Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes

In the paper

“For instance, induced exercise-stress decreased cecal levels of Turicibacter spp and increased Ruminococcus gnavus, which have well defined roles in intestinal mucus degradation and immune function.”

What the sources say

• Not checked yetcites [52] Allen JM, 2015, J Appl Physiol (1985) source

In the paper

“Other ways of communications between the gut-brain axis are: (i) gut hormones [9] (i.e. gamma aminobutyric acid (GABA), neuropeptide Y, dopamine) and (ii) gut microbiota molecules [10, 11] (i.e. short chain fatty acids (SCFA), tryptophan).”

What the sources say

• Not checked yetcites [9] Rhee SH, 2009, Nat Rev Gastroenterol Hepatol source
• Not checked yetcites [10] Lyte M, 2011, Cell Tissue Res source
• Not checked yetcites [11] Stilling RM, 2014, Genes Brain Behav source

In the paper

“The gut microbiome and its influence on host behavior, intestinal barrier and immune function are believed to be a critical aspect of the brain-gut axis.”

In the paper

“Briefly, exercise-induced stress results in activation of preganglionic sympathetic neurons in the intermediolateral cell column of the thoracolumbar spinal cord (shown in purple and clear grey). This sympathetic activation represents the classic 'fight or flight' response and it generally increases circulating levels of catecholamines.”

What the sources say

• Not checked yetcites [6] Ulrich-Lai YM, 2009, Nat Rev Neurosci source

In the paper

“The activation of these axes results in the release of catecholamines (norepinephrine (NE) and epinephrine) and glucocorticoids into circulatory system (reviewed by Ulrich-Lai et al [6]”

What the sources say

• Not checked yetcites [6] Ulrich-Lai YM, 2009, Nat Rev Neurosci source

In the paper

“What is troubling is that dietary recommendations for elite athletes are primarily based on a low consumption of plant polysaccharides, which is associated with reduced microbiota diversity and functionality (e.g. less synthesis of byproducts such as short chain fatty acids and neurotransmitters).”

What the sources say

• Not checked yetcites [28] Rodriguez NR, 2009, Med Sci Sports Exerc source

In the paper

“some preliminary experimental data obtained from studies using probiotics and prebiotics studies show some interesting results, indicating that the microbiota acts like an endocrine organ (e.g. secreting serotonin, dopamine or other neurotransmitters) and may control the HPA axis in athletes.”

In the paper

“The bidirectional communication between the ANS and the enteric nervous system (ENS) in the GI tract, the gut-brain axis, mainly occurs by way of the vagus nerve, which runs from the brain stem through the digestive tract and regulates almost every aspect of the passage of digested material through the intestines (reviewed by Eisenstein [8]).”

What the sources say

• Not checked yetcites [8] Eisenstein M, 2016, Nature source

In the paper

“Proper intestinal barrier function is crucial for maintaining immune and overall health [53].”

What the sources say

• Not checked yetcites [53] de Oliveira EP, 2014, Sports Med source

In the paper

“This aberrant stress response in GF mice was partially reversed by colonization with fecal matter from SPF animals and fully reversed by mono association of Bacillus infantis in a time dependent manner [47].”

What the sources say

• Not checked yetcites [47] Sudo N, 2004, J Physiol source

In the paper

“Within the HPA axis, stress activates hypophysiotropic neurons in the paraventricular nucleus of the hypothalamus (PVN) that secrete releasing hormones, such as corticotrophin-releasing hormone (CRH) and arginine vasopressin (AVP), into the portal circulation of the median eminence. These releasing hormones act on the anterior pituitary to promote the secretion of adrenocorticotropic hormone (ACTH”

What the sources say

• Not checked yetcites [6] Ulrich-Lai YM, 2009, Nat Rev Neurosci source

In the paper

“Additionally, Ruminococcus gnavus, which has well defined roles in intestinal mucus degradation, was increased in the forced group compared to sedentary group [52], together with Butyrivibrio spp., Oscillospira spp., and Coprococcus spp.”

What the sources say

• Not checked yetcites [52] Allen JM, 2015, J Appl Physiol (1985) source

In the paper

“An excessive release of stress hormones induced by physical and psychological stress can cause lipopolysaccharides (LPS) translocation outside of the GI tract triggering immune and inflammatory responses often resulting in increased intestinal permeability [56].”

What the sources say

• Not checked yetcites [56] Brown WM, 2015, Sports Med Open source

In the paper

“Moderate exercise can increase GABA levels in the hypothalamus resulting in lower resting blood pressure, heart rate and sympathetic tone [39].”

What the sources say

• Not checked yetcites [39] Hsu YC, 2011, J Hypertens source

In the paper

“This preliminary study in exercised and stressed-animals shows that physical activity can alter microbiota composition as well as metabolic function that could either positively or negatively affect performance.”

What the sources say

• Not checked yetcites [52] Allen JM, 2015, J Appl Physiol (1985) source

In the paper

“Dopamine production is dependent upon several factors: levels of its precursor tyrosine, enteric bacteria that directly produce dopamine, the type of stress experienced and sex [43].”

What the sources say

• Not checked yetcites [43] Eisenhofer G, 1997, J Clin Endocrinol Metab source

In the paper

“This later stressor, like novelty, caused an increase in hippocampal GABA (120% of baseline), suggesting a stimulatory effect of psychological stress [40].”

What the sources say

• Not checked yetcites [40] de Groote L, 2007, Neuroscience source

In the paper

“Microorganisms that colonize the digestive tract can be involved in the regulation of the HPA axis through the regulation or production of short chain fatty acids and neurotransmitters such as GABA, dopamine and serotonin, as well as cytokines.”

In the paper

“NPY is also released in response to various stress stimuli, such as intense exercise, in the GI tract and plays a role in attenuates the HPA axis [41].”

What the sources say

• Not checked yetcites [41] Ramson R, 2012, Eur J Appl Physiol source

In the paper

“Dietary changes can account for up to 57% of gut microbiota changes, whereas genes account for no more than 12% [25].”

What the sources say

• Not checked yetcites [25] Zhang C, 2010, ISME J source

In the paper

“A systematic review on endurance exercise and gut microbiota [23] suggested that gut microbiota might have a key role in controlling the oxidative stress and inflammatory responses as well as improving metabolism and energy expenditure during intense exercise.”

What the sources say

• Not checked yetcites [23] Mach N and Fuster-Botella D: Endurance exercise and gut microbiota: A review. J Sport Health Sci 2016 (In press). source

In the paper

“The human gut harbors more than 100 trillion microorganisms in the GI tract, which represents roughly 9 million genes [12].”

What the sources say

• Not checked yetcites [12] Li J, 2014, Nat Biotechnol source

In the paper

“Voluntary wheel running for 6 weeks attenuated symptoms, whereas forced treadmill running exacerbates intestinal inflammation and clinical outcomes in a colitis mouse model [52].”

What the sources say

• Not checked yetcites [52] Allen JM, 2015, J Appl Physiol (1985) source

In the paper

“The gut microbiota promotes digestion and food absorption for host energy production [14–16] and provide folate [17], vitamin K2 [18] and SCFAs [19].”

What the sources say

• Not checked yetcites [14] Hsu YJ, 2015, J Strength Cond Res source
• Not checked yetcites [15] Mach N, 2015, Environ Microbiol Rep source
• Not checked yetcites [16] Ramayo-Caldas Y, Mach N, Lepage P, et al.: Phylogenetic network analysis applied to pig gut microbiota identifies an ecosystem structure linked with growth traits. ISME 2016 (In press). source
• Not checked yetcites [17] Sugahara H, 2015, Biosci Microbiota Food Health source
• Not checked yetcites [18] Marley MG, 1986, Biochemistry source

In the paper

“Moreover, GF mice treated with Clostridium species, fecal flora from the SPF mice or E. coli showed elevated levels of free catecholamines suggesting that the gut microbiota plays a role in their synthesis through dopamine regulation [48].”

What the sources say

• Not checked yetcites [48] Asano Y, 2012, Am J Physiol Gastrointest Liver Physiol source

In the paper

“Acetate, propionate, and N-butyrate are present at a molar ratio of approximately 60:20:20 in the colon and feces [74].”

What the sources say

• Not checked yetcites [74] den Besten G, 2013, J Lipid Res source

In the paper

“In healthy young adult male cyclists who performed endurance sports activities during 4–10 hours per week, just one hour of physical activity at 70% maximum workload capacity produced splanchnic hypoperfusion, which can cause decreased GI circulation, increased intestinal permeability and damage to the small intestine [64].”

What the sources say

• Not checked yetcites [64] van Wijck K, 2012, Am J Physiol Gastrointest Liver Physiol source

In the paper

“Conversely, the microbiota’s production of butyrate and propionate can increase transepithelial resistance, which improves intestinal barrier function and decreases inflammation.”

In the paper

“Glucocorticoids released during intense exercise has also been shown to diminish the TLR expression, and therefore the capacity to produce anti-inflammatory cytokines and host antimicrobial defense [68].”

What the sources say

• Not checked yetcites [68] Gleeson M, 2007, J Appl Physiol (1985) source

In the paper

“The translocated LPS are detected by CD14 and toll-like receptor 4 (TLR4), which causes the release of pro-inflammatory cytokines such as tumor necrosis factor alpha (TNFα), interferon alpha (IFNα), interferon-gamma (INFγ) and interleukins (IL1β or IL6), which can eventually result in endotoxemia [57] (Fig. 2).”

What the sources say

• Not checked yetcites [57] Zuhl M, 2014, Br J Sports Med source

In the paper

“The central fatigue hypothesis states that increased of the neurotransmitter serotonin (5-hydroxytryptamine; 5-HTP) release is associated with sleep, drowsiness and central fatigue, which contribute to suboptimal physical performance (reviewed by Best et al [82], Fig. 3).”

What the sources say

• Not checked yetcites [82] Best J, 2010, Theor Biol Med Model source

In the paper

“The cecum was approximately 1.5 times larger in the exercise group than in the control group, and the cecal tissue weights and contents were much greater in the exercise group than in the control group, indicating that a significant change had occurred in the cecal environment in response to voluntary wheel running [80].”

What the sources say

• Not checked yetcites [80] Matsumoto M, 2008, Biosci Biotechnol Biochem source

In the paper

“Therefore hypoperfusion and ischemia can result in increased intestinal permeability opening the door for LPS and enteric bacteria to circulate the bloodstream, possibly leading to endotoxemia.”

In the paper

“In general, exercise-induced stress can diminish intestinal barrier function and cause LPS translocation which results in GI upset, hydration imbalances, poor uptake of nutrients and electrolytes, as well as thermal damage of the intestinal mucosa, all of which negatively affect athletic performance [64].”

What the sources say

• Not checked yetcites [64] van Wijck K, 2012, Am J Physiol Gastrointest Liver Physiol source

In the paper

“Additionally, intense exercise over a prolonged period of time increase stress hormones and lipopolysaccharides (LPS) translocation in the gastrointestinal tract, which triggers immune responses that often results in increased pro-inflammatory cytokines and intestinal permeability.”

In the paper

“Depending on the type of exercise, intensity, age and other factors, between 20-50% of athletes suffer gastrointestinal symptoms, which have been shown to increase with exercise intensity [60].”

What the sources say

• Not checked yetcites [60] Lamprecht M, 2012, J Int Soc Sports Nutr source

In the paper

“In the colon and cecum, complex plant-derived polysaccharides are digested and subsequently fermented by gut microorganisms, such as Lactobacillus, Bifidobacterium, Clostridium, Bacteroides, into SCFAs and gases which are also used as carbon and energy sources by specialized bacteria such as reductive acetogens, sulfate-reducing bacteria and methanogens (reviewed by Marchesi et al [36] and by Flin”

What the sources say

• Not checked yetcites [36] Marchesi JR, 2016, Gut source
• Not checked yetcites [19] Flint HJ, 2008, Nat Rev Microbiol source

In the paper

“The redistribution of blood flow away from the intestines together with thermal damage to the intestinal mucosa can cause intestinal barrier disruption, followed by an inflammatory response [63].”

What the sources say

• Not checked yetcites [63] Lambert GP, 2009, J Anim Sci source

In the paper

“Although there are few studies that show the effect exercise has on SCFA levels in the cecum and energy metabolism, those that do exist, illustrate how intense exercise affect SCFA production, which in turn affects the HPA axis, the GI health and may promote favorable athletic performance.”

In the paper

“According to a review conducted by Best et al [82], about 2% of ingested tryptophan is used for the synthesis of serotonin.”

What the sources say

• Not checked yetcites [82] Best J, 2010, Theor Biol Med Model source

In the paper

“During intense exercise, athletes’ body temperature increases and blood pools away from the gastrointestinal tract to periphery muscles and organs such as the heart and lungs during intense physical activity [62].”

What the sources say

• Not checked yetcites [62] Qamar MI, 1987, Gut source

In the paper

“The redistribution of blood flow away from the intestines together with thermal damage to the intestinal mucosa can cause intestinal barrier disruption, followed by an inflammatory response [63].”

What the sources say

• Not checked yetcites [63] Lambert GP, 2009, J Anim Sci source

In the paper

“Brock-Utne et al [66] discovered that 81% of randomly selected exhausted marathon runners showed endotoxemia (0,1 ng/mL), 2% presented lethal levels above 1 ng/mL and only 19% had normal levels.”

What the sources say

• Not checked yetcites [66] Brock-Utne JG, 1988, S Afr Med J

In the paper

“Ischemia also increases reactive oxygen species (ROS) production, which induces leaky gut as activated protein kinases phosphorylate tight junctions proteins resulting in hyperpermeability (Fig. 2) [57].”

What the sources say

• Not checked yetcites [57] Zuhl M, 2014, Br J Sports Med source

In the paper

“Hydrogen peroxide can also serve as a signaling molecule that activates transcription of several pro-inflammatory genes including nuclear factor kappa-light-chain-enhancer of activated B cells (NFKβ), TNFα, IL6, IFNγ, and IL1β [65] that can compromise barrier function.”

What the sources say

• Not checked yetcites [65] Holland AM, 2015, BMC Res Notes source

In the paper

“Furthermore, low serotonin in the brain also causes mood disorders and depression as well as changes in gut transit, blood pressure, cardiac function and platelet aggregation (reviewed by Evans et al [83], Fig. 3).”

What the sources say

• Not checked yetcites [83] Evans JM, 2013, J Endocrinol source

In the paper

“Additionally, the activation of the HPA axis may stimulate subepithelial mast cells to secrete immune mediators such as histamine, proteases and pro-inflammatory cytokines [58], trigging intestinal permeability [59].”

What the sources say

• Not checked yetcites [58] Ferrier L, 2008, Gut source
• Not checked yetcites [59] Wallon C, 2008, Gut source

In the paper

“All these studies show that intense exercise during prolonged periods not only can lead to increased intestinal permeability and thus increased plasma LPS levels, but it can also cause immunosuppression [69].”

What the sources say

• Not checked yetcites [69] Bosenberg AT, 1988, J Appl Physiol (1985) source

In the paper

“In a study of 29 highly trained male triathletes, Jeukendrup et al [61] discovered that upon competition, 93% reported digestive disturbances and two participants had to abandon the race because of severe vomiting and diarrhea.”

What the sources say

• Not checked yetcites [61] Jeukendrup AE, 2000, Clin Sci (Lond) source

In the paper

“Many athletes who suffer from stress enter into a vicious cycle of over exerting themselves with strenuous training and competitions, which results in fatigue causing them to over train in order to overcome fatigue and decreased athletic performance [4].”

What the sources say

• Not checked yetcites [4] Purvis D, 2010, PM R source

In the paper

“Approximately 95% of the body's serotonin is produced in the enterochromaffin cells (EC) of the intestines [8, 83], which plays a role in enteric motor and sensory functions such as visceral pain perception, further illustrating the gut-brain connection [84].”

What the sources say

• Not checked yetcites [8] Eisenstein M, 2016, Nature source
• Not checked yetcites [83] Evans JM, 2013, J Endocrinol source
• Not checked yetcites [84] Stasi C, 2012, J Gastroenterol source

In the paper

“N-butyrate and propionate can increase transepithelial resistance which improves intestinal barrier function and decreases inflammation [78].”

What the sources say

• Not checked yetcites [78] Puddu A, 2014, Mediators Inflamm

In the paper

“For instance, marathon, triathlete and ultra endurance athletes have been reported to have plasma LPS concentrations of 5 to 284 pg/mL along with up to 93% of athletes reporting digestive disturbances, which could be caused by the LPS-induced cytokine response [61].”

What the sources say

• Not checked yetcites [61] Jeukendrup AE, 2000, Clin Sci (Lond) source

In the paper

“Nevertheless, Fernstrom et al [95] state that the central fatigue hypothesis is weak because there lacks evidence that shows what specifically causes an increase in brain tryptophan during exercise [95].”

What the sources say

• Not checked yetcites [95] Fernstrom JD, 2006, J Nutr source

In the paper

“Like 5-HTP, dopamine cannot easily cross the blood–brain barrier [97]; therefore, neurons must synthesize dopamine from its precursor tyrosine that’s ingested from the diet [97].”

What the sources say

• Not checked yetcites [97] Foley TE, 2008, Neuromolecular Med source

In the paper

“The 5-HTP is then rapidly decarboxylated by the aromatic amino acid decarboxylase (AADC) to produce cytosolic serotonin [82].”

What the sources say

• Not checked yetcites [82] Best J, 2010, Theor Biol Med Model source

In the paper

“Of these enzymes, TPH1 is expressed in the periphery and in the pineal body, whereas TPH2 appears to be responsible for the synthesis of serotonin in the rest of the brain.”

What the sources say

• Not checked yetcites [87] McKinney J, 2005, J Neurochem source

In the paper

“The authors concluded that this probiotic may have antidepressant effects and illustrates how gut bacteria can ultimately modulate serotonin levels [107].”

What the sources say

• Not checked yetcites [107] Desbonnet L, 2008, J Psychiatr Res source

In the paper

“Moreover, dopamine is an important neurotransmitter associated with motivation and reward [97].”

What the sources say

• Not checked yetcites [97] Foley TE, 2008, Neuromolecular Med source

In the paper

“IDO is stimulated by oxidative stress and pro-inflammatory cytokines such as IL6 and TFNα, which are released due to LPS-induced intestinal permeability experienced during intense exercise [89].”

What the sources say

• Not checked yetcites [89] Xie W, 2014, J Neuroinflammation source

In the paper

“However, Walther and et al [88] have reported the existence of two distinct TPH genes in humans: TPH1 and TPH2.”

What the sources say

• Not checked yetcites [88] Walther DJ, 2003, Science source

In the paper

“Glutamine, a nonessential amino acid that’s the most abundant in the human body [102], is crucial not only for the glutamate and GABA synthesis but also for optimal functioning of leukocytes such as lymphocytes and macrophages, T cell proliferation and function [104], intestinal enterocytes growth [102].”

What the sources say

• Not checked yetcites [102] Desvergne B, 2006, Physiol Rev source
• Not checked yetcites [104] Mul JD, 2015, Prog Mol Biol Transl Sci source

In the paper

“Therefore, prolonged intense exercise could negatively affect neurotransmitter homeostasis and immune response when glutamine levels are depleted [80, 81] in order to detoxify ammonia in the brain causing a more excitatory-glutamate driven response to exercise-induced stress and a decline in GABA-mediated inhibitory pathways.”

What the sources say

• Not checked yetcites [80] Matsumoto M, 2008, Biosci Biotechnol Biochem source
• Not checked yetcites [81] Gleeson M, 2007, J Appl Physiol source

In the paper

“Although the probiotic had no effect on swim performance, there was a significant reduction of IFNγ, TNFα and IL-6 in the probiotic-treated rats compared to controls, and there was a significant increase in plasma concentrations of tryptophan but also kynurenic acid in the bifidobacteria-supplemented rats.”

What the sources say

• Not checked yetcites [107] Desbonnet L, 2008, J Psychiatr Res source

In the paper

“Under stress, nutrient availability has the potential to affect energy metabolism and protein synthesis as well as endocrine, nervous and immune systems [109].”

What the sources say

• Not checked yetcites [109] Desborough JP, 2000, Br J Anaesth source

In the paper

“On the other hand, moderate aerobic exercise has been shown to increase dopamine levels while reducing serotonin levels in the nigrostriatal tract [44], illustrating that exercise can greatly alter neurotransmitter metabolism.”

What the sources say

• Not checked yetcites [44] Heijnen S, 2015, Front Psychol

In the paper

“Consequently, glucocorticoids and pro-inflammatory cytokines induce TDO and IDO enzymes leading to less serotonin synthesis and possibly fatigue and depression that many athletes who suffer from stress.”

In the paper

“Increases in pro-inflammatory cytokines like IFNγ and IL6 have been associated with reduced exercise tolerance, acute viral or bacterial infection and increased tryptophan catabolism which could thus limit brain serotonin synthesis [100], leading to depressive behavior.”

What the sources say

• Not checked yetcites [100] Dunn AJ, 2006, Clin Neurosci Res source

In the paper

“GF rats on the other hand had lower levels of tryptophan that increase after administering bifidobacteria species [107].”

What the sources say

• Not checked yetcites [107] Desbonnet L, 2008, J Psychiatr Res source

In the paper

“It is suggested that altered dopaminergic pathways involving movement lead to fatigue (reviewed by Foley [97]).”

What the sources say

• Not checked yetcites [97] Foley TE, 2008, Neuromolecular Med source

In the paper

“As explained above, the gut microbiota serves as an endocrine organ in many ways facilitating the production and regulation of various neurotransmitters and hormones (Table 1), which can affect an athlete’s mood, motivation, and sensation of fatigue (Fig. 3).”

In the paper

“The overall metabolic effect of the hormonal changes is increased metabolism, which mobilizes substrates to provide energy sources, and a mechanism to retain salt and water and maintain fluid volume, cardiovascular homeostasis and immune system response [109].”

What the sources say

• Not checked yetcites [109] Desborough JP, 2000, Br J Anaesth source

In the paper

“Once in the CNS, L-tryptophan is converted from tryptophan hydroxylase (TPH) into 5-HTP, the rate limiting step in brain serotonin synthesis [87].”

What the sources say

• Not checked yetcites [87] McKinney J, 2005, J Neurochem source

In the paper

“These findings show that exercise stimulates glutamine synthesis that’s used for ammonia detoxification resulting in decreased production of the excitatory neurotransmitter glutamate possibly causing fatigue in endurance athletes [101].”

What the sources say

• Not checked yetcites [101] Guezennec CY, Abdelmalki A, Serrurier B, et al. Effects of prolonged exercise on brain ammonia and amino acids. Int J Sports Med. 1998;19:323–7. source

In the paper

“They discovered that both trained and untrained rats that ran until exhausted presented an increase in serum ammonia, which can reduce brain energy by stimulating the Krebs cycle and glycolysis.”

What the sources say

• Not checked yetcites [101] Guezennec CY, Abdelmalki A, Serrurier B, et al. Effects of prolonged exercise on brain ammonia and amino acids. Int J Sports Med. 1998;19:323–7. source

In the paper

“The trained exercise group had levels of ammonia 50% higher than the untrained group and also presented lower levels of the excitatory neurotransmitter glutamate as well as a decrease in GABA in the striatum of the brain [101].”

What the sources say

• Not checked yetcites [101] Guezennec CY, Abdelmalki A, Serrurier B, et al. Effects of prolonged exercise on brain ammonia and amino acids. Int J Sports Med. 1998;19:323–7. source

In the paper

“When focusing to the interaction between serotonin and exercise, running at low speed appears to increase cerebral serotonin levels and decrease depressive and anxious behavior, whereas high-speed running causes an increase in the gene expression of CRH [93].”

What the sources say

• Not checked yetcites [93] Otsuka T, 2016, Beh Brain Res source

In the paper

“There is strong evidence that low levels or an absence of gut microbiota (i.e. GF animals) increase tryptophan and serotonin levels and modify central higher order behavior [106].”

What the sources say

• Not checked yetcites [106] Clarke G, 2013, Mol Psychiatry source

In the paper

“Adequate protein intakes enhance host immunity with particularly effects on the T cell system, resulting in decreased incidences of infections.”

What the sources say

• Not checked yetcites [35] Carabotti M, 2015, Ann Gastroenterol

In the paper

“High-fat diet microbiota can increase anxiety-like behaviour and neuro-inflammation and disrupt intestinal barrier function [114].”

What the sources say

• Not checked yetcites [114] Achten J, 2004, J Appl Physiol (1985) source

In the paper

“1.2 to 1.6 g/kg per day in the top elite athletes [41, 42]”

What the sources say

• Not checked yetcites [41] Ramson R, 2012, Eur J Appl Physiol source
• Not checked yetcites [42] Saunders PR, 2002, Dig Dis Sci source

In the paper

“Low dietary fiber consumption is associated with lower microbiota diversity, fewer anti-pathogenic bacteria and less SCFA production [146], which may lead to inflammation [122] and less sympathetic nervous system stimulation [123]”

• Also stated in: § Dietary recommendations to reduce the exercise-induced stress behavior and symptoms and to improve the gut microbiota composition and function for athletes · plain

  “Low dietary fiber consumption is associated with lower microbiota diversity, less SCFA production [112] and fewer anti-pathogenic bacteria [153], all of which may have harmful long-term consequences for the host [112].”

What the sources say

• Not checked yetcites [146] Konig D, 1997, Exerc Immunol Rev
• Not checked yetcites [112] Sonnenburg ED, 2016, Nature source
• Not checked yetcites [153] Hold GL, 2014, Gut source

In the paper

“Low dietary fiber consumption is associated with lower microbiota diversity, fewer anti-pathogenic bacteria and less SCFA production [146], which may lead to inflammation [122] and less sympathetic nervous system stimulation [123]”

What the sources say

• Not checked yetcites [122] Bruunsgaard H, 2000, Immunol Cell Biol source
• Not checked yetcites [123] Pasiakos SM, 2011, Am J Clin Nutr source

In the paper

“Leucine supplementation can greatly increase leucine and total BCAA concentrations and improve endurance performance [49] and muscle protein synthesis.”

What the sources say

• Not checked yetcites [49] Bravo JA, 2011, Proc Natl Acad Sci U S A source

In the paper

“Elite athletes’ dietary plans are also based on the consumption of certain micronutrients such as iron, calcium, amino acids, essential fatty acids and antioxidants [111], but rarely is the health of the gut microbiota ever considered.”

What the sources say

• Not checked yetcites [111] Antonio J, Stout JR, Willoughby D, et al.: Essentials of sports nutrition and supplements. International society of sports nutrition, Human Press 2008

In the paper

“Although no negative effects have been reported, athletes´ diets enriched with polyphenol extracts (blueberry and green tea), they do not mitigate the physiological stress of heavy exertion nor do they improve recovery speed [120].”

• Also stated in: § Dietary recommendations to reduce the exercise-induced stress behavior and symptoms and to improve the gut microbiota composition and function for athletes · plain

  “Although no negative effects have been reported, athletes’ diets enriched with polyphenol extracts (blueberry and green tea) have not mitigated the physiological stress of heavy exertion nor did it improve recovery speed [151].”

What the sources say

• Not checked yetcites [120] Krzwkowski K, 2001, J Appl Physiol source
• Not checked yetcites [151] Nieman DC, 2013, PloS One source

In the paper

“An acute dose of oral glutamine 2 h before intense exercise may ameliorate stress-induced intestinal permeability, lower plasma endotoxins and be anti-inflammatory [65]”

What the sources say

• Not checked yetcites [65] Holland AM, 2015, BMC Res Notes source

In the paper

“Tyrosine ingestion does not influence time to exhaustion or several aspects of cognitive function while exercising in heat conditions [99].”

• Also stated in: § Dietary recommendations to reduce the exercise-induced stress behavior and symptoms and to improve the gut microbiota composition and function for athletes · plain

  “However, tyrosine ingestion does not influence time to exhaustion or several aspects of cognitive function while exercising in heat conditions [128].”

What the sources say

• Not checked yetcites [99] Sutton EE, 2005, Int J Sport Nutr Exerc Metab source
• Not checked yetcites [128] Watson P, 2012, Int J Sport Nutr Exerc Metab source

In the paper

“An initial bacterial community is established at birth, but develops as a person matures [8].”

What the sources say

• Not checked yetcites [8] Eisenstein M, 2016, Nature source

In the paper

“Since diet strongly influences microbiota composition and function, modulation of the gut microbiota via nutritional treatments may improve the stress response in athletes and improve performance.”

In the paper

“BCAA supplementation may be effective at reducing fatigue by increasing ammonia production”

In the paper

“7 to 12 g/kg per day for athletes who train for more than 2 h/day [145] | Restore muscle and liver glycogen stores during intense exercise; Attenuate stress hormone levels and immunosuppression; Reduce fatigue and improve performance and mood [35].”

What the sources say

• Not checked yetcites [145] Pedersen L, 2016, Cell Metab source
• Not checked yetcites [35] Carabotti M, 2015, Ann Gastroenterol

In the paper

“Adequate fiber intake is 14 g total fiber per 1,000 kcal, or 25 g for adult women and 38 g for adult men, based on research demonstrating protection against various diseases [121].”

• Also stated in: § Dietary recommendations to reduce the exercise-induced stress behavior and symptoms and to improve the gut microbiota composition and function for athletes · boosted

  “The Academy of Nutrition and Dietetics has recently established that adequate fiber intake is 14 g total fiber per 1,000 kcal, or 25 g for adult women and 38 g for adult men, based on research demonstrating protection against coronary heart disease among diseases [152].”

What the sources say

• Not checked yetcites [121] Kingsbury KJ, 1998, Br J Sports Med source
• Not checked yetcites [152] Dahl WJ, 2015, J Acad Nutr Diet source

In the paper

“Inadequate protein intake impairs host immunity with particularly detrimental effects on the T cell system, resulting in increased incidences of infections [113].”

What the sources say

• Not checked yetcites [113] Gleeson M, 2000, Immunol Cell Biol source

In the paper

“Leucine supplementation resulted in significant increases in plasma leucine and total branched chain amino acids concentrations and improved endurance performance and upper body power, affecting the plasma tryptophan: BCAA ratio [124].”

What the sources say

• Not checked yetcites [124] Crowe MJ, 2006, Eur J Appl Physiol source