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Cited by 448Probiotics and Fermented FoodsGut microbiota and healthInflammatory Bowel Disease

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Bifidobacterium infantis35624 modulates host inflammatory processes beyond the gut

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Groeger, David, O’Mahony, Liam, Murphy, Eileen F., Bourke, John F., Dinan, Timothy G., Kiely, Barry, Shanahan, Fergus, Quigley, Eamonn M.M.·2013·Gut Microbes
DOI 10.4161/gmic.25487PMC PMC3744517
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Abstract

Certain therapeutic microbes, including Bifidobacteria infantis (B. infantis) 35624 exert beneficial immunoregulatory effects by mimicking commensal-immune interactions; however, the value of these effects in patients with non-gastrointestinal inflammatory conditions remains unclear. In this study, we assessed the impact of oral administration of B. infantis 35624, for 6‒8 weeks on inflammatory biomarker and plasma cytokine levels in patients with ulcerative colitis (UC) (n = 22), chronic fatigue syndrome (CFS) (n = 48) and psoriasis (n = 26) in three separate randomized, double-blind, placebo-controlled interventions. Additionally, the effect of B. infantis 35624 on immunological biomarkers in healthy subjects (n = 22) was assessed. At baseline, both gastrointestinal (UC) and non-gastrointestinal (CFS and psoriasis) patients had significantly increased plasma levels of C-reactive protein (CRP) and the pro-inflammatory cytokines tumor necrosis factor α (TNF-α) and interleukin-6 (IL-6) compared with healthy volunteers. B. infantis 35624 feeding resulted in reduced plasma CRP levels in all three inflammatory disorders compared with placebo. Interestingly, plasma TNF-α was reduced in CFS and psoriasis while IL-6 was reduced in UC and CFS. Furthermore, in healthy subjects, LPS-stimulated TNF-α and IL-6 secretion by peripheral blood mononuclear cells (PBMCs) was significantly reduced in the B. infantis 35624-treated groups compared with placebo following eight weeks of feeding. These results demonstrate the ability of this microbe to reduce systemic pro-inflammatory biomarkers in both gastrointestinal and non-gastrointestinal conditions. In conclusion, these data show that the immunomodulatory effects of the microbiota in humans are not limited to the mucosal immune system but extend to the systemic immune system.

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Figure 1. Plasma pro-inflammatory biomarkers are elevated in patients with inflammatory disorders. Plasma CRP and pro-inflammatory cytokines levels are significantly elevated in chronic fatigue syndrome (CFS) (n = 48), psoriasis (n = 26) and ulcerative colitis (UC) (n = 22) patients compared with healthy volunteers (n = 35). Results are expressed as median values. (Healthy volunteers vs. each inflammatory disorder) (Mann-Whitney U test) p < 0.05 *, p < 0.01 ** p < 0.01 ***.
Figure 1. Plasma pro-inflammatory biomarkers are elevated in patients with inflammatory disorders. Plasma CRP and pro-inflammatory cytokines levels are significantly elevated in chronic fatigue syndrome (CFS) (n = 48), psoriasis (n = 26) and ulcerative colitis (UC) (n = 22) patients compared with healthy volunteers (n = 35). Results are expressed as median values. (Healthy volunteers vs. each inflammatory disorder) (Mann-Whitney U test) p < 0.05 *, p < 0.01 ** p < 0.01 ***.CC BY-NC · PubMed Central
Figure 2.B. infantis 35624-feeding reduces plasma CRP levels compared with placebo. Plasma levels of CRP were significantly reduced in the B. infantis 35624 treated groups compared with placebo treatment following 6–8 weeks of feeding in patients with chronic fatigue syndrome (CFS), psoriasis and ulcerative colitis (UC). Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each patient. *p < 0.05 vs. placebo; (Mann-Whitney U test).
Figure 2.B. infantis 35624-feeding reduces plasma CRP levels compared with placebo. Plasma levels of CRP were significantly reduced in the B. infantis 35624 treated groups compared with placebo treatment following 6–8 weeks of feeding in patients with chronic fatigue syndrome (CFS), psoriasis and ulcerative colitis (UC). Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each patient. *p < 0.05 vs. placebo; (Mann-Whitney U test).CC BY-NC · PubMed Central
Figure 3.B. infantis 35624-feeding reduces plasma CRP levels compared with pretreatment level. Placebo-feeding for 8 weeks did not alter plasma CRP levels compared with pretreatment levels in any patients with inflammatory disorders. Plasma CRP levels were significantly reduced following 8 weeks of feeding with B. infantis 35624 compared with pretreatment levels in (A) psoriasis (n = 12). and (B) chronic fatigue syndrome (CFS) (n = 28), However, there was no difference in CRP levels following 6 weeks feeding with B. infantis 35624 in patients with (C) ulcerative colitis (UC) (n = 13) compared with their pretreatment levels. Results are expressed as the individual responses of each patient (mg/L) (pre-treatment vs. post-treatment level) *p < 0.05 (Wilcoxon matched pair test).
Figure 3.B. infantis 35624-feeding reduces plasma CRP levels compared with pretreatment level. Placebo-feeding for 8 weeks did not alter plasma CRP levels compared with pretreatment levels in any patients with inflammatory disorders. Plasma CRP levels were significantly reduced following 8 weeks of feeding with B. infantis 35624 compared with pretreatment levels in (A) psoriasis (n = 12). and (B) chronic fatigue syndrome (CFS) (n = 28), However, there was no difference in CRP levels following 6 weeks feeding with B. infantis 35624 in patients with (C) ulcerative colitis (UC) (n = 13) compared with their pretreatment levels. Results are expressed as the individual responses of each patient (mg/L) (pre-treatment vs. post-treatment level) *p < 0.05 (Wilcoxon matched pair test).CC BY-NC · PubMed Central
Figure 4.B. infantis 35624-feeding reduces plasma TNF-α levels compared with placebo. Plasma levels of TNF-α were significantly reduced in the B. infantis 35624-treated groups compared with placebo treatment following 8 weeks of feeding in patients with chronic fatigue syndrome (CFS) and psoriasis. However, there was no difference in TNF-α levels following 6 weeks feeding with B. infantis 35624 in patients with ulcerative colitis (UC) compared with placebo treatment. Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each patient. *p < 0.05 vs. placebo; (Mann-Whitney U test).
Figure 4.B. infantis 35624-feeding reduces plasma TNF-α levels compared with placebo. Plasma levels of TNF-α were significantly reduced in the B. infantis 35624-treated groups compared with placebo treatment following 8 weeks of feeding in patients with chronic fatigue syndrome (CFS) and psoriasis. However, there was no difference in TNF-α levels following 6 weeks feeding with B. infantis 35624 in patients with ulcerative colitis (UC) compared with placebo treatment. Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each patient. *p < 0.05 vs. placebo; (Mann-Whitney U test).CC BY-NC · PubMed Central
Figure 5.B. infantis 35624-feeding reduces plasma TNF-α levels compared with pretreatment level. Placebo treatment did not alter plasma TNF-α levels, compared with pretreatment levels, in all the patient groups tested. Plasma TNF-α levels were significantly reduced following 8 weeks of feeding with B. infantis 35624, compared with pretreatment levels, in (A) psoriasis (n = 12) and (B) chronic fatigue syndrome (CFS) (n = 28). However there was no difference in TNF-α levels following 6 weeks feeding with B. infantis 35624 in patients with (C) ulcerative colitis (UC) (n = 13) compared with their pretreatment levels. Results are expressed as the individual responses of each patient (pg/ml) (pre-treatment vs. post-treatment level) *p < 0.05 (Wilcoxon matched pair test).
Figure 5.B. infantis 35624-feeding reduces plasma TNF-α levels compared with pretreatment level. Placebo treatment did not alter plasma TNF-α levels, compared with pretreatment levels, in all the patient groups tested. Plasma TNF-α levels were significantly reduced following 8 weeks of feeding with B. infantis 35624, compared with pretreatment levels, in (A) psoriasis (n = 12) and (B) chronic fatigue syndrome (CFS) (n = 28). However there was no difference in TNF-α levels following 6 weeks feeding with B. infantis 35624 in patients with (C) ulcerative colitis (UC) (n = 13) compared with their pretreatment levels. Results are expressed as the individual responses of each patient (pg/ml) (pre-treatment vs. post-treatment level) *p < 0.05 (Wilcoxon matched pair test).CC BY-NC · PubMed Central
Figure 6.B. infantis 35624-feeding reduces plasma IL-6 levels compared with placebo. Plasma levels of IL-6 were reduced in the B. infantis 35624 treated groups compared with placebo treatment following 6–8 weeks of feeding in patients with chronic fatigue syndrome (CFS) (#p = 0.054) and ulcerative colitis (UC) (~p = 0.057). However, there was no difference in IL-6 levels following 8 weeks feeding with B. infantis 35624 in patients with psoriasis compared with placebo treatment. Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each patient. *p < 0.05 vs. placebo groups (Mann-Whitney U test).
Figure 6.B. infantis 35624-feeding reduces plasma IL-6 levels compared with placebo. Plasma levels of IL-6 were reduced in the B. infantis 35624 treated groups compared with placebo treatment following 6–8 weeks of feeding in patients with chronic fatigue syndrome (CFS) (#p = 0.054) and ulcerative colitis (UC) (~p = 0.057). However, there was no difference in IL-6 levels following 8 weeks feeding with B. infantis 35624 in patients with psoriasis compared with placebo treatment. Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each patient. *p < 0.05 vs. placebo groups (Mann-Whitney U test).CC BY-NC · PubMed Central
Figure 7.B. infantis 35624-feeding reduces plasma IL-6 levels compared with pretreatment level. There was no change in plasma IL-6 levels following 8 weeks feeding with placebo, compared with pretreatment levels, in patients with inflammatory disorders. Plasma IL-6 levels were significantly reduced following 8 weeks of feeding with B. infantis 35624 compared with pretreatment levels in patients with chronic fatigue syndrome (CFS) (n = 28). However, there was no difference in IL-6 levels following 6 or 8 weeks feeding respectively with B. infantis 35624 in patients with ulcerative colitis (UC) (n = 13) or psoriasis (n = 12) compared with their pretreatment levels. Results are expressed as the individual responses of each patient (pg/ml) (pre-treatment vs. post-treatment level) **p < 0.01 (Wilcoxon matched pair test).
Figure 7.B. infantis 35624-feeding reduces plasma IL-6 levels compared with pretreatment level. There was no change in plasma IL-6 levels following 8 weeks feeding with placebo, compared with pretreatment levels, in patients with inflammatory disorders. Plasma IL-6 levels were significantly reduced following 8 weeks of feeding with B. infantis 35624 compared with pretreatment levels in patients with chronic fatigue syndrome (CFS) (n = 28). However, there was no difference in IL-6 levels following 6 or 8 weeks feeding respectively with B. infantis 35624 in patients with ulcerative colitis (UC) (n = 13) or psoriasis (n = 12) compared with their pretreatment levels. Results are expressed as the individual responses of each patient (pg/ml) (pre-treatment vs. post-treatment level) **p < 0.01 (Wilcoxon matched pair test).CC BY-NC · PubMed Central
Figure 8.B. infantis 35624-feeding reduces pro-inflammatory biomarkers in a highly correlated way in inflammatory disorder patients. 3D Cluster analysis of plasma levels of CRP (z), TNF-α (x) and IL-6 (y) from patients with psoriasis and ulcerative colitis (UC) and of CRP (x), IL-6 (y) and TNF-α (z) from patients with chronic fatigue syndrome (CFS) displayed a separation between the B. infantis 35624 treated groups compared with the placebo treated groups. Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each patient.
Figure 8.B. infantis 35624-feeding reduces pro-inflammatory biomarkers in a highly correlated way in inflammatory disorder patients. 3D Cluster analysis of plasma levels of CRP (z), TNF-α (x) and IL-6 (y) from patients with psoriasis and ulcerative colitis (UC) and of CRP (x), IL-6 (y) and TNF-α (z) from patients with chronic fatigue syndrome (CFS) displayed a separation between the B. infantis 35624 treated groups compared with the placebo treated groups. Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each patient.CC BY-NC · PubMed Central
Figure 9.B. infantis 35624-feeding reduces pro-inflammatory cytokines levels from LPS stimulated PBMCs in healthy volunteers. In vitro LPS stimulated PBMCs displayed decreased secretion of IL-6 and TNF-α following B. infantis 35624 oral consumption (n = 10) for eight weeks. This finding was not observed in the placebo group (n = 12). Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each individual. *p < 0.05 vs. placebo group (Mann-Whitney U test).
Figure 9.B. infantis 35624-feeding reduces pro-inflammatory cytokines levels from LPS stimulated PBMCs in healthy volunteers. In vitro LPS stimulated PBMCs displayed decreased secretion of IL-6 and TNF-α following B. infantis 35624 oral consumption (n = 10) for eight weeks. This finding was not observed in the placebo group (n = 12). Results are expressed as the change from baseline (post-treatment minus pre-treatment level) for each individual. *p < 0.05 vs. placebo group (Mann-Whitney U test).CC BY-NC · PubMed Central

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  1. Biljan D, 2009, Coll Antropol, 33, 83
  2. Federico A, 2009, Eur Rev Med Pharmacol Sci, 13, 285

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Metadata

Authors
Groeger, D., O’Mahony, L., Murphy, E. F., Bourke, J. F., Dinan, T. G., Kiely, B., Shanahan, F., & Quigley, E. M. M.
Affiliations
  • Alimentary Health (Ireland) (IE)
  • University of Zurich (CH)
  • South Infirmary Victoria University Hospital (IE)
  • University College Cork (IE)
Corresponding author
Quigley, Eamonn M.M.
ORCID
Venue
Gut Microbes
Publisher
Informa UK Limited
Published
2013-07-12
Volume
4
Issue
4
Pages
325-339
ISSN
  • 1949-0976 (ISSN-L)
  • 1949-0984
DOI
10.4161/gmic.25487
PMC
PMC3744517
OpenAlex
W2056812430
Cited by
448
References
57
Citations by year
2026: 16 · 2025: 52 · 2024: 54 · 2023: 52 · 2022: 56 · 2021: 40 · 2020: 29 · 2019: 36 · 2018: 28 · 2017: 30 · 2016: 16 · 2015: 21 · 2014: 15 · 2013: 3
FWCI
27.31
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Gut Microbes (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
Keywords
probiotics, immunomodulation, ulcerative colitis, chronic fatigue syndrome, psoriasis, systemic inflammation, C-reactive protein, TNF-α, interleukin-6, peripheral blood mononuclear cells, gut microbiota
MeSH terms
Administration, Oral, Adolescent, Adult, Aged, Bifidobacterium, C-Reactive Protein, Colitis, Ulcerative, Double-Blind Method, Female, Humans, Immunosuppression Therapy, Male, Middle Aged, Placebos, Psoriasis, Fatigue Syndrome, Chronic, Cytokines, Treatment Outcome, Probiotics, Gastrointestinal Tract, Young Adult

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