Implications of the Gut Microbiome in Sports

Abstract

Context:

Two-thirds of an individual’s gut microbiota is unique and influenced by dietary and exercise habits, age, sex, genetics, ethnicity, antibiotics, health, and disease. It plays important roles in nutrient and vitamin metabolism, inflammatory modulation, immune system function, and overall health of an individual. Specifically, in sports it may help decrease recovery time and improve athletic performance.

Evidence Acquisition:

PubMed and Medline databases were used for the literature search. Bibliographies based on the original search were utilized to pursue further literature search.

Study Design:

Clinical review.

Level of Evidence:

Level 4.

Results:

Diet and exercise play very important roles in the composition of the gut microbiota in the athletic and nonathletic individual. Ingestion of carbohydrates during and after exercise seems to have an anti-inflammatory effect postexercise. Supplementation with probiotic seems to aid in recovery after exercise, too, especially restoring the “normal” gut microbiota. Physically active individuals of all levels have more alpha diversity and “health-promoting gut species” in their microbiome than nonactive individuals, along with higher concentrations of short-chain fatty acids (SCFA) and SCFA-producing organisms. However, exercise interventions should be longer than 8 weeks to see these positive characteristics. Immune function is highly influenced by the gut microbiota’s response to exercise. A transient immune dysfunction occurs after prolonged high-intensity exercise, which correlates with microbiota dysregulation. Nevertheless, long-term exposure to exercise will enhance the immune response and lead to positive changes in the gut microbiota.

Conclusion:

Although the exact mechanisms of the effects that diet, exercise, and genetics have on the gut microbiota remain largely unknown, there is evidence that suggests overall health benefits. In the athletic population, these benefits can ultimately lead to performance improvement.

The adult gut microbiota contains up to 100 trillion microorganisms, including not only bacteria but also a diverse community of archaea, viruses, protozoans, and microfungi.^25,27,24 Collectively, the microbiota contributes to the gut microbiome, which is a rich collection of genomes from all the microorganisms residing in the human colon.^17,39 The number and diversity of microorganisms in the gut microbiome have been studied through the sequencing and analysis of ribosomal DNA and RNA. One-third of the gut microbiota is common among all individuals and the other two-thirds are unique to each individual. While studies are still limited, gut microbiome can be influenced by a variety of intrinsic, lifestyle, and environmental factors such as dietary and exercise habits, age, gender, genetics, ethnicity, antibiotics use, health, and disease.^3,27 The gut microbiota plays important roles in nutrient and vitamin metabolism, inflammatory modulation, immune system function, and overall health of an individual.^24,32,39 Thus, understanding the role of the microbiome is of particular interest in elite-level athletes—those who are performing high-intensity exercise over extended periods of time—because of its potential value in enhancing athletic performance and reducing training recovery time, but also in altering the risk of illness.

The aim of this article is to review the effect of nutrition and physical activity on the microbiome and to describe its role in immune function, as they relate to athletic performance and recovery time in the athlete.

Impact of Nutrition on the Gut Microbiome

Nutrition plays an important role in the gut microbiota environment by shaping and influencing its composition. Dietary changes can alter gut microbial diversity within a 24-hour period. ²⁴ In general, the gut microbiota produces enzymes that will help digest nutrients not normally broken down by human digestive enzymes. For example, enzymatic digestion and fermentation of carbohydrates produces short-chain fatty acids (SCFA), such as butyrate (which makes up the majority of SCFAs), acetate, and propionate. Each SCFA has different effects both locally and systematically on the gut, microbiota flora population, and human body. Butyrate affects the local colonic epithelium metabolism and gene expression, whereas acetate and propionate affect systemic circulation and are taken up by adipose tissue and the liver, which help make up 10% of the energy used by the host. ²⁴

Depending on the type and amount of nutrients consumed, fermentation by gut microbiota may lead to colonic or systemic effects. For example, high protein with concurrent high saturated fat diets may lead to a negative impact on colonic barrier function and epithelial cell metabolism, increased activity by proteolytic bacteria such as Clostridium, an increase in the production of branched chain fatty acids, lactate, amine sulfides, and indoles, which increase gut permeability and expose the body systemically to harmful and inflammatory protein fermentation byproducts. ²⁴ An important note is that the effect of a high-protein (plant more than animal based), low-fat diet on the gut microbiota is not well-known but is very important in the athletic population. ²⁴ Fatty diets increase the prevalence of bile acid resistant gut bacteria such as Bacteroides and Bilophila. An increase in these bacteria populations raises one’s risk of developing inflammatory bowel disease, while the disruption of the balance between Bacteroides and Firmicutes phyla increases the presence of inflammatory cytokines and liposaccharides in the body. ²⁴ It is theorized that the relationship between gut flora diversity, colonic wall permeability, and microbiota byproducts may predispose one to autoimmune conditions such as Crohn’s disease and allergies. ²⁴

The human gut has more enzymes to break down fats and proteins than it does for carbohydrates. Carbohydrates are typically the main source of fuel for muscular activity and are required to maintain and replete glycogen stores. The recommended amount of carbohydrate intake prior, during, and after exercise varies on the individual and with the duration and type of activity. Most carbohydrates are enzymatically digested and absorbed in the small intestine, with complex carbohydrates (such as fruits and vegetables) in the form of fiber, being used as fuel for microbiota and modulation of bacteria groups. It has been suggested that complex carbohydrates, often avoided prior to and during competition to avoid gastrointestinal distress, assist in reducing the potentially negative effects of high protein consumption and increase fat oxidation.^10,24 During and after exercise, carbohydrate ingestion has been linked with decreased postexercise inflammation by reducing stress hormone levels. ²⁷ A high proportion of ingested polyphenols from fruits (such as dates, raisins, and bananas), vegetables, and other plant foods pass through the small intestine unabsorbed and reach the colon exerting anti-inflammatory, antiviral, antioxidative, and immune cell signaling effects that may enhance metabolic recovery. ²⁷

Dietary supplements in the form of prebiotics and probiotics may also similarly modify the gut microbiome. Prebiotics are indigestible substrates that are selectively used and fermented by host microorganisms, which confer a health benefit. Examples of prebiotics include inulin, oligosaccharide, and arabinogalactans.^9,31 These substances often serve as fiber for host bacteria and may be found in human breast milk or foods such as bananas, carrots, flax and chia seeds, garlic, yams, and asparagus. In contrast, as defined by the World Health Organization, probiotics are “live microorganisms,” and “when administered in adequate amounts, [may also] confer a health benefit [to] the host.” ¹⁷ Examples of probiotics include bacterial and yeast strains, with most probiotics generally the same beneficial microbiota species found in the human gut (eg, Lactobacillus and Escherichia coli bacteria). ³¹ They can be found and commercially sold in the form of capsules, powders, or in yogurt, kombucha, and wine. There is emerging evidence to suggest that some probiotics are able to perform several functions. Consumption of probiotics may help ease gastrointestinal symptoms such as abdominal cramping, bloating, reflux symptoms; decrease vulnerability to infections; and boost immune function.^17,39 For example, in both animal and mouse model studies, Faecalibacterium prausnitzii strains seem to show promise as protective against inflammatory bowel disease and to upregulate the expression of the anti-inflammatory cytokine, interleukin 10.^4,31,35 However, thus far there is only level 1 evidence for probiotics in the “prevention of antibiotic associated diarrhea, post Heliobacter pylori treatment, prevention of postoperative sepsis infection after gastrointestinal surgeries, lactose maldigestion, and reducing symptoms associated with pouchitis post ulcerative colitis surgery.” ³¹

There are no large, prospective, double-blinded, randomized controlled studies assessing the role of nutrition and its effect on gut microbiota and on human athletic performance. However, there are some small studies looking at the effect of probiotics on endurance athletes. Most studies have looked at the effect of probiotic supplementation on aerobic exercise performance measures such as VO_2max, run time to fatigue, and 10-yard sprint, with some looking at strength and anaerobic measures such as grip strength, 1 repetition max lifts, or vertical jump power. ¹⁵ A majority have shown null or mixed beneficial effects on performance,^15,24 with some positive effects on run time to fatigue,^13,15,36-38 body composition, ¹⁴ and inflammatory markers.^13,23

Effect of Physical Activity on the Gut Microbiota

The effect of physical activity on the gut microbiome has only recently been a focus of research. Initial research was restricted to animal models. In recent years, there has been an increase in human studies because of advances in techniques and technologies that allow better quantification of the human gut microbiome, but the mechanism(s) by which exercise influences the gut microbiota is unknown.^1,6,11,20 Studies have been designed comparing athletes with nonathletes and creating interventions to measure the impact of acute bouts of exercises less than 60 minutes on gut microbiome. An ever-present cofounding variable is the impact of diet in these studies.

The 2 most common approaches to measure the effect of physical activity on gut microbiome are assessments of gut microbiome diversity and quantification of SCFA. Gut microbiome diversity is divided into alpha diversity and beta diversity. Alpha diversity refers to bacterial diversity within 1 sample or individual. Beta diversity refers to bacterial diversity among different samples or individuals. ¹¹ Although there is great variation in studies, Faecalibacterium prausnitzii, Roseburia hominis, Akkermansia muciniphila, and Prevotella species are some of the most commonly referenced as healthy or health-promoting gut species. ²⁴

Two recent systematic reviews^24,29 have summarized the findings of human studies. Both found there is limited high-quality evidence regarding the impact of exercise on the gut microbiome of humans. The limited evidence that does exist in humans indicates that physically active/exercising individuals have a higher abundance of health-promoting species within the gut microbiota as well as increased diversity of species (alpha diversity). High physical fitness is associated with higher levels of SCFA and/or higher concentrations of the bacteria that produce SCFA. A key distinction was seen between analysis of high-fitness individuals and analysis that used exercise interventions. Short-duration exercise interventions (<8 weeks) had little or no impact on the bacterial alpha or beta diversity. The authors proposed that longer interventions (greater than 8 weeks) were needed to see beneficial change in the microbiome. ²⁹

Exercise seems to enhance the effect that specific diets have on microbiome composition. In elite race walkers, the combination of an intensive 3-week training program with a low-carbohydrate, high-fat diet resulted in the most dramatic changes in the oral microbiome with a resultant loss of exercise economy compared with those who were on a carbohydrate-rich diet. ²⁵ Increased protein, whether through meat/meat products or supplements, induced a greater species diversity. ⁵ The comparison across bodybuilders, distance runners, and controls, each ingesting a different sport-specific diet, revealed that the type of exercise training and athlete diet influenced the relative abundance of microbiota at both the genus and the species levels. ¹⁸ Bodybuilders ingested a high-protein, low-carbohydrate, and low-fiber diet, and demonstrated less SCFA-producing bacteria when compared with distance runners who ingested a low-protein, low-carbohydrate, low-fiber diet. ¹⁸

High heterogeneity of studies, few long-term interventions and high numbers of observational studies limit the ability to make strong conclusions about how exercise might influence the composition and activity of the gut microbiome, but this area of research has a promising impact on the athletic and nonathletic population.

The Role of the Microbiome in Immune Function

Both physical activity and the gut microbiota affect the function of the immune system. The gut microbiota plays a major role in the maturation of the immune system in part by signaling harmful bacteria and regulating the gut environment. ³ Dysbiosis or dysregulation of innocuous bacteria is reduced via mucosal regulatory T-cell activation by the microbiota helping decrease the risk of inflammatory medical conditions. Probiotic supplementation may modulate the immune system by increasing engagement of the mucosal immune system through toll-like receptors to help promote type 1 T helper cell differentiation ³¹ ; by maintaining tight junction proteins, which decrease gut permeability to harmful antigens and systemic exposure to endotoxins^17,34; by decreasing pathogen colonization by the creation of a more acidic environment (not ideal for proinflammatory bacteria, yet promotes growth of beneficial bacteria species such as Lactobacilli and Bifidobacterium strains); and increased secretion of circulating specific IgG, IgA, and IgM immunoglobulins.^3,8,19,33 Further research regarding what strains of bacteria and the safety and regulation of their use is required to better understand the potential beneficial effects. ³⁹

Although exercise has a chronic accumulative benefit in immune function, it may cause an acute transient immune dysfunction when performed for more than 60 minutes at high intensity. ²⁷ There is evidence in animal models that demonstrate proinflammatory changes in the colonic flora postexercise and thus a possible link with gut microbiota dysregulation. ³ Furthermore, it seems that the “normal” microbiota is not fully recovered after 72 hours. ³ This is the reasoning behind the possible role of consuming probiotics prior to long-duration exercise to promote gut microbiota recovery. On the other hand, an acute bout of moderate- to high-intensity exercise less than 60 minutes improves the antipathogen activity of tissue macrophages in parallel with an enhanced recirculation of immunoglobulins, anti-inflammatory cytokines, neutrophils, natural killer cells, cytotoxic T cells, and immature B cells; all processes associated with the gut microbiota. ²⁷

The Elite Athlete’s Microbiome

More studies have begun to shed light on how diet and exercise affects the gut microbiome, looking at subsets of athletes in diverse sports and training levels to determine whether there are differences in composition and function. With that being said, there does seem to be some consensus among studies comparing athletes with sedentary controls that appear to show a more diverse and healthier gut microbiota population.^15,17,24 A common finding in both murine and human studies has been an increase in alpha diversity, as a result of increased exercise. ³⁰ Moreover, many of these genera that are in higher abundance in the elite-level athlete negatively correlate with metabolic syndromes and obesity. As mentioned above, SCFA are derived from the gut microbiome. Butyrate, acetate, and propionate are commonly measured SCFA. Systemic reviews have found that athletes have enriched profile of SCFA and pathways that allow higher rate of production of SCFA. ²⁴ SCFA have been shown to have numerous health benefits and are associated with enhanced muscle turnover (fitness) and overall health.^12,21

The analysis of the gut microbial compositions of professional- and amateur-level cyclists found that those who cycled more than 11 hours per week had higher abundance of microbial genera known to upregulate numerous amino acid and carbohydrate metabolism pathways. ³⁰ Another study looking at the gut microbiota of Irish professional rugby players compared with healthy age- and sex-matched controls showed increased microbial diversity; whether this effect is directly correlated with exercise alone or a combination of increased exercise and strict dietary intake is not fully elucidated. ⁵ A comparison of professional international union rugby players with more sedentary controls resulted not only in differences in fecal microbiota compositionally, but the athletes also had increased amino acid and carbohydrate metabolism, enhanced muscle turnover and overall better health. ² While these studies looked at an individual sport, O’Donovan et al ²⁸ studied elite-level athletes across 16 different sports. The microbiome samples were significantly different from a microbial composition and potential functional perspective between the groups, though the etiology of these differences remains to be identified. ²⁸ It is, however, important to note that there were no significant differences in dietary nutrients between the groups studied, so the differences may, in fact, be exercise based.

In addition to the diversity of microorganisms composing the microbiome, some microorganisms have been linked to increasing performance in elite-level athletes. Scheiman et al ³⁶ recently identified an abundance of species in a particular genus, Veillonella, while studying athletes who ran the 2015 Boston Marathon. This genus is now believed to be linked to better performance in long-distance runners. It may increase the metabolism of lactate to propionate, improving run time in murine models. ³⁶ Based on studies of endurance athletes and populations from rural Africans, as well as some Asian countries, there seems to be an increased abundance of the bacteria genus Prevotella.^{7,16,22,24,26} It is unclear what effects this bacteria population has on the human gut and immune system since it is also affiliated with a few disease states. ²⁴

Conclusion

An individual’s microbiome seems to be influenced by multiple factors that in part correlate with characteristics present in the athletic population. Diet modifications and exercise may have synergistic effects on changes in the microbiome composition that may enhance immune function and athletic performance. These effects remain largely unknown and should be a research focus in the near future.