Abstract
ercise decreases systemic pH and increases metabolic acidosis in athletes, altering the acid-base homeostasis. In addition, nutritional recommendations advising athletes to intake higher amounts of proteins and simple carbohydrates (including from sport functional supplements) could be detrimental to restoring acid-base balance. Here, this specific nutrition could be classified as an acidic diet and defined as ‘Westernized athletic nutrition’. The maintenance of a chronic physiological state of low-grade metabolic acidosis produces detrimental effects on systemic health, physical performance, and inflammation. Therefore, nutrition must be capable of compensating for systemic acidosis from anaerobic exercise. The healthy gut microbiota can contribute to improving health and physical performance in athletes and, specifically, decrease the systemic acidic load through the conversion of lactate from systemic circulation to short-chain fatty acids in the proximal colon. On the contrary, microbial dysbiosis results in negative consequences for host health and physical performance because it results in a greater accumulation of systemic lactate, hydrogen ions, carbon dioxide, bacterial endotoxins, bioamines, and immunogenic compounds that are transported through the epithelia into the blood circulation. In conclusion, the systemic metabolic acidosis resulting from anaerobic exercise can be aggravated through an acidic diet, promoting chronic, low-grade metabolic acidosis in athletes. The individuality of athletic training and nutrition must take into consideration the acid-base homeostasis to modulate microbiota and adaptive physiological responses. Keywords:acid base; pH; metabolic acidosis; anaerobic exercise; animal protein diet 1. Introduction The control of the systemic and cellular acid-base balance is vital
anaerobic exercise can be aggravated through an acidic diet, promoting chronic, low-grade metabolic acidosis in athletes. The individuality of athletic training and nutrition must take into consideration the acid-base homeostasis to modulate microbiota and adaptive physiological responses. Keywords:acid base; pH; metabolic acidosis; anaerobic exercise; animal protein diet 1. Introduction The control of the systemic and cellular acid-base balance is vital to maintain physi- ological homeostasis in humans. The narrow range of blood pH needs to be maintained between 7.35 and 7.45 (mean pH 7.4) [1]. The reduction of blood pH levels below 7.35 pro- motes metabolic acidosis, where in non-clinical conditions, both the central nervous system and immune responses activate different innate buffer mechanisms to restore homeostasis (hemoglobin, bicarbonate, phosphates, and plasma proteins such as albumin). Increased systemic acidosis is a physiological condition resulting from the respiratory system (dif- ficulty in removing carbon dioxide from the lungs) and/or metabolic sources (loss of bicarbonate, elevated acid production, and reduced ability of the kidneys to excrete excess acids) [2]. There are several physiological circumstances that can lead to the dysregulation of acid- base homeostasis. Athletic exercise, especially those involved in anaerobic/intermittent sports, are more likely to exhibit metabolic acidosis. Exercise intensity increases the levels of cell and systemic lactate and hydrogen ions [3], decreasing the systemic pH, sometimes below the homeostatic levels (<7.3) [4]. In basal conditions, another exogenous stimulus that affects acid-base homeostasis in athletes is diet and hydration. Anaerobic athletes typically adhere to acidic diets, which are characterized by substantial intakes of animal proteins and simple carbohydrates (here defined as ‘Westernized athletic nutrition’; WAN). Microorganisms2024,12, 1138.
Microorganisms2024,12, 1138 2 of 25 In this regard, recent studies have even questioned whether animal sources of protein are more beneficial than other vegetable protein sources for muscle mass synthesis and strength [5]. Furthermore, acidic diets increase the risk of gastrointestinal stress and gut microbiota (GM) dysbiosis and elevate the systemic acid load in comparison to other plant-based sources of proteins and complex carbohydrates. [6]. An important fact is that altering differ- ent parts of the gut is related to the change of pH during the digestion and metabolization of animal proteins and simple carbohydrates. The change in the pH promotes adaptive bacterial specialization of the GM [7]. The GM is the community of microorganisms that colonize the gut from birth and mature dynamically in parallel with the host throughout life. The interaction between the host and the GM is of particular interest in athletes because it involves different physiological functions such as digestive, metabolic, endocrine, and immune [8,9]. On the other hand, the persistence of stimulus that negatively impairs GM homeostasis surely impairs the local immunity, establishes inflammation itself, and elevates systemic endotoxemia from an intestinal ‘gut leaky syndrome’ condition to the whole body [10]. In this regard, it has been reported that higher systemic endotoxemia aggravates the inflammatory response in the tissues, elevating systemic acidosis, too [11]. Therefore, promoting a healthy GM would be beneficial for athletes because it improves gut functions, reduces local and systemic inflammation, and contributes to modulating metabolic acidosis in athletes [12,13]. Recently, it has been demonstrated how the gut, and more particularly a certain composition of the gut microbiota (GM), can contribute to regulating metabolic acidosis by recycling lactate into short-chain fatty acids (SCFAs), mainly in the colon [14]. This process takes place through bacterial communities, which in turn modulate the gut pH in a healthy way [15]. Hence, the main objective of this narrative review is to show how great specificity of exercise (anaerobic/intermittent sports) in athletes can promote a chronic state of systemic acidosis when, moreover, it is accompanied by elevated intake of acidic macronutrients such as animal proteins and simple
through bacterial communities, which in turn modulate the gut pH in a healthy way [15]. Hence, the main objective of this narrative review is to show how great specificity of exercise (anaerobic/intermittent sports) in athletes can promote a chronic state of systemic acidosis when, moreover, it is accompanied by elevated intake of acidic macronutrients such as animal proteins and simple carbohydrates. The maintenance of a chronic state of systemic acidosis has negative consequences on health and physical capacities. Fur- thermore, the impairment of the GM composition, promoting bacterial dysbiosis, can reduce physical performance in athletes through multiple functions related to metabolism, immunomodulation, endocrine, and musculoskeletal and/or neural activity. The main objectives of this review were the following: (i) to describe how high-intensity exercise promotes acid-base disturbance, (ii) how specific nutritional recommendations in athletes (high protein, simple carbohydrates, and supplements, here termed as WAN) contribute to aggravating systemic acid load, and (iii) describe the importance of GM balance to co-ordinately modulate acid-base balance through the bacterial potential to buffer acidosis through the gut. 2. Methods This review article was prepared using a narrative approach, contextualizing the topic as to how the metabolic acidosis derived from a physical and nutritional regimen in anaerobic athletes may promote a chronic low grade of acid-base disbalance. Moreover, a dysbiosis of the GM surely appears in athletes following specific acid diets, which are advised. Different databases, including PubMed, Medline, Google Scholar, and Scopus, were used to search for articles for this article, last accessed on 10 April 2024. Common keywords used to search for articles were the following: “effects of diet on metabolic acidosis and exercise”, “metabolic acidosis and systemic inflammation”, “high-intensity exercise, pH and acid base homeostasis”, “anaerobic exercise effects on gut microbiota”, and “high animal protein diet, gut microbiota and metabolic acidosis”. Articles were chosen for inclusion based on the information they described and were incorporated throughout this paper.
Microorganisms2024,12, 1138 3 of 25 3. Effects of Anaerobic Exercise on Acid-Base Homeostasis The anaerobic metabolism implied during high-intensity exercise involves the acti- vation of phosphocreatine and the glycolysis pathways, with a limitation on time [16]. Exercise intensity increases muscle and systemic acidosis, which leads to a decrease in systemic pH through the accumulation of lactate and hydrogen ions [16]. In these sports disciplines, training goals include (i) improving the efficiency of anaerobic pathways to produce energy and (ii) higher recycling and tolerance for lactate and acidosis during and after exercise [16]. Anaerobic metabolism increases the excretion of acids through urine and carbon dioxide during respiration to maintain acid-base homeostasis [17,18]. Therefore, reducing the systemic pH through exercise intensity encompasses lowering acid-base and plasma bicarbonate levels, which, when elevated, can result in a decrease in glomerular filtration by enhancing proximal bicarbonate reabsorption and enhancing levels of angiotensin and mineralocorticoids [1,19]. According to Lindinger and Robergs et al. [17,20], any form of physical activity, even submaximal, leads to an increase in acid production and stress on the body’s buffer systems. In events of high anaerobic intensity, such as a 400 m sprint at maximum intensity, blood pH levels are reduced to levels of 6.8–6.9 [18,21]. Elevation of cellular and systemic acidosis leads to a more perceived fatigue [22] and reduced rate of muscle contraction and anabolism of muscle proteins [23]. In summary, anaerobic sports cause a chronic stimulus over the acid-base homeostasis, which can impair adaptive physiological responses in different ways if maintained. The musculoskeletal adaptation can be impaired by [24] (1) negative protein degradation, increasing muscle breakdown [25–28], (2) impaired mitochondrial function and reduction of energy production, and (3) lower muscle contraction (force) [29]. Moreover, systemic acidosis also impairs tissue oxygenation due to the Bohr effect [30], bone demineralization, increased fracture risk [26], and joint structures degenerate faster [31] (see Figure).Microorganisms 2024, 12, x FOR PEER REVIEW 3 of 25 intensity increases muscle and systemic acidosis, which leads to a decrease in systemic pH through the accumulation of lactate and hydrogen ions [16]. In these sports disciplines, training goals include
oxygenation due to the Bohr effect [30], bone demineralization, increased fracture risk [26], and joint structures degenerate faster [31] (see Figure).Microorganisms 2024, 12, x FOR PEER REVIEW 3 of 25 intensity increases muscle and systemic acidosis, which leads to a decrease in systemic pH through the accumulation of lactate and hydrogen ions [16]. In these sports disciplines, training goals include (i) improving the efficiency of anaerobic pathways to produce energy and (ii) higher recycling and tolerance for lactate and acidosis during and after exercise [16]. Anaerobic metabolism increases the excretion of acids through urine and carbon diox- ide during respiration to maintain acid-base homeostasis [17,18]. Therefore, reducing the systemic pH through exercise intensity encompasses lowering acid-base and plasma bicar- bonate levels, which, when elevated, can result in a decrease in glomerular filtration by en- hancing proximal bicarbonate reabsorption and enhancing levels of angiotensin and miner- alocorticoids [1,19]. According to Lindinger and Robergs et al. [17,20], any form of physical activity, even submaximal, leads to an increase in acid production and stress on the body’s buffer systems. In events of high anaerobic intensity, such as a 400 m sprint at maximum intensity, blood pH levels are reduced to levels of 6.8–6.9 [18,21]. Elevation of cellular and systemic acidosis leads to a more perceived fatigue [22] and reduced rate of muscle contrac- tion and anabolism of muscle proteins [23]. In summary, anaerobic sports cause a chronic stimulus over the acid-base homeostasis, which can impair adaptive physiological responses in different ways if maintained. The musculoskeletal adaptation can be impaired by [24] (1) negative protein degradation, in- creasing muscle breakdown [25–28], (2) impaired mitochondrial function and reduction of energy production, and (3) lower muscle contraction (force) [29]. Moreover, systemic acido- sis also impairs tissue oxygenation due to the Bohr effect [30], bone demineralization, in- creased fracture risk [26], and joint structures degenerate faster [31] (see Figure 1). Figure 1. Systemic health describes the efficacy of homeostasis control and interconnection between dif- ferent physiological thresholds. The body’s homeostatic control modulates coordinatively responses of immune and neural systems (CNS). Acid-base (pH range 7.35–7.45) control depends on
oxygenation due to the Bohr effect [30], bone demineralization, in- creased fracture risk [26], and joint structures degenerate faster [31] (see Figure 1). Figure 1. Systemic health describes the efficacy of homeostasis control and interconnection between dif- ferent physiological thresholds. The body’s homeostatic control modulates coordinatively responses of immune and neural systems (CNS). Acid-base (pH range 7.35–7.45) control depends on systemic/cell buffers. Anaerobic exercise and digestion of some macronutrients (animal proteins and simple carbs) de- crease systemic pH activating buffers in a dependent manner. The sum of exercise and diet may induce a double inertial metabolic acidosis that can chronically impair the buffer reserve. 4. Effects of Nutrition on Metabolic Acidosis in High-Intensity Sports The actual model of sports nutrition advocates regular intakes of simple carbohydrates, nutritional supplements, and proteins before and after exercise (here defined as ‘Westernized athletic nutrition’) to restore burning energy and structural protein synthesis [32]. Here, we Figure 1.Systemic health describes the efficacy of homeostasis control and interconnection between different physiological thresholds. The body’s homeostatic control modulates coordinatively re- sponses of immune and neural systems (CNS). Acid-base (pH range 7.35–7.45) control depends on systemic/cell buffers. Anaerobic exercise and digestion of some macronutrients (animal proteins and simple carbs) decrease systemic pH activating buffers in a dependent manner. The sum of exercise and diet may induce a double inertial metabolic acidosis that can chronically impair the buffer reserve.
Microorganisms2024,12, 1138 4 of 25 4. Effects of Nutrition on Metabolic Acidosis in High-Intensity Sports The actual model of sports nutrition advocates regular intakes of simple carbohydrates, nutritional supplements, and proteins before and after exercise (here defined as ‘Western- ized athletic nutrition’) to restore burning energy and structural protein synthesis [32]. Here, we would like to present an alternative viewpoint based on the premise that systemic health is before acute performance to stimulate the innate biological potential (see Figures and). Nowadays, human metabolism and energy homeostasis are studied from a mecha- nistic perspective—that is, “fuel is burned, energy needs to be restored”—this established concept is widely accepted [32] because it does not characterize human adaptive responses as a living structure where epigenetic modifications exist in a narrow range. In fact, during the last decade, the consumption of nutritional supplements such as fast-absorption carbo- hydrates or whey proteins has grown exponentially with a reductionist character [32]. The healthiness regarding the chronic consume of these products in athletes requires proof, and longitudinal investigations to support their global commercialization.Microorganisms 2024, 12, x FOR PEER REVIEW 4 of 25 would like to present an alternative viewpoint based on the premise that systemic health is before acute performance to stimulate the innate biological potential (see Figures 1 and 2). Nowadays, human metabolism and energy homeostasis are studied from a mechanistic per- spective—that is, “fuel is burned, energy needs to be restored”—this established concept is widely accepted [32] because it does not characterize human adaptive responses as a living structure where epigenetic modifications exist in a narrow range. In fact, during the last dec- ade, the consumption of nutritional supplements such as fast-absorption carbohydrates or whey proteins has grown exponentially with a reductionist character [32]. The healthiness regarding the chronic consume of these products in athletes requires proof, and longitu- dinal investigations to support their global commercialization. Figure 2. Comparison of biological effects of diet on metabolic acidosis from an acute or chronic stim- ulation of metabolism. The primary feature of diet-induced metabolic acidosis is the shift over decades or even centuries from an ancestral alkaline
healthiness regarding the chronic consume of these products in athletes requires proof, and longitu- dinal investigations to support their global commercialization. Figure 2. Comparison of biological effects of diet on metabolic acidosis from an acute or chronic stim- ulation of metabolism. The primary feature of diet-induced metabolic acidosis is the shift over decades or even centuries from an ancestral alkaline diet, high in fruits and vegetables, to a ‘Westernized’ diet composed of foods derived from animals (proteins) and deemed ‘acidogenic’ [28,33–39]. This kind of consumption decreases the consumption of other foods high in bicarbonate and po- tassium [35], as well as the deficiency of other minerals that form bases, like calcium and mag- nesium [37], which are generally present in fruits and vegetables [28,33–39]. This feature has contributed to an increase in diet-induced systemic acidosis, along with a higher consumption of simple sugars [40]. A higher need for pH-buffering homeostatic mechanisms is encouraged by the chronicity of acidic diets in comparison to basic foods [41]. Dietary inflammatory pro- cesses are activated in a state of systemic acidosis [42], where a higher intake of animal proteins and simple sugars raises levels of pro-inflammatory markers such as C-reactive protein (CRP), IL-6, and fibrinogen [42–44] in comparison with diets of vegetables, fruits, and healthy fats from olive oil or oily fish [42,45]. In relation to simple carbohydrates, many scientists recommend eating more simple carbs before, during, and after exercise; however, these practices can inhibit predictive adap- tive responses related to innate metabolic processes (see Figure 2). In this regard, constantly replenishing energy fuel may reduce the innate biological potential because it minimizes better metabolic efficiency and systemic buffer capacity (see Figure 2). Previous studies put in doubt the real efficacy of ‘Westernized Athletic Nutrition’. Maughan and Williams [46] Figure 2.Comparison of biological effects of diet on metabolic acidosis from an acute or chronic stimulation of metabolism. The primary feature of diet-induced metabolic acidosis is the shift over decades or even centuries from an ancestral alkaline diet, high in fruits and vegetables, to a ‘Westernized’ diet composed of foods derived from animals (proteins) and
Nutrition’. Maughan and Williams [46] Figure 2.Comparison of biological effects of diet on metabolic acidosis from an acute or chronic stimulation of metabolism. The primary feature of diet-induced metabolic acidosis is the shift over decades or even centuries from an ancestral alkaline diet, high in fruits and vegetables, to a ‘Westernized’ diet composed of foods derived from animals (proteins) and deemed ‘acidogenic’ [28,33–39]. This kind of consumption decreases the consumption of other foods high in bicarbonate and potassium [35], as well as the deficiency of other minerals that form bases, like calcium and magnesium [37], which are generally present in fruits and vegetables [28,33–39]. This feature has contributed to an increase in diet-induced systemic acidosis, along with a higher consumption of simple sugars [40]. A higher need for pH-buffering homeostatic mechanisms is encouraged by the chronicity of acidic diets in comparison to basic foods [41]. Dietary inflammatory processes are activated in a state of systemic acidosis [42], where a higher intake of animal proteins and simple sugars raises levels of pro-inflammatory markers such as C-reactive protein (CRP), IL-6, and fibrinogen [42–44] in comparison with diets of vegetables, fruits, and healthy fats from olive oil or oily fish [42,45]. In relation to simple carbohydrates, many scientists recommend eating more simple carbs before, during, and after exercise; however, these practices can inhibit predictive adaptive responses related to innate metabolic processes (see Figure). In this regard,
Microorganisms2024,12, 1138 5 of 25 constantly replenishing energy fuel may reduce the innate biological potential because it minimizes better metabolic efficiency and systemic buffer capacity (see Figure). Previous studies put in doubt the real efficacy of ‘Westernized Athletic Nutrition’. Maughan and Williams [46] found that muscle glycogen levels did not change after fasting for 24 h to 82 h when exercising at a low level. To Piehl [47], at 90% of the maximum oxygen uptake intensity, the pattern of glycogen depletion of muscle fiber types during cycle ergometer exercise was not affected by the initial glycogen content of the muscle. Jansson and Kaijser [48] found that eating more fat and less carbs 5 days before exercising at 65% of maximum oxygen uptake did not significantly reduce muscle glycogen, increase the amount of fat used in oxidative metabolism, or decrease CHO use during exercise. Despite the fact that actual nutritional recommendations advocate for eating more carbs regularly to improve physical performance, other studies have shown an innate predictive response, as cited above, is really more effective if stimulated in the long term [49–52]. Related to fast carbohydrate products, we had reported that elevated consumption of sports functional products might impair GM and host health physiology in the long term [12,53]. Recently, Moreno-Pérez et al. [54] have reported that 10 weeks of protein supplementation promoted changes in the GM with reductions of beneficial bacteria such asRoseburia,Blautia, and Bifidobacterium longum.Consequently, specialized sports nutrition guidelines for anaerobic activities might not be the healthiest way to counteract the metabolic acidosis brought on by exercise. Animal protein is the biggest source of dietary acid because its metabolism leads to the formation of sulfuric acid and hydrogen ions in the body. The results of supplementing the colon microbiota with more protein showed a significant decrease in the proportions of beneficial bacteria likeBifidobacteriaspp.,Roseburia, orEurobacterium rectaleand a significant increase in pro-inflammatory bacteria likeClostridium perfrigens,Enterococcus,Shigella, and Eschericia colispp. that produce remarkable levels of ammonia [55]. Therefore, an elevated intake of animal proteins can promote the proteolytic bacteria growth in the colon favoring a context of gut dysbiosis. This gut environment
microbiota with more protein showed a significant decrease in the proportions of beneficial bacteria likeBifidobacteriaspp.,Roseburia, orEurobacterium rectaleand a significant increase in pro-inflammatory bacteria likeClostridium perfrigens,Enterococcus,Shigella, and Eschericia colispp. that produce remarkable levels of ammonia [55]. Therefore, an elevated intake of animal proteins can promote the proteolytic bacteria growth in the colon favoring a context of gut dysbiosis. This gut environment changes the pH of the colon and reduces the formation of SCFAs and lactate [56]. The amount of protein fermentation that occurs in the colon depends on the amount of dietary protein ingested but also on the proportion of protein obtained through non-fermentative pathways. These endogenous sources can come from pathological processes such as those associated with inflammatory and/or ulcerative conditions of the intestine [55]. The increase in metabolic acidosis due to the increase in the intake of animal protein also affects the muscles and connective tissues for the formation of ammonia [57,58]. Therefore, producing large amounts of ammonia to excrete large amounts of acid can have long-term health consequences [58]. The fermentation of protein substrates results in the production of toxic metabolites in the colon, which have the potential to cause harm to the gastrointestinal tract [55]. Although theoretically, the regulation of muscle mass is mediated by a net balance between breakdown and synthesis, the bioavailability of essential amino acids and proteins is also influenced by the actions of GM [6]. Therefore, the stimulus required to promote muscle protein synthesis requires primarily muscle activation with exercise but also nutrient bioavailability [59]. According to Lynch et al. (2018), a higher intake of animal protein as opposed to vegetable protein does not guarantee its beneficial effects on intestinal and systemic health. Furthermore, at the sporting level, physical performance and even strength do not seem to be altered in the long term [5,6]. It is necessary to achieve an equilibrium between the quantitative nutrient load and the GM capacity to digest, metabolize, and absorb. From a digestive perspective, protein fermentation in the colon can produce harmful putrefactive metabolites such as branched-chain fatty acids (BCFAs), ammonia, amines, hydrogen sulfides, phenols, and indoles [60–62].
Description
This review discusses the impact of anaerobic exercise and diet on gut health and metabolic acidosis.