-17A blockade correlated with features of subclinical gut inflammation and intestinal dysbiosis of certain bacterial and fungal taxa, most notably C albicans. Further, IL-17i-related CD was associated with overexpression of IL-25/IL-17E-producing tuft cells and ILC2s. These results may help to explain the potential link between inhibition of a specific IL-17 pathway and the (sub)clinical gut inflammation observed in SpA.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Monoclonal, Humanized / pharmacology
  • Antibodies, Monoclonal, Humanized / therapeutic use*
  • Arthritis, Psoriatic / drug therapy*
  • Arthritis, Psoriatic / metabolism
  • Arthritis, Psoriatic / microbiology
  • Female
  • Gastrointestinal Microbiome / drug effects*
  • Humans
  • Inflammation / metabolism*
  • Interleukin-17 / immunology*
  • Intestinal Mucosa / metabolism
  • Intestines / drug effects
  • Intestines / microbiology
  • Male
  • Middle Aged
  • Spondylarthritis / drug therapy*
  • Spondylarthritis / metabolism
  • Spondylarthritis / microbiology
  • Tumor Necrosis Factor Inhibitors / pharmacology
  • Tumor Necrosis Factor Inhibitors / therapeutic use*

Substances

  • Antibodies, Monoclonal, Humanized
  • Interleukin-17
  • Tumor Necrosis Factor Inhibitors
  • secukinumab