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

View Article: PubMed Central - PubMed

ABSTRACT

Fatigue, mood disturbances, under performance and gastrointestinal distress are common among athletes during training and competition. The psychosocial and physical demands during intense exercise can initiate a stress response activating the sympathetic-adrenomedullary and hypothalamus-pituitary-adrenal (HPA) axes, resulting in the release of stress and catabolic hormones, inflammatory cytokines and microbial molecules. The gut is home to trillions of microorganisms that have fundamental roles in many aspects of human biology, including metabolism, endocrine, neuronal and immune function. 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. Recent evidence in murine models shows that there is a high correlation between physical and emotional stress during exercise and changes in gastrointestinal microbiota composition. 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.

Diet is known to dramatically modulate the composition of the gut microbiota. Due to the considerable complexity of stress responses in elite athletes (from leaky gut to increased catabolism and depression), defining standard diet regimes is difficult. However, 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. 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). As more elite athletes suffer from psychological and gastrointestinal conditions that can be linked to the gut, targeting the microbiota therapeutically may need to be incorporated in athletes’ diets that take into consideration dietary fiber as well as microbial taxa not currently present in athlete’s gut.

No MeSH data available.


Related in: MedlinePlus

Stress hormones released during high intense exercise. Stress responses to intense exercise are mediated by largely overlapping circuits in the limbic forebrain, the hypothalamus and the brainstem, so that the respective contributions on the neuroendocrine and autonomic systems are tuned in accordance with stressor and intensity [6]. When brainstem receives inputs that signal major homeostatic perturbations, such as respiratory distress, energy imbalance, desydration, visceral or somatic pain, inflammation or exteroceptive factors respond through a coordinated modulation of the HPA axis and the sympathetic and parasympathetic branch of the autonomic nervous system (ANS). By contrast, forebrain limbic regions have no direct connections with the HPA axis or the ANS and thus require intervening synapses before they can access autonomic or neuroendocrine neurons (top-down regulation) [6]. 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. Parasympathetic tone can also be modulated during stress (shown in dark grey color). Parasympathetic actions are generally opposite to those of the sympathetic system and alter the vagal tone to the heart and lungs. 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), which in turn acts on the inner adrenal cortex to initiate the synthesis and release of glucocorticoid hormones. Moreover, the adrenal cortex is directly innervated by the sympathetic nervous system, which can also regulate corticosteroid release. Additionally, gastrointestinal tract responds to stress in an endocrine manner by releasing hormones such as Gamma-amino butyric acid (GABA), neuropeptide Y and dopamine that have been purported to be involved in the gastrointestinal disturbances, anxiety, depression, reduced food intake and less stress coping. 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. The neuroendocrine stress response to exercise is determined not only by the emotional stress but the volume of physical exposure, where volume consists of the intensity and/or duration of the exercise session. As exercise intensity is increased, there are approximately proportional increases in circulating concentrations of ACTH and cortisol. There is a critical threshold of exercise intensity that must be reached (~50–60% of maximal oxygen uptake [VO2max]) before circulating levels increase in response to exercise [170, 171]
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Fig1: Stress hormones released during high intense exercise. Stress responses to intense exercise are mediated by largely overlapping circuits in the limbic forebrain, the hypothalamus and the brainstem, so that the respective contributions on the neuroendocrine and autonomic systems are tuned in accordance with stressor and intensity [6]. When brainstem receives inputs that signal major homeostatic perturbations, such as respiratory distress, energy imbalance, desydration, visceral or somatic pain, inflammation or exteroceptive factors respond through a coordinated modulation of the HPA axis and the sympathetic and parasympathetic branch of the autonomic nervous system (ANS). By contrast, forebrain limbic regions have no direct connections with the HPA axis or the ANS and thus require intervening synapses before they can access autonomic or neuroendocrine neurons (top-down regulation) [6]. 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. Parasympathetic tone can also be modulated during stress (shown in dark grey color). Parasympathetic actions are generally opposite to those of the sympathetic system and alter the vagal tone to the heart and lungs. 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), which in turn acts on the inner adrenal cortex to initiate the synthesis and release of glucocorticoid hormones. Moreover, the adrenal cortex is directly innervated by the sympathetic nervous system, which can also regulate corticosteroid release. Additionally, gastrointestinal tract responds to stress in an endocrine manner by releasing hormones such as Gamma-amino butyric acid (GABA), neuropeptide Y and dopamine that have been purported to be involved in the gastrointestinal disturbances, anxiety, depression, reduced food intake and less stress coping. 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. The neuroendocrine stress response to exercise is determined not only by the emotional stress but the volume of physical exposure, where volume consists of the intensity and/or duration of the exercise session. As exercise intensity is increased, there are approximately proportional increases in circulating concentrations of ACTH and cortisol. There is a critical threshold of exercise intensity that must be reached (~50–60% of maximal oxygen uptake [VO2max]) before circulating levels increase in response to exercise [170, 171]

Mentions: Two main distinct but interrelated systems that affect the stress response during exercise are: the sympatho-adrenomedullary (SAM) and hypothalamus-pituitary-adrenal (HPA) axes. 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] (Fig. 1). Stress during exercise also activates the autonomic nervous system (ANS) [7], which provides the most immediate response to stressor stimulus through its sympathetic and parasympathetic arms, and increases the neuronal release of NE and other neurotransmitters in peripheral tissues such as the gastrointestinal (GI) tract or cardiovascular system (extensively reviewed by Ulrich-Lai et al [6]). 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]). 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).Fig. 1


Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes
Stress hormones released during high intense exercise. Stress responses to intense exercise are mediated by largely overlapping circuits in the limbic forebrain, the hypothalamus and the brainstem, so that the respective contributions on the neuroendocrine and autonomic systems are tuned in accordance with stressor and intensity [6]. When brainstem receives inputs that signal major homeostatic perturbations, such as respiratory distress, energy imbalance, desydration, visceral or somatic pain, inflammation or exteroceptive factors respond through a coordinated modulation of the HPA axis and the sympathetic and parasympathetic branch of the autonomic nervous system (ANS). By contrast, forebrain limbic regions have no direct connections with the HPA axis or the ANS and thus require intervening synapses before they can access autonomic or neuroendocrine neurons (top-down regulation) [6]. 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. Parasympathetic tone can also be modulated during stress (shown in dark grey color). Parasympathetic actions are generally opposite to those of the sympathetic system and alter the vagal tone to the heart and lungs. 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), which in turn acts on the inner adrenal cortex to initiate the synthesis and release of glucocorticoid hormones. Moreover, the adrenal cortex is directly innervated by the sympathetic nervous system, which can also regulate corticosteroid release. Additionally, gastrointestinal tract responds to stress in an endocrine manner by releasing hormones such as Gamma-amino butyric acid (GABA), neuropeptide Y and dopamine that have been purported to be involved in the gastrointestinal disturbances, anxiety, depression, reduced food intake and less stress coping. 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. The neuroendocrine stress response to exercise is determined not only by the emotional stress but the volume of physical exposure, where volume consists of the intensity and/or duration of the exercise session. As exercise intensity is increased, there are approximately proportional increases in circulating concentrations of ACTH and cortisol. There is a critical threshold of exercise intensity that must be reached (~50–60% of maximal oxygen uptake [VO2max]) before circulating levels increase in response to exercise [170, 171]
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5121944&req=5

Fig1: Stress hormones released during high intense exercise. Stress responses to intense exercise are mediated by largely overlapping circuits in the limbic forebrain, the hypothalamus and the brainstem, so that the respective contributions on the neuroendocrine and autonomic systems are tuned in accordance with stressor and intensity [6]. When brainstem receives inputs that signal major homeostatic perturbations, such as respiratory distress, energy imbalance, desydration, visceral or somatic pain, inflammation or exteroceptive factors respond through a coordinated modulation of the HPA axis and the sympathetic and parasympathetic branch of the autonomic nervous system (ANS). By contrast, forebrain limbic regions have no direct connections with the HPA axis or the ANS and thus require intervening synapses before they can access autonomic or neuroendocrine neurons (top-down regulation) [6]. 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. Parasympathetic tone can also be modulated during stress (shown in dark grey color). Parasympathetic actions are generally opposite to those of the sympathetic system and alter the vagal tone to the heart and lungs. 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), which in turn acts on the inner adrenal cortex to initiate the synthesis and release of glucocorticoid hormones. Moreover, the adrenal cortex is directly innervated by the sympathetic nervous system, which can also regulate corticosteroid release. Additionally, gastrointestinal tract responds to stress in an endocrine manner by releasing hormones such as Gamma-amino butyric acid (GABA), neuropeptide Y and dopamine that have been purported to be involved in the gastrointestinal disturbances, anxiety, depression, reduced food intake and less stress coping. 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. The neuroendocrine stress response to exercise is determined not only by the emotional stress but the volume of physical exposure, where volume consists of the intensity and/or duration of the exercise session. As exercise intensity is increased, there are approximately proportional increases in circulating concentrations of ACTH and cortisol. There is a critical threshold of exercise intensity that must be reached (~50–60% of maximal oxygen uptake [VO2max]) before circulating levels increase in response to exercise [170, 171]
Mentions: Two main distinct but interrelated systems that affect the stress response during exercise are: the sympatho-adrenomedullary (SAM) and hypothalamus-pituitary-adrenal (HPA) axes. 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] (Fig. 1). Stress during exercise also activates the autonomic nervous system (ANS) [7], which provides the most immediate response to stressor stimulus through its sympathetic and parasympathetic arms, and increases the neuronal release of NE and other neurotransmitters in peripheral tissues such as the gastrointestinal (GI) tract or cardiovascular system (extensively reviewed by Ulrich-Lai et al [6]). 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]). 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).Fig. 1

View Article: PubMed Central - PubMed

ABSTRACT

Fatigue, mood disturbances, under performance and gastrointestinal distress are common among athletes during training and competition. The psychosocial and physical demands during intense exercise can initiate a stress response activating the sympathetic-adrenomedullary and hypothalamus-pituitary-adrenal (HPA) axes, resulting in the release of stress and catabolic hormones, inflammatory cytokines and microbial molecules. The gut is home to trillions of microorganisms that have fundamental roles in many aspects of human biology, including metabolism, endocrine, neuronal and immune function. 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. Recent evidence in murine models shows that there is a high correlation between physical and emotional stress during exercise and changes in gastrointestinal microbiota composition. 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.

Diet is known to dramatically modulate the composition of the gut microbiota. Due to the considerable complexity of stress responses in elite athletes (from leaky gut to increased catabolism and depression), defining standard diet regimes is difficult. However, 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. 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). As more elite athletes suffer from psychological and gastrointestinal conditions that can be linked to the gut, targeting the microbiota therapeutically may need to be incorporated in athletes’ diets that take into consideration dietary fiber as well as microbial taxa not currently present in athlete’s gut.

No MeSH data available.


Related in: MedlinePlus