Abstract
Purpose of Review
Modulation of the host microbiota through probiotics has been shown to have beneficial effects on health in the growing body of research. Exercise increases the amount and diversity of beneficial microorganisms in the host microbiome. Although low- and moderate-intensity exercise has been shown to reduce physiological stress and improve immune function, high-intensity prolonged exercise can suppress immune function and reduce microbial diversity due to intestinal hypoperfusion. The effect of probiotic supplementation on sports performance is still being studied; however, questions remain regarding the mechanisms of action, strain used, and dose. In this review, the aim was to investigate the effects of probiotic supplements on exercise performance through modulation of gut microbiota and alleviation of GI symptoms, promotion of the immune system, bioavailability of nutrients, and aerobic metabolism.
Recent Findings
Probiotic supplementation may improve sports performance by reducing the adverse effects of prolonged high-intensity exercise.
Summary
Although probiotics have been reported to have positive effects on sports performance, information about the microbiome and nutrition of athletes has not been considered in most current studies. This may have limited the evaluation of the effects of probiotic supplementation on sports performance.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Probiotic is derived from the Greek word “pro bios” meaning “vitality,” as opposed to “antibiotic” meaning “anti-vitality.” Although the presence of acid-producing bacteria in fermented dairy products was mentioned by Metchnikoff in 1907, the concept of “probiotic” was first used by Lilly and Stillwell in 1965. Later, this concept was defined by Fuller in 1989 as “microbial reinforcement that increases the stability of the host’s gut” [1]. Because of the rapid increase in research on this subject, the need for a common “probiotic” definition has emerged. The World Health Organization (WHO) and United Nations Food and Agriculture Organization (FAO) have defined probiotics as “live microorganisms that provide health benefits to the host when administered in adequate amounts” [2]. A sufficient amount to be administered should be more than 106 colony-forming units (CFU)/mL of live microorganism population for the aforementioned health benefits [3]. In addition, live microorganism species must be safe, have a high tolerance to low pH conditions and bile acids, promote intestinal colonization, and not be vectors of antibiotic resistance genes [4, 5].
The potential health benefits of probiotics may differ according to the microorganism strains [3]. Probiotics may generally produce health effects through the synthesis of beneficial molecules such as short-chain fatty acids (SCFAs), bacteriocins, vitamin K, and vitamin B complex; secretion of protein/peptide structures such as antimicrobial peptides and secretory IgA from the intestines; reduction of pathogenic toxins; protection of epithelial barrier integrity; and immune system regulation [6, 7]. Research on the health effects of probiotics is constantly increasing, and probiotics are thought to exert health effects primarily by modulating host microbiota [8].
In athletes, the number of beneficial microorganisms and microbial diversity has been shown to be greater than in their sedentary counterparts. However, prolonged high-intensity exercise is associated with reduced microbial diversity due to intestinal hypoperfusion [10]. Probiotic supplementation may be an effective strategy to offset the negative effects of prolonged high-intensity exercise [11, 12]. Specifically, probiotics have been associated with reduced gastrointestinal symptoms and infection susceptibility, and may improve performance by improving muscle energy production capabilities, muscle mass and strength, and aerobic capabilities [11, 13, 14]. However, the omission of information regarding the microbiomes of athletes and their diets at the beginning of existing studies hinders the interpretation of the outcomes obtained. Furthermore, probiotic supplementation has also been reported to have no effect on sports performance [15, 16]. Exercise intensity, type of probiotic, dose used, and duration of treatment may have contributed to the heterogeneous results. The aim of our study was to examine the direct and indirect effects of various probiotic interventions on sports performance in line with current literature.
Definitions and Types of the Probiotics
The use of probiotics in human history dates back to 7000 BC to ferment milk and fruits for long-term preservation. In ancient Greece, fermented foods were used in medical treatment for antiseptic, diuretic, and sedative purposes. Turks tried to prevent and treat gastrointestinal (GI) symptoms by consuming yogurt during the Karakhanid period [17]. Lactobacillus spp. were first discovered by Pasteur in 1856, after the early modern period. Although beneficial bacterial species were defined by Metchnikoff, the concept of probiotics was first defined by Lilley and Stillwell in 1965 as “microbes that stimulate the growth of other microorganisms.” In 1989, Fuller defined probiotics as “microbial supplements that increase the stability of the host’s gut.” In 2001, WHO and FAO updated the definition of probiotics based on the latest evidence as “live microorganisms that provide health benefits to the host when applied in adequate amounts” [18].
Many microorganism species have been defined to date, and the range of microorganisms claimed to have probiotic properties is gradually expanding owing to improved culture methods and sequencing techniques. However, according to the definition of probiotics by the International Scientific Association for Probiotics and Prebiotics (ISAPP), when taken by the host, probiotics must be alive, create health benefits, and be administered in effective doses [19]. In a significant number of studies, the microorganism survival and colonization in the host GI tract have been considered to determine probiotic efficacy [3, 5]. However, ISAPP states that probiotics do not require conditions such as survival, colonization, anti-pathogenic properties, or balancing of the host microbiota [19]. The decision tree shown in Fig. 1 is used to name the newly discovered microorganism strain as a probiotic. According to this tree, (i) probiotic strains should be named in accordance with the International Nomenclature Code, (ii) the health effects of probiotics should be supported by at least one clinical study, and (iii) microorganisms should remain alive at the effective dose until the expiration date of the probiotic product and be safe [20]. Many strains of Lactobacillus spp., Bifidobacterium spp., and some yeasts have a history of safe use, which does not pose a significant safety concern in the diet. However, the European Food Safety Authority (EFSA) has recommended the evaluation of the Qualified Presumption of Safety (QPS) list published for healthy populations and safety reports of in vivo studies on the consumption of food and dietary supplements containing probiotics [20, 21].
Decision tree used to determine a candidate probiotic
Probiotics can be consumed as food or as dietary supplements. However, the terms probiotic food and fermented food are often confused by consumers. The health benefits of fermented foods such as pickles, yogurt, cheese, and vinegar are supported in some epidemiological studies [22]. For example, EFSA has validated the health claim that yogurt can improve lactose tolerance in lactose intolerant individuals (EFSA, 2010). In a cohort study, consumption of fermented soy products was linked to a reduction in cardiovascular disease risk [23]. Despite their health benefits, not all fermented foods meet probiotic definition criteria. While the types of microorganisms in fermented foods may differ according to the producer or production region, the type of microorganisms in probiotic foods should be defined. Some probiotic foods can be produced by adding probiotics to the production process of fermented food [19]. Although Lactobacillus, Bifidobacterium, and Saccharomyces cultures are frequently used in this process, research on the determination of candidate probiotic species, called new-generation probiotics, has been increasing in recent years. New-generation probiotics may be important for the development of live biotherapeutic products for prophylactic and therapeutic purposes.
In Vitro and Animal Studies on Benefaction of Probiotics for Sports Performance
Probiotics can exert bioactivity by inhibiting pathogens by secreting antimicrobial substances such as bacteriocins and increasing intestinal acidity through SCFA synthesis [24, 25]. Probiotics can also contribute to the development of the epithelial barrier by increasing the expression of tight junctions such as claudin-1 and occludin, increasing the secretion of antimicrobial compounds such as defensin, and stimulating the activation of lymphocytes in gut-associated lymphoid tissue [26, 27]. Thus, researchers have aimed to reshape the gut microbiome with probiotic supplementation. However, clinical evidence regarding the effects of probiotics on the intestinal microbial balance is limited. Claims regarding the sports performance of probiotics have mostly been derived from in vitro and animal studies.
Probiotics may affect sports performance through several local or systemic effects, such as regulating the immune response, increasing resistance to infections, reducing depressive symptoms, and maintaining skeletal muscle health [28,29,30]. According to Vargoorani et al. Lactobacillus casei extracellular vesicle can reduce inflammation in Caco-2 cells by decreasing Toll-like receptor (TLR)-9 expression and Interferon (IFN)-γ levels, and increasing Interleukin (IL)-4 and IL10 levels [31]. Similarly, Weissella cibaria JW15 strain inhibited inflammation by reducing IL1ß, IL6, and Tumor necrosis factor (TNF)-α levels in Lipopolysaccharide (LPS)-induced RAW 264.7 cells [32]. Evidence regarding the ability of probiotics to inhibit the inflammatory response has been reported by several meta-analyses [33, 34•]. Additionally, probiotics may reduce susceptibility to certain infections, such as upper respiratory tract infections (URTIs). For example, the Lactobacillus plantarum strain inhibited Streptococcus pyogenes, which frequently infects the respiratory tract, in human lung alveolar epithelial cell culture [35]. Furthermore, L. casei 431 and L. fermentum PCC can beneficially regulate penicillin-induced imbalance in the URT microbial compositional structure of experimental mice and thus modulate the immune response [36].
The influence of gut microbiota via the gut-brain axis on the psychological state and brain function of the host has become a popular topic in recent years. In animal models, intestinal dysbiosis has been associated with an abnormal stress response and neuroinflammation in the host [37, 38]. In particular, Lactobacillus spp. have been shown to prevent dysbiosis by regulating intestinal serotonin metabolism, which leads to a reduction of abnormal behavior in experimental animals [39, 40]. More recently, the health implications of the gut microbiome have been extended beyond the gut-brain axis. Gut health has been linked to muscle health, which is termed the gut-muscle axis. In patients with inflammatory bowel disease, decreased levels of Firmicutes and Bacteroides, and increased levels of Enterobacteriaceae were observed. This shift in microbial community may be associated with decreased muscle function and cachexia [41]. Probiotic supplementation can limit decreased muscle function and cachexia in rodents [42, 43]. In rodent models, probiotics have been reported to exert their effects on muscle mass and function through protein bioavailability, preservation of muscle strength and endurance, reduction of fatigue markers, and an increase in muscle glycogen stores [44, 45].
Mechanisms of Action of Probiotics on Sports Performance
Athletes are at risk for various diseases because of training, travel, insufficient rest, and malnutrition [46]. For example, GI symptoms and endotoxemia are frequently reported, especially in long-distance athletes such as marathons and triathlons [47, 48]. Although low- and moderate-intensity exercise reduce physiological stress and improve immune function, high-intensity prolonged exercise suppresses immune function from a few hours to several days [49, 50]. This is called the “open window period,” in which susceptibility to infections, such as URTIs, increases in athletes. Probiotics may be effective in infection control [13, 51]. Probiotics can also increase the amount of glycogen in the liver and skeletal muscles, and increase the absorption of amino acids, which are important for protein synthesis, such as branched-chain amino acids (BCAAs) and glutamine [52,53,54]. Moreover, the gut microbiota can improve muscle strength and function through the intestinal axis action [55,56,57]. Therefore, the effectiveness of probiotics in improving physical performance has become a focus of research in recent years.
Gastrointestinal System and Modulation of Intestinal Microbiota
Modulation of the intestinal microbiota and various metabolites, such as short-chain fatty acids, can reduce intestinal epithelial barrier permeability and production of inflammatory cytokines. Thus, it reduces GI disturbances, delays fatigue symptoms, increases skeletal muscle mass and function, and enhances athletic performance [58,59,60,61]. Furthermore, short-chain fatty acids, such as butyrate, increase the proportion of oxidative fibers by stimulating peroxisome proliferator-activated receptor-1/ (PGC-1) [62]. This increase may positively affect skeletal muscle endurance and exercise performance [63].
Probiotics may help restore impaired intestinal microbiota and support microbiota under stress conditions [64, 65]. The frequency and severity of GI symptoms were reduced by probiotic supplementation and microbiota modulation in athletes [66••, 67]. These symptoms are caused, in part, by decreased oxygen and nutrient supply to enterocytes due to intestinal hypoperfusion, decreased mucus layer thickness, increased intestinal permeability, and bacterial translocation into the bloodstream [68]. Increased levels of inflammatory cytokines and bacterial endotoxins were observed as a result of intestinal permeability. Runners with high endotoxin levels after a race are four times more likely to experience GI symptoms than those with low endotoxin levels [69]. GI symptoms can significantly reduce the athletic capacity and performance. Therefore, new strategies that specifically focus on reducing these symptoms should be developed. Dietary strategies have the potential to increase the physical comfort of athletes and reduce the risk of GI disturbances [14]. Probiotic supplementation, an important dietary strategy, can help improve the intestinal barrier, prevent endotoxemia, and alleviate the inflammatory response [70]. Probiotics are effective and safe in preventing and treating GI disturbances caused by intense exercise, thereby improving physical performance [46, 71].
Immune System Modulation
In addition to modulating the intestinal microbiota, probiotics may regulate the mucosal immune response, enhance macrophage activity, and modulate the expression of genes associated with macrophage activity [72]. Furthermore, probiotics have been shown to reduce the expression of nuclear factor kappa β (NF-κβ) and proinflammatory cytokines by interacting with TLRs [73, 74]. Moreover, anti-inflammatory cytokines, immunoglobulin levels, immune cell proliferation, and production of proinflammatory cytokines by T cells can also be modulated by probiotic supplementation [75, 76]. Probiotics can affect sports performance by modulating the immune system and by improving fatigue indicators and muscle soreness. Moreover, it may indirectly contribute to sports performance by preventing immunosuppressive effects and URTIs caused by intense exercise.
In contrast to recreational and moderate exercise, intense exercise increases the synthesis of proinflammatory cytokines, such as IL-1, IL-6, and TNF-α [77,78,79,80]. Changes in salivary IgA levels after exercise may be associated with a higher risk of infection among athletes. However, the literature on salivary IgA is conflicting [81, 82]. Some authors have stated that saliva quality should be evaluated by measuring the total protein concentration as well as the salivary IgA concentration [82]. Moreover, after intense and prolonged exercise, a decrease in the frequency and function of acquired immune cells, such as lymphocytes, has been detected in peripheral blood [83, 84]. This may cause an increase in infection susceptibility and, therefore, a decrease in sports performance. Probiotic supplementation may have an important role in improving factors that may adversely affect sports performance, such as fatigue, pain, mood changes, and concentration disorders after exercise through cytokine modulation. It may also contribute to sports performance indirectly by improving lung performance during and after URTIs or by preventing immunosuppressive effects [78•].
Bioavailability of Nutrients
Several factors can lead to GI disturbances during endurance exercise, including splanchnic oxidative stress, hypoxia, mechanical stress, exercise-induced hyperthermia, and carbohydrate malabsorption [85, 86]. Reduction in carbohydrate absorption is considered a limiting factor for performance in endurance exercises lasting longer than 60 min. According to some researchers, the ability of probiotics to maintain intestinal integrity may affect sports performance by improving the absorption of carbohydrates and amino acids during prolonged exercise [66••, 87]. It is one of the main claims that probiotic supplementation provides an increase in proteolytic activity by optimizing intestinal microbiota composition [88]. Second, probiotic supplementation increases the absorption of amino acids in vegetable proteins, which are considered low-quality protein sources, and BCAAs, which are important for protein cycling [12, 89]. Thus, the use of probiotics may increase protein bioavailability. However, research on the potential of probiotics in improving nutrient metabolism in relation to exercise remains limited.
Another topic of interest in the relationship between probiotics and nutrient absorption is inorganic iron supplementation. Iron is important for oxygen transport, mitochondrial energy production, and cellular immune response. Physical performance and adaptation to training may be negatively affected by iron deficiency [90]. Increased iron absorption may be a strategy for improving the iron status and avoiding adverse effects from the use of traditional high-dose iron supplements. According to meta-analysis findings, iron absorption was increased in humans supplemented with L. plantarum 299v alone [91]. Although the impact of probiotics apart from L. plantarum 299v on iron absorption remains unclear, it is still a topic of investigation. Furthermore, the consequences of probiotic supplementation on biochemical markers of iron status, rather than iron absorption, should also be reported in comprehensive studies.
Aerobic Capacity
Changes in intestinal microbial flora have been suggested to affect hematopoiesis and erythropoiesis by affecting the levels of circular SCFA [93, 94]. Hematopoiesis is suppressed in conditions that cause intestinal microbiome imbalance such as obesity, malnutrition, and antibiotic use [93]. Therefore, the relationship between dysbiosis and hematological problems, such as anemia and neutropenia, has been emphasized in recent studies [95, 96]. Because of the possible improvements in microbial flora and the synthesis of some metabolites in the gut, such as SCFAs, the possibility that probiotic supplementation can increase aerobic performance and endurance by accelerating erythropoiesis has emerged. Aerobic capacity is measured directly using maximal physical workrate tests or indirectly using some equations and is expressed as maximal oxygen uptake (VO2max) [97]. Although probiotics have been reported to improve endurance by increasing VO2max in a few studies, some researchers have not confirmed this effect in athletes [98••, 99]. Furthermore, the correlation between VO2max and sports performance is weak in highly trained athletes, owing to compensatory factors [97].
Clinical Evidence on the Effect of Probiotic Supplementation on Sports Performance
As shown in Table 1, the potential effects of probiotic supplementation on sports performance have been reported in several randomized controlled trials (RCTs). Single- or multi-strain supplements at the level 108–1011 CFU/day were used in these studies. In recent studies, sports performance has generally been associated with indicators of fatigue, physical performance, aerobic capacity, carbohydrate and protein bioavailability, inflammatory responses, URTIs, GI symptoms, and psychological status. Researchers have tried to determine the effect of probiotic supplementation on sports performance, mostly directly by measuring physical performance or indirectly by evaluating the inflammatory response and GI symptoms. There is some evidence to suggest that probiotic supplementation modulates the inflammatory responses and reduces the severity of GI symptoms. However, further studies with larger groups are needed to clarify whether probiotic supplementation enhances physical performance.
Intense exercise can induce GI damage, causing GI symptoms, such as abdominal pain, diarrhea, and blood in the stool [98••]. Therefore, intense exercise-induced GI damage has been reported to reduce macronutrient absorption [85, 86]. Multi-strain probiotic supplementation has reduced GI symptoms in intensely trained athletes such as long-distance runners and road cyclists [99, 100]. Additionally, probiotic supplementation has been demonstrated to enhance intestinal macronutrient absorption in a few randomized controlled trials (RCTs) [101, 102]. Jäger et al. (2020) reported that multi-strain probiotic supplementation increased the absorption of plant proteins in the diet of physically active men [89]. Vegetable proteins contain low amounts of BCAAs. Among BCAAs, especially leucine is of high importance for muscle protein turnover. Huang et al. (2019) reported that L. plantarum PS128 supplementation improved BCAA absorption after intense exercise and thus maintained exercise performance by increasing muscle power [12]. This finding was also supported by Tarik et al. using Bacillus coagulans Unique IS-2 support [102].
Probiotic supplementation can improve physical performance by increasing muscle protein turnover, muscle strength and endurance, fatigue indicators, and aerobic capacity. Lactobacillus and Bifidobacterium strains can ameliorate exercise-induced fatigue indicators [66••, 103]. Furthermore, multi-strain probiotic supplementation has been reported to increase maximal oxygen uptake and decrease maximal heart rate in road cyclists [98••]. Conversely, Axling et al. (2020) conducted a study which revealed that L. plantarum 299v had no impact on aerobic capacity, which was not dissimilar to the effect observed with iron supplementation [104]. The study results may have differed according to the protocols, such as the dose, composition, and test time of probiotics, assessment methods of aerobic capacity, and target population. In addition, some athletes with a lower VO2max can compensate for their performance by using a higher ratio of VO2max to obtain similar oxygen uptake during a race [97].
Currently, the relationship between probiotic supplementation and physical performance in athletes has received increasing attention from researchers. Despite promising findings, a few researchers have shown that probiotics do not affect the physical performance of athletes [105,106,107]. These current studies were mostly conducted using a single-strain probiotic supplement or B. subtilis DE111 supplement. In addition, physical performance measurements have been associated with aerobic capacity in some studies. Aerobic capacity is recognized as an important component of physical performance, and its measurement has almost become routine in the physiological testing of elite athletes [108]. However, physical performance is associated with a combination of several factors, such as type I muscle fibers, glycogen storage capacity, anaerobic power, and aerobic capacity [97]. Consequently, these differences in the evaluation of the results can lead to heterogeneous findings regarding physical performance. It is important to conduct further research to understand the relationship between probiotics and physical performance and provide clearer inferences.
Intense exercise increases intestinal permeability and endotoxemia by causing GI disturbances. This causes an increase in plasma LPS levels in the blood, thus increasing the secretion of proinflammatory cytokines, such as IL1, IL6, and TNF-α, from monocytes [47, 48]. Probiotic supplementation may alleviate the increased inflammatory response after exercise. In a meta-analysis, probiotic supplementation was found to reduce proinflammatory cytokine levels in elite athletes [34•]. Additionally, intense exercises temporarily suppress the immune response and, as a result, increase the risk of infections such as URTIs [46]. Limited current studies with a few participants are available, showing the effect of probiotics on URTI symptoms in athletes. These studies provide conflicting findings regarding the incidence and severity of URTI symptoms [109, 110]. In a meta-analysis, probiotic supplementation had no effect on the number of days of illness or mean number or duration of URTI episodes. However, single-strain probiotics, in particular, have been reported to reduce the total symptom severity score of URTIs [78•]. In this current review, studies investigating the effect of probiotics on URTI were conducted using multi-strain supplementation.
Studies demonstrating the effects of probiotic supplementation on sports performance either, directly or indirectly, present conflicting findings. These discrepancies are thought to be due to different methodologies, such as supplementation type (single or multi-strain) and timing [111, 112]. Factors such as dose of probiotic used, duration of the study, and the evaluation of the data are also likely to affect the results of the studies [98••]. Additionally, information about the microbiome and dietary patterns of athletes has not been investigated in most current studies, which may have caused the findings to be different.
Conclusion and Future Perspectives
In conclusion, in this review, we consider some potential effects of probiotics such as a decrease in intestinal permeability, decrease in inflammation, decrease in symptoms of upper respiratory tract infections, increase in aerobic capacity, and modulation of immune response. Accordingly, probiotics may be recommended for individuals who exercise. However, the exclusion of information about the microbiome of the athletes and their diets at the beginning of current studies limits the assessment of the results obtained. Additionally, it is difficult to determine direct evidence between exercise-induced impairments in cytokine secretion, intestinal barrier function, and immune response and improvements after probiotic supplementation in these studies. Therefore, well-designed interventional studies are needed to clarify the effects of probiotic supplementation on sports performance. These studies should also evaluate different markers of bowel barrier function, inflammation, and aerobic capacity. Additionally, it may be important to focus on how probiotics alone or in combination with prebiotics can affect the exercise performance of athletes. Further studies are required to draw firm conclusions, as most studies have important methodological limitations such as study design, variation in populations, strain types used, and criteria used to evaluate performance.
Data Availability
The data that support the findings of this study are available from the corresponding author.
References
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
Das TK, et al. Current status of probiotic and related health benefits. Appl Food Res. 2022;2(2):100185.
Hotel, A. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria – Joint FAO/WHO Expert Consultation. 2001.
Misra S, Pandey P, Mishra HN. Novel approaches for co-encapsulation of probiotic bacteria with bioactive compounds, their health benefits and functional food product development: a review. Trends Food Sci Technol. 2021;109:340–51.
Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A. Mechanisms of action of probiotics. Adv Nutr. 2019;10(suppl_1):S49-66.
Mazloom K, Siddiqi I, Covasa M. Probiotics: how effective are they in the fight against obesity? Nutrients. 2019;11(2):258.
Azad MAK, et al. Probiotic species in the modulation of gut microbiota: an overview. Biomed Res Int. 2018;2018:1–8.
Lin T-L, et al. Investiture of next generation probiotics on amelioration of diseases – strains do matter. Med Microecol. 2019;1–2: 100002.
Robles-Vera I, Toral M, Romero M, Jiménez R, Sánchez M, Pérez-Vizcaíno F, Duarte J. Antihypertensive effects of probiotics. Curr Hypertens Rep. 2017;19:1-8.
Clarke SF, et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014;63(12):1913–20.
Mohr AE, et al. The athletic gut microbiota. J Int Soc Sports Nutr. 2020;17(1).
Lee M-C, et al. Probiotic Lactiplantibacillus plantarum Tana isolated from an international weightlifter enhances exercise performance and promotes antifatigue effects in mice. Nutrients. 2022;14(16):3308.
Huang W-C, et al. The beneficial effects of Lactobacillus plantarum PS128 on high-intensity, exercise-induced oxidative stress, inflammation, and performance in triathletes. Nutrients. 2019;11(2):353.
Cox AJ, et al. Oral administration of the probiotic Lactobacillus fermentum VRI-003 and mucosal immunity in endurance athletes. Br J Sports Med. 2010;44(4):222–6.
Roberts J, et al. An exploratory investigation of endotoxin levels in novice long distance triathletes, and the effects of a multi-strain probiotic/prebiotic, antioxidant intervention. Nutrients. 2016;8(11):733.
Kekkonen RA, et al. The effect of probiotics on respiratory infections and gastrointestinal symptoms during training in marathon runners. Int J Sport Nutr Exerc Metab. 2007;17(4):352–63.
Gleeson M, et al. Effects of a Lactobacillus salivarius probiotic intervention on infection, cold symptom duration and severity, and mucosal immunity in endurance athletes. Int J Sport Nutr Exerc Metab. 2012;22(4):235–42.
Ozen M, Dinleyici EC. The history of probiotics: the untold story. Benef Microbes. 2015;6(2):159–65.
O’Toole PW, Marchesi JR, Hill C. Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nat Microbiol. 2017;2(5):17057.
Sanders ME, et al. Probiotics for human use. Nutr Bull. 2018;43(3):212–25.
Binda S, et al. Criteria to qualify microorganisms as “probiotic” in foods and dietary supplements. Front Microbiol. 2020;11.
Koutsoumanis K, et al. Update of the list of QPS-recommended biological agents intentionally added to food or feed as notified to EFSA 15: suitability of taxonomic units notified to EFSA until September 2021. EFSA J. 2022;20(1).
Zhang K, et al. Fermented dairy foods intake and risk of cancer. Int J Cancer. 2019;144(9):2099–108.
Nozue M, et al. Fermented soy products intake and risk of cardiovascular disease and total cancer incidence: the Japan Public Health Center-based Prospective study. Eur J Clin Nutr. 2021;75(6):954–68.
Nagpal R, et al. Human-origin probiotic cocktail increases short-chain fatty acid production via modulation of mice and human gut microbiome. Sci Rep. 2018;8(1):12649
Toscano M, et al. Effect of Lactobacillus rhamnosusHN001 andBifidobacterium longumBB536 on the healthy gut microbiota composition at phyla and species level: a preliminary study. World J Gastroenterol. 2017;23(15):2696.
Butel MJ. Probiotics, gut microbiota and health. Med Mal Infect. 2014;44(1):1–8.
Ren S, et al. Lactobacillus paracasei from koumiss ameliorates diarrhea in mice via tight junctions modulation. Nutrition. 2022;98: 111584.
Bagga D, et al. Influence of 4-week multi-strain probiotic administration on resting-state functional connectivity in healthy volunteers. Eur J Nutr. 2019;58(5):1821–7.
Chong H-X, et al. Lactobacillus plantarum DR7 improved upper respiratory tract infections via enhancing immune and inflammatory parameters: a randomized, double-blind, placebo-controlled study. J Dairy Sci. 2019;102(6):4783–97.
Suliburska J, et al. The impact of multispecies probiotics on calcium and magnesium status in healthy male rats. Nutrients. 2021;13(10):3513.
Vargoorani ME, et al. Stimulatory effects of Lactobacillus casei derived extracellular vesicles on toll-like receptor 9 gene expression and cytokine profile in human intestinal epithelial cells. J Diabetes Metab Disord. 2020;19(1):223–31.
Yu H-S, et al. Anti-inflammatory potential of probiotic strain Weissella cibaria JW15 isolated from kimchi through regulation of NF- -κB and MAPKs pathways in LPS-induced RAW 264.7 cells. J Microbiol Biotechnol. 2019;29(7):1022–1032.
Dai Y, et al. Probiotics improve renal function, glucose, lipids, inflammation and oxidative stress in diabetic kidney disease: a systematic review and meta-analysis. Ren Fail. 2022;44(1):862–80.
• Guo Y-T, et al. Effects of probiotic supplementation on immune and inflammatory markers in athletes: a meta-analysis of randomized clinical trials. Medicina. 2022;58(9):1188. This study is the first meta-analysis to examine the effects of probiotic supplementation on the levels of inflammatory markers. Researchers had reported inconsistent results regarding the effect of probiotics on inflammatory markers. This meta-analysis presented which inflammatory biomarkers probiotics were effective on before and after exercise.
Rizzo A, et al. Lactobacillus plantarum reduces Streptococcus pyogenes virulence by modulating the IL-17, IL-23 and Toll-like receptor 2/4 expressions in human epithelial cells. Int Immunopharmacol. 2013;17(2):453–61.
Gao F, Fang Z, Lu W. Regulation divergences of Lactobacillus fermentum PCC and Lactobacillus paracasei 431 on penicillin-induced upper respiratory tract microbial dysbiosis in BALB/c mice. Food Funct. 2021;12(23):11913–25.
Geng S, et al. Gut microbiota are associated with psychological stress-induced defections in intestinal and blood-brain barriers. Front Microbiol. 2019;10:3067.
Sun J, et al. Clostridium butyricum attenuates chronic unpredictable mild stress-induced depressive-like behavior in mice via the gut-brain axis. J Agric Food Chem. 2018;66(31):8415–21.
Nakaita Y, Kaneda H, Shigyo T. Heat-killed Lactobacillus brevis SBC8803 induces serotonin release from intestinal cells. Food Nutr Sci. 2013;04(08):767–71.
Huang C, et al. Restorative effects of Lactobacillus rhamnosus LR-32 on the gut microbiota, barrier integrity, and 5-HT metabolism in reducing feather-pecking behavior in laying hens with antibiotic-induced dysbiosis. Front Microbiol. 2023;14:1173804
Chew W, et al. Gut-muscle crosstalk. A perspective on influence of microbes on muscle function. Front Med. 2023;9:1065365
Giron M, et al. Gut microbes and muscle function: can probiotics make our muscles stronger? J Cachexia Sarcopenia Muscle. 2022;13(3):1460–76.
Lee C-C, et al. Lactobacillus plantarum TWK10 attenuates aging-associated muscle weakness, bone loss, and cognitive impairment by modulating the gut microbiome in mice. Front Nutr. 2021;8:708096
Chen L-H, et al. Lactobacillus paracasei PS23 decelerated age-related muscle loss by ensuring mitochondrial function in SAMP8 mice. Aging. 2019;11(2):756–70.
Lee M-C, et al. In vivo ergogenic properties of the Bifidobacterium longum OLP-01 isolated from a weightlifting gold medalist. Nutrients. 2019;11(9):2003.
Leite GSF, et al. Probiotics and sports: a new magic bullet? Nutrition. 2019;60:152–60.
Gill SK, et al. Circulatory endotoxin concentration and cytokine profile in response to exertional-heat stress during a multi-stage ultra-marathon competition. Exerc Immunol Rev. 2015;21:114–28.
Pugh JN, et al. Gastrointestinal symptoms in elite athletes: time to recognise the problem? Br J Sports Med. 2018;52(8):487–8.
Suzuki K, Hayashida H. Effect of exercise intensity on cell-mediated immunity. Sports. 2021;9(1):8.
Nishihira J. Chapter 36 - The role of probiotics in sports: application of probiotics to endurance exercise, in nutrition and enhanced sports performance (Second Edition), D. Bagchi, S. Nair, and C.K. Sen, Editors. 2019. Academic Press. 423–428.
West NP, et al. Lactobacillus fermentum (PCC®) supplementation and gastrointestinal and respiratory-tract illness symptoms: a randomised control trial in athletes. Nutr J. 2011;10(1):30.
Lee M-C, et al. Effectiveness of human-origin Lactobacillus plantarum PL-02 in improving muscle mass, exercise performance and anti-fatigue. Sci Rep. 2021;11(1):19469
Huang W-C, et al. Exercise training combined with Bifidobacterium longum OLP-01 supplementation improves exercise physiological adaption and performance. Nutrients. 2020;12(4):1145.
Yan Y, et al. Probiotic Bifidobacterium lactis V9 attenuates hepatic steatosis and inflammation in rats with non-alcoholic fatty liver disease. AMB Express. 2020;10(1):101
Grosicki GJ, Fielding RA, Lustgarten MS. Gut microbiota contribute to age-related changes in skeletal muscle size, composition, and function: biological basis for a gut-muscle axis. Calcif Tissue Int. 2018;102(4):433–42.
Ticinesi A, et al. Gut microbiota, muscle mass and function in aging: a focus on physical frailty and sarcopenia. Nutrients. 2019;11(7):1633.
Li Y, et al. Co-administering yeast polypeptide and the probiotic, Lacticaseibacillus casei Zhang, significantly improves exercise performance. J Funct Foods. 2022;95: 105161.
Peters HPF. Potential benefits and hazards of physical activity and exercise on the gastrointestinal tract. Gut. 2001;48(3):435–9.
De Oliveira EP, Burini RC, Jeukendrup A. Gastrointestinal complaints during exercise: prevalence, etiology, and nutritional recommendations. Sports Med. 2014;44(S1):79–85.
Marlicz W, Loniewski I. The effect of exercise and diet on gut microbial diversity. Gut. 2015;64(3):519–20.
Frampton J, et al. Short-chain fatty acids as potential regulators of skeletal muscle metabolism and function. Nat Metab. 2020;2(9):840–8.
Gao Z, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58(7):1509–17.
Zhang B, et al. The I allele of the angiotensin-converting enzyme gene is associated with an increased percentage of slow-twitch type I fibers in human skeletal muscle. Clin Genet. 2003;63(2):139–44.
Kim N, et al. Mind-altering with the gut: modulation of the gut-brain axis with probiotics. J Microbiol. 2018;56(3):172–82.
Santosa S, Farnworth E, Jones PJ. Probiotics and their potential health claims. Nutr Rev. 2006;64(6):265–74.
•• Pugh JN, et al. Four weeks of probiotic supplementation alters the metabolic perturbations induced by marathon running: insight from metabolomics. Metabolites. 2021;11(8):535. This study has characterized the mechanisms by which probiotic supplementation could result in beneficial physiological effects in athletes by untargeted metabolomics analysis. The metabolomic profile of athletes may reveal new insights into how probiotics affect systemic metabolism and improve exercise performance.
Huang W-C, et al. Lactobacillus plantarum PS128 improves physiological adaptation and performance in triathletes through gut microbiota modulation. Nutrients. 2020;12(8):2315.
de Paiva AKF, et al. Effects of probiotic supplementation on performance of resistance and aerobic exercises: a systematic review. Nutr Rev. 2023;81(2):153–67.
Brock-Utne JG, et al. Endotoxaemia in exhausted runners after a long-distance race. S Afr Med J. 1988;73(9):533–6.
Lamprecht M, et al. Probiotic supplementation affects markers of intestinal barrier, oxidation, and inflammation in trained men; a randomized, double-blinded, placebo-controlled trial. J Int Soc Sports Nutr. 2012;9(1):45.
Maughan RJ, et al. IOC consensus statement: dietary supplements and the high-performance athlete. Br J Sports Med. 2018;52(7):439–55.
Ng SC, et al. Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis. 2009;15(2):300–10.
Plaza-Diaz J. Modulation of immunity and inflammatory gene expression in the gut, in inflammatory diseases of the gut and in the liver by probiotics. World J Gastroenterol. 2014;20(42):15632.
Miettinen M, Vuopio-Varkila J, Varkila K. Production of human tumor necrosis factor alpha, interleukin-6, and interleukin-10 is induced by lactic acid bacteria. Infect Immun. 1996;64(12):5403–5.
Nazemian V, et al. Probiotics and inflammatory pain: a literature review study. Middle East J Rehabil Health. 2016;3(2).
Ohland CL, Macnaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 2010;298(6):G807–19.
Starkie RL, et al. Circulating monocytes are not the source of elevations in plasma IL-6 and TNF-alpha levels after prolonged running. Am J Physiol Cell Physiol. 2001;280(4):C769–74.
• Łagowska K, Bajerska J. Probiotic supplementation and respiratory infection and immune function in athletes: systematic review and meta-analysis of randomized controlled trials. J Athl Train. 2021;56(11):1213–1223. This study is the first systematic review and meta-analysis to investigate the effect of probiotic supplementation on respiratory tract infection. Moreover, as in this review, the authors analyzed the effect of not only multi-strain but also single-strain probiotic supplementation on the total symptom severity score of URTI.
Nieman DC, et al. Change in salivary IgA following a competitive marathon race. Int J Sports Med. 2002;23(1):69–75.
Nehlsen-Cannarella SL, et al. Saliva immunoglobulins in elite women rowers. Eur J Appl Physiol. 2000;81(3):222–8.
Killer SC, Svendsen IS, Gleeson M. The influence of hydration status during prolonged endurance exercise on salivary antimicrobial proteins. Eur J Appl Physiol. 2015;115(9):1887–95.
Walsh NP. The effects of high-intensity intermittent exercise on saliva IgA, total protein and alpha-amylase. J Sports Sci. 1999;17(2):129–34.
Mooren FC, Lechtermann A, Völker K. Exercise-induced apoptosis of lymphocytes depends on training status. Med Sci Sports Exerc. 2004;36(9):1476–83.
Siedlik JA, et al. Acute bouts of exercise induce a suppressive effect on lymphocyte proliferation in human subjects: a meta-analysis. Brain Behav Immun. 2016;56:343–51.
De Oliveira E, Burini R. Carbohydrate-dependent, exercise-induced gastrointestinal distress. Nutrients. 2014;6(10):4191–9.
Van Wijck K, et al. Exercise-induced splanchnic hypoperfusion results in gut dysfunction in healthy men. PLoS ONE. 2011;6(7): e22366.
Jäger R, et al. ProbioticBacillus coagulansGBI-30, 6086 reduces exercise-induced muscle damage and increases recovery. PeerJ. 2016;4: e2276.
Jäger R, Mohr AE, Pugh JN. Recent advances in clinical probiotic research for sport. Curr Opin Clin Nutr Metab Care. 2020;23(6):428–36.
Jäger R, et al. Probiotic administration increases amino acid absorption from plant protein: a placebo-controlled, randomized, double-blind, multicenter, crossover study. Probiotics and Antimicrobial Proteins. 2020;12(4):1330–9.
Sim M, et al. Iron considerations for the athlete: a narrative review. Eur J Appl Physiol. 2019;119(7):1463–78.
Vonderheid SC, et al. A systematic review and meta-analysis on the effects of probiotic species on iron absorption and iron status. Nutrients. 2019;11(12):2938.
Jäger R, et al. International Society of Sports Nutrition Position Stand: probiotics. J Int Soc Sports Nutr. 2019;16(1):62
Yan H, Baldridge MT, King KY. Hematopoiesis and the bacterial microbiome. Blood. 2018;132(6):559–64.
Salva S, et al. Dietary supplementation with probiotics improves hematopoiesis in malnourished mice. PLoS ONE. 2012;7(2): e31171.
Long Y, et al. Gut Microbiota signatures in gestational anemia. Front Cell Infection Microbiol. 2021;11:549678
Lajqi T, et al. The role of microbiota in neutrophil regulation and adaptation in newborns. Front Immunol. 2020;11:568685
Bosquet L, Léger L. Methods to determine aerobic endurance. Sports Med. 2002;32(11):675–700.
•• Mazur-Kurach P, Frączek B, Klimek AT. Does multi-strain probiotic supplementation impact the effort capacity of competitive road cyclists? Int J Environ Res Public Health. 2022;19(19):12205. This placebo-controlled study examined the exercise capacity of a multi-strain probiotic supplement in road cyclists. The authors measured aerobic capacity, one of the important components of exercise capacity, not only through exercise duration, maximum load power, and maximal heart rate, but also maximal oxygen uptake. This study is the rare study that directly examines the effect of multi-strain probiotic supplementation on aerobic capacity using a cycle ergometer.
Schreiber C, et al. The effect of probiotic supplementation on performance, inflammatory markers and gastro-intestinal symptoms in elite road cyclists. J Int Soc Sports Nutr. 2021;18(1):36
Smarkusz-Zarzecka J, et al. Effect of a multi-strain probiotic supplement on gastrointestinal symptoms and serum biochemical parameters of long-distance runners: a randomized controlled trial. Int J Environ Res Public Health. 2022;19(15):9363.
Pugh JN, et al. Probiotic supplementation increases carbohydrate metabolism in trained male cyclists: a randomized, double-blind, placebo-controlled crossover trial. Am J Physiol-Endocrinol Metab. 2020;318(4):E504–13.
Tarik M, et al. The effect of Bacillus coagulans Unique IS-2 supplementation on plasma amino acid levels and muscle strength in resistance trained males consuming whey protein: a double-blind, placebo-controlled study. Eur J Nutr. 2022;61(5):2673–85.
Harnett JE, et al. Probiotic supplementation elicits favourable changes in muscle soreness and sleep quality in rugby players. J Sci Med Sport. 2021;24(2):195–9.
Axling U, et al. The effect of Lactobacillus plantarum 299v on iron status and physical performance in female iron-deficient athletes: a randomized controlled trial. Nutrients. 2020;12(5):1279.
Toohey JC, et al. Effects of probiotic (Bacillus subtilis) supplementation during offseason resistance training in female division I athletes. J Strength Cond Res. 2020;34(11):3173–81.
Carbuhn A, et al. Effects of probiotic (Bifidobacterium longum 35624) supplementation on exercise performance, immune modulation, and cognitive outlook in division I female swimmers. Sports. 2018;6(4):116.
Townsend J, et al. Effects of probiotic (Bacillus subtilis DE111) supplementation on immune function, hormonal status, and physical performance in division I baseball players. Sports. 2018;6(3):70.
Ranković G, et al. Aerobic capacity as an indicator in different kinds of sports. Bosn J Basic Med Sci. 2010;10(1):44–8.
Tavares-Silva E, et al. Effect of multi-strain probiotic supplementation on URTI symptoms and cytokine production by monocytes after a marathon race: a randomized, double-blind, placebo study. Nutrients. 2021;13(5):1478.
Batatinha H, et al. Probiotic supplementation in marathonists and its impact on lymphocyte population and function after a marathon: a randomized placebo-controlled double-blind study. Sci Rep. 2020;10(1):18777
Tong TK, Fu FH, Chow BC. Reliability of a 5-min running field test and its accuracy in VO2max evaluation. J Sports Med Phys Fitness. 2001;41(3):318–23.
Santibañez-Gutierrez A, et al. Effects of probiotic supplementation on exercise with predominance of aerobic metabolism in trained population: a systematic review, meta-analysis and meta-regression. Nutrients. 2022;14(3):622.
Lee M-C, et al. Live and heat-killed probiotic Lactobacillus paracasei PS23 accelerated the improvement and recovery of strength and damage biomarkers after exercise-induced muscle damage. Nutrients. 2022;14(21):4563.
••Lee C-C, et al. Different impacts of heat-killed and viable Lactiplantibacillus plantarum TWK10 on exercise performance, fatigue, body composition, and gut microbiota in humans. Microorganisms. 2022;10(11):2181. This placebo-controlled trial investigated the effects of both viable and heat-killed probiotic supplementation in improving exercise performance and reducing exercise-induced inflammatory responses. Additionally, bacterial diversity comparison was performed using 16S RNA sequencing in fecal samples to determine how the overall profile of microbial composition was modulated by administration of viable or heat-killed TWK10.
Engel S, et al. Safety of Bifidobacterium breve, Bif195, employing a human exercise-induced intestinal permeability model: a randomised, double-blinded, placebo-controlled, parallel group trial. Beneficial Microbes. 2022;13(3):243–52.
Salleh RM, et al. Effects of probiotics on anxiety, stress, mood and fitness of badminton players. Nutrients. 2021;13(6):1783.
Smarkusz-Zarzecka J, et al. Analysis of the impact of a multi-strain probiotic on body composition and cardiorespiratory fitness in long-distance runners. Nutrients. 2020;12(12):3758.
Lin C-L, et al. Bifidobacterium longum subsp. longum OLP-01 supplementation during endurance running training improves exercise performance in middle- and long-distance runners: a double-blind controlled trial. Nutrients. 2020;12(7):1972.
Dong W, et al. Bifidobacterium animalis subsp. lactis BB-12 improves the state anxiety and sports performance of young divers under stress situations: a single-arm, prospective proof-of-concept study. Front Psychol. 2021;11:570298
Pugh JN, et al. Four weeks of probiotic supplementation reduces GI symptoms during a marathon race. Eur J Appl Physiol. 2019;119(7):1491–501.
Axelrod CL, et al. UCC118 supplementation reduces exercise-induced gastrointestinal permeability and remodels the gut microbiome in healthy humans. Physiol Rep. 2019;7(22):e14276
Ibrahim NS, et al. Effects of probiotics supplementation and circuit training on immune responses among sedentary young males. J Sports Med Phys Fitness. 2018;58(7–8):1102–9.
Ibrahim NS, et al. The effects of combined probiotic ingestion and circuit training on muscular strength and power and cytokine responses in young males. Appl Physiol Nutr Metab. 2018;43(2):180–6.
Acknowledgements
The figure and table produced by Miray Nur Aykut (first author) are original.
Funding
Open access funding provided by the Scientific and Technological Research Council of Türkiye (TÜBİTAK).
Author information
Authors and Affiliations
Contributions
AYKUT, MN: conceptualization, writing, drawing and editing; ERDOĞAN, EN: conceptualization, writing and editing; ÇELİK MN: writing and editing; GÜRBÜZ, M: conceptualization, writing, editing and supervision. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics Approval
The authors declare that the article is original and not submitted anywhere else and the table and figure included in the article are original.
Conflict of Interest
The authors declare no competing interests.
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Aykut, M.N., Erdoğan, E.N., Çelik, M.N. et al. An Updated View of the Effect of Probiotic Supplement on Sports Performance: A Detailed Review. Curr Nutr Rep 13, 251–263 (2024). https://doi.org/10.1007/s13668-024-00527-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13668-024-00527-x