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Cited by 333Gut microbiota and healthAdipokines, Inflammation, and Metabolic DiseasesOral microbiology and periodontitis research

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Exercise Training Modulates Gut Microbiota Profile and Improves Endotoxemia

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MOTIANI, KUMAIL K., COLLADO, M. CARMEN, ESKELINEN, JARI-JOONAS, VIRTANEN, KIRSI A., LÖYTTYNIEMI, ELIISA, SALMINEN, SEPPO, NUUTILA, PIRJO, KALLIOKOSKI, KARI K., HANNUKAINEN, JARNA C.·2020·Medicine & Science in Sports & Exercise
DOI 10.1249/mss.0000000000002112PMC PMC7028471
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Abstract

Introduction: Intestinal metabolism and microbiota profiles are impaired in obesity and insulin resistance. Moreover, dysbiotic gut microbiota has been suggested to promote systemic low-grade inflammation and insulin resistance through the release of endotoxins particularly lipopolysaccharides. We have previously shown that exercise training improves intestinal metabolism in healthy men. To understand whether changes in intestinal metabolism interact with gut microbiota and its release of inflammatory markers, we studied the effects of sprint interval (SIT) and moderate-intensity continuous training (MICT) on intestinal metabolism and microbiota in subjects with insulin resistance. Methods: Twenty-six, sedentary subjects (prediabetic, n = 9; type 2 diabetes, n = 17; age, 49 [SD, 4] yr; body mass index, 30.5 [SD, 3]) were randomized into SIT or MICT. Intestinal insulin-stimulated glucose uptake (GU) and fatty acid uptake (FAU) from circulation were measured using positron emission tomography. Gut microbiota composition was analyzed by 16S rRNA gene sequencing and serum inflammatory markers with multiplex assays and enzyme-linked immunoassay kit. Results: V˙O 2peak improved only after SIT ( P = 0.01). Both training modes reduced systematic and intestinal inflammatory markers (tumor necrosis factor-α, lipopolysaccharide binding protein) (time P < 0.05). Training modified microbiota profile by increasing Bacteroidetes phylum (time P = 0.03) and decreasing Firmicutes/Bacteroidetes ratio (time P = 0.04). Moreover, there was a decrease in Clostridium genus (time P = 0.04) and Blautia (time P = 0.051). Only MICT decreased jejunal FAU ( P = 0.02). Training had no significant effect on intestinal GU. Colonic GU associated positively with Bacteroidetes and inversely with Firmicutes phylum, ratio Firmicutes/Bacteroidetes and Blautia genus. Conclusions: Intestinal substrate uptake associates with gut microbiota composition and whole-body insulin sensitivity. Exercise training improves gut microbiota profiles and reduces endotoxemia.

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FIGURE 1 A, Consort flow diagram showing the total number of subjects recruited and analyzed. B, Study design: Subjects were studied on three separate days before and after the exercise intervention. OGTT, oral glucose tolerance test.
FIGURE 1 A, Consort flow diagram showing the total number of subjects recruited and analyzed. B, Study design: Subjects were studied on three separate days before and after the exercise intervention. OGTT, oral glucose tolerance test.CC BY-NC-ND · PubMed Central
FIGURE 2 Impact of exercise intervention on specific inflammatory markers. A, TNF α, (B) CRP, and (C) LBP. All values are expressed as model-based means and bars are 95% CI. (§) Log transformation was performed to achieve normal distribution. *P value for time interaction (i.e., the groups (SIT + MICT) behaved similarly for the change in the parameter with a significant difference between them.
FIGURE 2 Impact of exercise intervention on specific inflammatory markers. A, TNF α, (B) CRP, and (C) LBP. All values are expressed as model-based means and bars are 95% CI. (§) Log transformation was performed to achieve normal distribution. *P value for time interaction (i.e., the groups (SIT + MICT) behaved similarly for the change in the parameter with a significant difference between them.CC BY-NC-ND · PubMed Central
FIGURE 3 Impact of exercise intervention on the gut microbiota composition. A, Ratio (Firmicutes/Bacteroidetes), (B) Bacteroidetes, and the genus (C) Blautia and (D) Clostridium. All values are expressed as model-based means and bars are 95% CI. (§) Log transformation was performed to achieve normal distribution. *P value for time interaction (i.e., the groups (SIT + MICT) behaved similarly for the change in the parameter with a significant difference between them.
FIGURE 3 Impact of exercise intervention on the gut microbiota composition. A, Ratio (Firmicutes/Bacteroidetes), (B) Bacteroidetes, and the genus (C) Blautia and (D) Clostridium. All values are expressed as model-based means and bars are 95% CI. (§) Log transformation was performed to achieve normal distribution. *P value for time interaction (i.e., the groups (SIT + MICT) behaved similarly for the change in the parameter with a significant difference between them.CC BY-NC-ND · PubMed Central
FIGURE 4 A, Insulin-stimulated GU and (B) fasting free FAU in different parts of intestine before and after 2 wk of either SIT or MICT. All values are expressed as model-based means and bars are 95% CI. (§) Log transformation was performed to achieve normal distribution. **P value for time–training interaction (i.e., the groups behaved differently for the change in the parameter with a significant difference between them).
FIGURE 4 A, Insulin-stimulated GU and (B) fasting free FAU in different parts of intestine before and after 2 wk of either SIT or MICT. All values are expressed as model-based means and bars are 95% CI. (§) Log transformation was performed to achieve normal distribution. **P value for time–training interaction (i.e., the groups behaved differently for the change in the parameter with a significant difference between them).CC BY-NC-ND · PubMed Central
FIGURE 5 Correlation between insulin-stimulated colonic GU and (A) Firmicutes (B) Ratio (Firmicutes/Bacteroidetes), (C) Blautia, and (D) Bacteroides phylum in pooled analysis of both SIT and MICT subjects at baseline. (◊) SIT and (●) MICT. (§) Log transformation was performed to achieve normal distribution.
FIGURE 5 Correlation between insulin-stimulated colonic GU and (A) Firmicutes (B) Ratio (Firmicutes/Bacteroidetes), (C) Blautia, and (D) Bacteroides phylum in pooled analysis of both SIT and MICT subjects at baseline. (◊) SIT and (●) MICT. (§) Log transformation was performed to achieve normal distribution.CC BY-NC-ND · PubMed Central

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Authors
MOTIANI, K. K., COLLADO, M. C., ESKELINEN, J.-J., VIRTANEN, K. A., LÖYTTYNIEMI, E., SALMINEN, S., NUUTILA, P., KALLIOKOSKI, K. K., & HANNUKAINEN, J. C.
Affiliations
  • University of Turku (FI)
  • Consejo Superior de Investigaciones Científicas (ES)
  • Turku University Hospital (FI)
ORCID
Venue
Medicine & Science in Sports & Exercise
Publisher
Ovid Technologies (Wolters Kluwer Health)
Published
2019-08-19
Volume
52
Issue
1
Pages
94-104
ISSN
  • 0195-9131 (ISSN-L)
  • 1530-0315
DOI
10.1249/mss.0000000000002112
PMC
PMC7028471
OpenAlex
W2969245839
Cited by
333
References
54
Citations by year
2026: 39 · 2025: 68 · 2024: 64 · 2023: 58 · 2022: 48 · 2021: 40 · 2020: 13 · 2019: 2
FWCI
8.52
Type
journal article
Language
en
Open access
Licence
Locations
  • Medicine & Science in Sports & Exercise (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by-nc-nd)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
  • Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Keywords
exercise training, gut microbiota, endotoxemia, lipopolysaccharide, insulin resistance, type 2 diabetes, prediabetes, sprint interval training, moderate-intensity continuous training, intestinal glucose absorption, fatty acid uptake, Bacteroidetes, Firmicutes/Bacteroidetes ratio, Blautia, Clostridium, low-grade inflammation, intestinal metabolism
MeSH terms
Gastrointestinal Microbiome, Lipopolysaccharide-Binding Protein, Acute-Phase Proteins, Carrier Proteins, Diabetes Mellitus, Type 2, Female, Humans, Inflammation, Insulin Resistance, Intestinal Mucosa, Male, Membrane Glycoproteins, Middle Aged, Obesity, Oxygen Consumption, Prediabetic State, Tumor Necrosis Factor-alpha, Biomarkers, Body Mass Index, Endotoxemia, Physical Conditioning, Human

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