Endurance exercise and gut microbiota: A review

Núria Mach, Dolors Fuster-Botella, Núria Mach, Dolors Fuster-Botella

Abstract

Background: The physiological and biochemical demands of intense exercise elicit both muscle-based and systemic responses. The main adaptations to endurance exercise include the correction of electrolyte imbalance, a decrease in glycogen storage and the increase of oxidative stress, intestinal permeability, muscle damage, and systemic inflammatory response. Adaptations to exercise might be influenced by the gut microbiota, which plays an important role in the production, storage, and expenditure of energy obtained from the diet as well as in inflammation, redox reactions, and hydration status.

Methods: A systematic and comprehensive search of electronic databases, including MEDLINE, Scopus, ClinicalTrials.gov, ScienceDirect, Springer Link, and EMBASE was done. The search process was completed using the keywords: "endurance", "exercise", "immune response", "microbiota", "nutrition", and "probiotics".

Results: Reviewed literature supports the hypothesis that intestinal microbiota might be able to provide a measureable, effective marker of an athlete's immune function and that microbial composition analysis might also be sensitive enough to detect exercise-induced stress and metabolic disorders. The review also supports the hypothesis that modifying the microbiota through the use of probiotics could be an important therapeutic tool to improve athletes' overall general health, performance, and energy availability while controlling inflammation and redox levels.

Conclusion: The present review provides a comprehensive overview of how gut microbiota may have a key role in controlling the oxidative stress and inflammatory responses as well as improving metabolism and energy expenditure during intense exercise.

Keywords: Endurance; Exercise; Immune response; Microbiota; Nutrition; Probiotics.

Figures

Fig. 1
Fig. 1
The physiological and biochemical demands of endurance exercise elicit both muscle-based and systemic responses. The main adaptations to endurance exercise include an improvement of mechanical, metabolic, neuromuscular and contractile functions in muscle, a rebalance of electrolytes, a decrease in glycogen storage and an increase in mitochondrial biogenesis in muscle tissue. Moreover, endurance exercise has a profound impact on oxidative stress, intestinal permeability, muscle damage, systemic inflammation and immune responses. Additionally, there is increased ventilation and pumping function of the heart associated with substantially decreased peripheral vascular resistance in the muscles. This facilitates the delivery of oxygen and nutrients to working muscles, which consume high amounts of oxygen and nutrients, especially when exercise intensity increases. ↑: increases; ↔: no change in response; ↓: decreases; ↕: may increase or decrease.
Fig. 2
Fig. 2
Complex polysaccharides are metabolized by the colonic microbiota to oligosaccharides and monosaccharides and then fermented to short-chain fatty acid (SCFA) end products, mainly acetate, propionate, and butyrate. The SCFAs are absorbed in the colon, where butyrate provides energy for colonic epithelial cells, and acetate and propionate reach the liver and peripheral organs, where they are substrates for gluconeogenesis and lipogenesis. The types and amount of SCFAs produced by gut microorganisms are determined by the composition of the gut microbiota and the metabolic interactions between specie. In addition to being energy sources, SCFAs control colonic gene expression involved in the immune response. It must be borne in mind that endurance diets are rich in protein (1.2–1.6 g/kg/day), which besides liberating beneficial SCFAs, produces a range of potentially harmful compounds in the intestine.
Fig. 3
Fig. 3
Endurance: crosstalk between intestinal microbiota, immune responses and redox status. Endurance exercise may cause an increase in the number of pro-inflammatory cytokines, such as TNF-α, IL-1, IL-6, IL-1 receptor antagonist, TNF receptors, but also anti-inflammatory modulators (e.g., IL-10, IL-8), sIgA and intestinal lymphocytes. In turn, this inflammatory response may induce disbiosis and modifications of intestinal microbiome composition and their secreted products. Additionally there is an increase of tissue hyperthermia, gastrointestinal permeability and destruction of gut mucous thickness. Moreover, the activity of antioxidant enzymes may become weaker, which modify the mesenteric redox environment. In parallel, the epithelial barrier disruption enhances the TLRs-mediated recognition of gut commensal bacteria by effector cell types, which potentiate the immune response. IgA = immunoglobulin A; IL = interleukin; RONS = reactive oxygen and nitrogen species; ROS = reactive oxygen species; sIgA = secretory IgA; TLRs = toll-like receptors; TNF = tumor necrosis factor.

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