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Cited by 359Exercise and Physiological ResponsesGastrointestinal motility and disordersCardiovascular and exercise physiology

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Exercise-Induced Splanchnic Hypoperfusion Results in Gut Dysfunction in Healthy Men

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van Wijck, Kim, Lenaerts, Kaatje, van Loon, Luc J. C., Peters, Wilbert H. M., Buurman, Wim A., Dejong, Cornelis H. C.·2011·PLoS ONE
DOI 10.1371/journal.pone.0022366PMC PMC3141050
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Abstract

BACKGROUND: Splanchnic hypoperfusion is common in various pathophysiological conditions and often considered to lead to gut dysfunction. While it is known that physiological situations such as physical exercise also result in splanchnic hypoperfusion, the consequences of flow redistribution at the expense of abdominal organs remained to be determined. This study focuses on the effects of splanchnic hypoperfusion on the gut, and the relationship between hypoperfusion, intestinal injury and permeability during physical exercise in healthy men. METHODS AND FINDINGS: Healthy men cycled for 60 minutes at 70% of maximum workload capacity. Splanchnic hypoperfusion was assessed using gastric tonometry. Blood, sampled every 10 minutes, was analyzed for enterocyte damage parameters (intestinal fatty acid binding protein (I-FABP) and ileal bile acid binding protein (I-BABP)). Changes in intestinal permeability were assessed using sugar probes. Furthermore, liver and renal parameters were assessed. Splanchnic perfusion rapidly decreased during exercise, reflected by increased gap(g-a)pCO(2) from -0.85±0.15 to 0.85±0.42 kPa (p<0.001). Hypoperfusion increased plasma I-FABP (615±118 vs. 309±46 pg/ml, p<0.001) and I-BABP (14.30±2.20 vs. 5.06±1.27 ng/ml, p<0.001), and hypoperfusion correlated significantly with this small intestinal damage (r(S) = 0.59; p<0.001). Last of all, plasma analysis revealed an increase in small intestinal permeability after exercise (p<0.001), which correlated with intestinal injury (r(S) = 0.50; p<0.001). Liver parameters, but not renal parameters were elevated. CONCLUSIONS: Exercise-induced splanchnic hypoperfusion results in quantifiable small intestinal injury. Importantly, the extent of intestinal injury correlates with transiently increased small intestinal permeability, indicating gut barrier dysfunction in healthy individuals. These physiological observations increase our knowledge of splanchnic hypoperfusion sequelae, and may help to understand and prevent these phenomena in patients.

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Figure 1 Physical exercise results in splanchnic hypoperfusion and intestinal cell damage. A) Gastric tonometry shows decreased splanchnic perfusion during cycling and post cycling (n = 9). B) Plasma I-FABP levels reflect the development of intestinal epithelial cell damage during cycling and post cycling in healthy volunteers (n = 20). C) Normalized plasma I-FABP levels measured during exercise tonometry correlate significantly with the normalized values of splanchnic hypoperfusion (gapg-a pCO2 t-20 min) in healthy men (samples from 9 men). Data are mean ± SEM. Different from baseline (t = 0) (* p<0.01, ** p<0.001, *** p<0.0001).
Figure 1 Physical exercise results in splanchnic hypoperfusion and intestinal cell damage. A) Gastric tonometry shows decreased splanchnic perfusion during cycling and post cycling (n = 9). B) Plasma I-FABP levels reflect the development of intestinal epithelial cell damage during cycling and post cycling in healthy volunteers (n = 20). C) Normalized plasma I-FABP levels measured during exercise tonometry correlate significantly with the normalized values of splanchnic hypoperfusion (gapg-a pCO2 t-20 min) in healthy men (samples from 9 men). Data are mean ± SEM. Different from baseline (t = 0) (* p<0.01, ** p<0.001, *** p<0.0001).CC BY · PubMed Central
Figure 2 Physical exercise leads to ileal epithelial damage and inflammation, but does not result in renal injury. A) Increased plasma IBABP levels point toward the development of exercise-induced ileal epithelial cell damage. B) Urinary NAG levels indicate absence of renal damage after cycling. Increased plasma MPO (C) and calprotectin (D) levels reveal exercise-induced inflammation in healthy volunteers. Data are mean ± SEM (n = 20). Different from baseline (t = 0) (NS, not significant; ** p<0.001, *** p<0.0001).
Figure 2 Physical exercise leads to ileal epithelial damage and inflammation, but does not result in renal injury. A) Increased plasma IBABP levels point toward the development of exercise-induced ileal epithelial cell damage. B) Urinary NAG levels indicate absence of renal damage after cycling. Increased plasma MPO (C) and calprotectin (D) levels reveal exercise-induced inflammation in healthy volunteers. Data are mean ± SEM (n = 20). Different from baseline (t = 0) (NS, not significant; ** p<0.001, *** p<0.0001).CC BY · PubMed Central
Figure 3 Physical exercise is associated with liver damage. Plasma L-FABP (A), ALT (B), AST (C), and alpha GST (D) suggest liver injury after cycling. Data are mean ± SEM (n = 20) of samples collected before, immediately after and 1 hour post cycling (* p<0.05, ** p<0.01, *** p<0.001).
Figure 3 Physical exercise is associated with liver damage. Plasma L-FABP (A), ALT (B), AST (C), and alpha GST (D) suggest liver injury after cycling. Data are mean ± SEM (n = 20) of samples collected before, immediately after and 1 hour post cycling (* p<0.05, ** p<0.01, *** p<0.001).CC BY · PubMed Central
Figure 4 Physical exercise induces a mild increase in small intestinal permeability. A) Urinary L/R ratios over time are elevated from baseline, especially in the first 2 hours after cycling, but not to a significant level. B) Plasma permeability analysis revealed an overall increase in small intestinal permeability after exercise compared to rest (P<0.001). Plasma L/R ratios after exercise at individual time points were not significantly different from L/R ratios in rest. C) Permeability of the large intestine, reflected by the 5–24 h urinary S/E ratio, remains unaltered during exercise. Data are mean ± SEM (n = 6). Different from baseline (t = 0) (NS, not significant; ** p<0.001).
Figure 4 Physical exercise induces a mild increase in small intestinal permeability. A) Urinary L/R ratios over time are elevated from baseline, especially in the first 2 hours after cycling, but not to a significant level. B) Plasma permeability analysis revealed an overall increase in small intestinal permeability after exercise compared to rest (P<0.001). Plasma L/R ratios after exercise at individual time points were not significantly different from L/R ratios in rest. C) Permeability of the large intestine, reflected by the 5–24 h urinary S/E ratio, remains unaltered during exercise. Data are mean ± SEM (n = 6). Different from baseline (t = 0) (NS, not significant; ** p<0.001).CC BY · PubMed Central

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Metadata

Authors
van Wijck, K., Lenaerts, K., van Loon, L. J. C., Peters, W. H. M., Buurman, W. A., & Dejong, C. H. C.
Affiliations
  • Maastricht University Medical Centre (NL)
  • Radboud University Nijmegen (NL)
Corresponding author
Lenaerts, Kaatje
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2011-07-21
Volume
6
Issue
7
Pages
e22366
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0022366
PMC
PMC3141050
OpenAlex
W1986330043
Cited by
359
References
48
Citations by year
2026: 26 · 2025: 28 · 2024: 21 · 2023: 32 · 2022: 32 · 2021: 33 · 2020: 30 · 2019: 24 · 2018: 24 · 2017: 27 · 2016: 18 · 2015: 12 · 2014: 17 · 2013: 18 · 2012: 15
FWCI
16.54
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Radboud Repository (Radboud University) (submittedVersion, other-oa)
  • Research Bank (Australian Catholic University) (submittedVersion, cc-by)
  • Research Publications (Maastricht University) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Radboud Repository (Radboud University) (submittedVersion)
  • Research Publications (Maastricht University) (submittedVersion, other-oa)
Funders
GlaxoSmithKline
Topics
  • Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
  • Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
Keywords
splanchnic hypoperfusion, physical activity, gastrointestinal dysfunction, intestinal injury, intestinal permeability, intestinal barrier dysfunction, gastric tonometry, intestinal fatty acid binding protein, ileal bile acid binding protein, small intestine, healthy men
MeSH terms
Bacteria, Health, Humans, Inflammation, Kidney, Liver, Male, Perfusion, Permeability, Splanchnic Circulation, Exercise, Gastrointestinal Tract, Young Adult

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