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Nutrition and Performance in Sport

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Christophe Hausswirth

Chapter 2. Nutrition, sport and health

Topic 3. Immunonutrition support for athletes: does it work?

David C Nieman

Résumé

Prolonged and intensive exercise causes transient physiologic stress, elevations in biomarkers related to inflammation and oxidative stress, immune dysfunction, and disturbances in host pathogen defense. Immunonutrition support for athletes is a burgeoning area of scientific investigation, and a variety of nutritional products have been tested as countermeasures to exercise-induced indicators of physiologic stress. Carbohydrate ingestion before, during, and after heavy exercise has emerged as an effective but partial countermeasure to immune dysfunction, with favourable effects on measures related to stress hormones and inflammation, but limited effects on oxidative stress and markers of innate or adaptive immunity. Flavonoid-rich plant extracts and unique flavonoid-nutrient mixtures partially counter exercise-induced oxidative stress, inflammation, and delayed onset of muscle soreness (DOMS), and additional research is needed to determine optimal dosing regimens and flavonoid-nutrient mixtures containing carbohydrate. Antioxidant, N-3 PUFAs, and glutamine supplements do not counter exercise-induced immune dysfunction, and vitamin E may actually compound the oxidative stress and inflammation experienced by the endurance athlete. More research is needed for mushroom and yeast β-glucan, probiotics, and bovine colostrum.

Texte intégral

1. Introduction

1Prolonged and intensive exercise has transient but significant, wide-ranging effects on the immune system (Gleeson, 2007; Nieman, 1997). The exercise-induced immune perturbations and associated physiologic stress are associated with an elevated risk of upper respiratory tract infections (URTI), especially during the one to two week period following competitive endurance races (Nieman, 2000, 2007, 2009).

2Immunonutrition support for athletes is an active area of research endeavor, and this chapter will summarize the efficacy of various nutritional products in countering exercise-induced immune dysfunction, oxidative stress, and inflammation (Gleeson, Nieman, & Pedersen, 2004; Nieman, 2008; Walsh et al. 2011). In contrast, near-daily moderate physical activity is associated with a reduced URTI risk, and favourable acute immune changes, thus falls outside the context of this chapter (Nieman et al, 2011).

3The value of using immunonutrition support for athletes has been questioned because blocking the transient oxidative stress, inflammation, and elevations in stress hormones following heavy exertion potentially interferes with important signalling mechanisms for training adaptations (Gomez-Cabrera, et al. 2008; Ristow et al. 2009). Another viewpoint is that even the most effective immunonutrition support systems only partially block exercise-induced physiologic stress indicators, analogous to the beneficial use of ice packs to reduce swelling following mild injuries (Sureda et al. 2008; Yfanti et al. 2010). In the end, the value of immunonutrition support (still to be determined) for athletes during periods of heavy exertion and competitive races will be evaluated by whether or not the athlete has improved recovery, lowered URTI, reduced muscle damage and soreness, and enhanced overall athletic performance.

2. Exercise-induced immune dysfunction and infection risk

4Each acute bout of heavy exertion leads to alterations in immunity and host pathogen defense, and to elevations in stress hormones, pro-inflammatory and anti-inflammatory cytokines, and reactive oxygen species (Gleeson, 2007; Nieman, 1997). Natural killer cell (NK cell) activity, various measures of T and B cell function, upper airway neutrophil function, salivary IgA concentration, granulocyte oxidative burst activity, skin delayed-type hypersensitivity response, and major histocompatibility complex (MHC) II expression in macrophages are suppressed for several hours to days during recovery from prolonged, intense endurance exercise. These immune changes occur in several compartments of the immune system and body including the skin, upper respiratory tract mucosal tissue, lung, blood, muscle, and peritoneal cavity. Many mechanisms appear to be involved, including exercise-induced changes in stress hormone and sympathetic nervous system stimulation, body temperature changes, increases in blood flow, dehydration, muscle damage, oxidative stress, and use of non-steroidal anti-inflammatory drugs including ibuprofen (Nieman, 2007, 2009). Transcriptome analysis of neutrophils and muscle tissue after heavy exertion indicates that upregulated groups of functionally related genes include those related to tissue damage, inflammation, chemokine signalling, leukocyte migration, immune and chaperone activation, and cell stress management (Neubauer et al. 2013, 2014).

5Intensive and sustained exercise can create an imbalance between reactive oxygen species and antioxidant defenses, increasing oxidative stress. One of the best oxidative stress biomarkers is F 2-isoprostanes (McAnulty et al. 2011). Inflammation also rises, and typical measures include C-reactive protein (CRP), and a variety of cytokines and chemokines, including IL-6, IL-10, IL-8, IL-1ra, granulocyte colony-stimulating factor (G-CSF), monocyte chemotactic protein 1 (MCP-1), macrophage inflammatory protein 1 beta (MIP-1β), macrophage migration inhibitory factor 1 (MIF-1), and tumor necrosis factor alpha (TNF-α) [Nieman, 1997, 2009]. The longer and more intense the exercise bout, the greater and more prolonged the inflammation response, with the highest levels measured in athletes with the greatest muscle damage after ultra-marathons (Nieman 2007, 2009; Nieman et al. 2012). Figure 1 summarizes plasma IL-6 levels following a variety of exercise workloads.

Figure 1: Plasma IL-6 response to varying exercise workloads. Data taken from a wide range of studies from Nieman’s lab.

Figure 1: Plasma IL-6 response to varying exercise workloads. Data taken from a wide range of studies from Nieman’s lab.

6Despite the large but transient acute changes in oxidative stress, inflammation, and immune function, chronic, resting immunity of athletes varies little from that of non-athletes (Nieman et al. 1995). Natural killer cell activity may be elevated in some types of athletes while neutrophil function is slightly suppressed. The adaptive immune system is largely unaffected by athletic endeavor. In general, the acute immune changes during and after each exercise bout appear to better explain URTI risk in athletes than the small alterations in chronic, resting immunity.

7During the “open window” of impaired immunity (which may last between 3 and 72 hours, depending on the immune measure), pathogen resistance is lowered, increasing the risk of subclinical and clinical infection (Gleeson, 2007; Murphy et al. 2009; Nieman, 2000). Epidemiological studies indicate that athletes engaging in marathon and ultra-marathon race events and/or very heavy training are at increased risk of URTI (Nieman et al. 1990; Peters et al. 1993; Nieman, 2000). Nearly 13% of marathoners reported URTI during the week following the Los Angeles Marathon race compared to 2.2% of control marathon runners (odds ratio, 5.9) [Nieman et al. 1990]. Forty per cent of the runners reported at least one URTI episode during the two-month winter period prior to the marathon race. Controlling for various confounders, it was determined that runners training more than 96 km/wk doubled their odds for sickness compared to those training less than 32 km/wk.

8Similar results have been reported by other investigators in both humans and rodents (Davis et al. 2004; Murphy et al. 2009; Scherr et al. 2012). One in four athletes reported URTI during the two-week period following the 160-km Western States Endurance Run (WSER), and this was linked to low post-race salivary IgA output levels but not the variation in change of inflammatory factors such as plasma cytokines (Nieman, 2009). A one-year retrospective study of 852 German athletes showed that URTI risk was highest in endurance athletes who also reported significant stress and sleep deprivation (Konig et al. 2000). Thus URTI risk may be exceptionally high when an athlete goes through repeated cycles of unusually heavy exertion, has been exposed to novel pathogens, and has experienced other stressors to the immune system including lack of sleep, severe mental stress, malnutrition, or weight loss.

3. Immunonutrition support for athletes

9Various nutritional agents have been tested for their capacity to attenuate immune changes, oxidative stress, and inflammation following intensive exercise (Gleeson, Nieman, & Pedersen, 2004; Nieman, 2008, 2010; Walsh et al. 2011). The list of efficacious immunonutrition support practices and products for athletes is small, but increasing attention is being directed to this field of scientific endeavor (see Table 1) [Walsh et al. 2011]. Results for most nutritional supplements tested as countermeasures to exercise-induced inflammation, oxidative stress, and immune dysfunction following heavy exertion have been disappointing, but some have impressive results such as carbohydrate, and fruit/vegetable extracts.

Table 1: Summary of rationale and findings for selected immunonutrition supplements.

Immunonutrition supplement

Rationale

Recommendation based on current evidence

Carbohydrate

Maintains blood glucose during exercise, lowers release of cortisol and epinephrine, and thus counters negative immune changes post-exercise

Recommended; up to 60 g per hour of heavy exertion helps dampen increases in leukocyte subset counts, and cytokines, but does not counter changes in T and NK cell function

Fruit and vegetable extracts rich in polyphenols and flavonoids (e.g. green tea extract, black currant and blueberry extract…)

Act as ibuprofen substitutes by attenuating exercise induced inflammation; decrease oxidative stress; mitigate ability of viruses to replicate in serum.

Recommended, but most research focused on countermeasure effects for oxidative stress and inflammation; more research needed on immune function

Quercetin (aglycone and glucoside forms such as isoquercetin)

In vitro studies show strong anti-inflammatory, antioxidative, and antipathogenic effects. Animal data indicate increase in mitochondrial biogenesis and endurance performance, reduction in mortality following pathogen exposure.

Recommended when mixed with other flavonoids and nutrients; human studies show reduction in illness rates during heavy training and a small, 3% influence on performance

Bovine colostrums

Mix of immune, growth, and hormonal factors improves immune function and the neuroendocrine system, and lowers illness risk

Mixed results, and more data needed

Probiotics

Improve intestinal microbial flora, and thereby enhance gut and systemic immune function

Mixed results, and more data needed

β-glucan

Receptors found on intestinal wall immune cells interact with β-glucan as it passes through, improving systemic innate immunity and thereby reducing infection rates

Mixed results: oat β-glucan was not effective in one human study; mushroom and yeast β-glucan may be more effective, but more data needed

Vitamin E

Quenches exercise-induced reactive oxygen species (ROS) and augments immunity

Not recommended; may be pro-oxidative and pro-inflammatory with heavy exertion

Vitamin C

Quenches ROS and augments immunity

Not recommended; not consistently different from placebo

Multiple vitamins and minerals

Work together to quench ROS and reduce inflammation

Not recommended; not different from placebo; balanced diet is sufficient

Glutamine

Important immune cell energy substrate that is lowered with prolonged exercise

Not recommended; body stores exceed exercise-lowering effects

N-3 PUFAs (fish oil)

Exerts anti-inflammatory and immune-regulatory effects post-exercise

Not recommended; no different from placebo

Herbal supplements (e.g. ginseng, echinacea)

Contain bioactive molecules that augment immunity and counter infection

Not recommended; humans studies do not show consistent support within an athletic context

3.1 Carbohydrate

10A series of studies dating back to the mid-1990s showed that ingestion of carbohydrate supplements before and/or during prolonged, intensive exercise (e.g. about 30 to 60 grams carbohydrate per hour) attenuated increases in blood neutrophil and monocyte counts, stress hormones and anti-inflammatory cytokines such as IL-6, IL-10, and IL-1ra (Figure 2) [Chen et al. 2008; Davison & Gleeson, 2005; Gleeson, 2007; Nieman, 1998; Nieman et al. 2006]. At the same time, however, little effect of carbohydrate ingestion was measured for exercise-induced decrements in salivary IgA output, and T cell and natural killer cell function. Thus, carbohydrate ingestion during heavy exercise emerged as an effective but partial countermeasure to immune dysfunction. Little is known regarding whether or not URTI rates are decreased when athletes remain carbohydrate-fed during endurance races. One study of marathon runners showed that illness rates following a competitive marathon tended to be lower in athletes ingesting carbohydrate compared to placebo beverages during the race (Nieman et al. 2001).

Figure 2 (A, B, C): Comparison of cortisol, epinephrine, and IL-6 responses to 2-hour exercise in cyclists consuming carbohydrate or placebo beverages (1 l/h, 6% carbohydrate) (data from Nieman et al. 2006). Interaction effects, all P<0.05.

Figure 2 (A, B, C): Comparison of cortisol, epinephrine, and IL-6 responses to 2-hour exercise in cyclists consuming carbohydrate or placebo beverages (1 l/h, 6% carbohydrate) (data from Nieman et al. 2006). Interaction effects, all P&lt;0.05.

11Carbohydrate may exert these effects through multiple mechanisms including an elevation in blood glucose and tissue glucose uptake leading to a diminished stress hormone output, decreased cytokine mRNA expression, reduced pro-inflammatory signals, and attenuated IL-6 release from the working muscle tissue (Gleeson, 2007; Nieman, 2008). A reduction in blood glucose levels during intense and prolonged exertion when athletes drink plain water increases hypothalamic-pituitary-adrenal activation, leading to a release of adrenocorticotrophic hormone and cortisol, growth hormone, and epinephrine. Stress hormones have an intimate link with genes that control cytokine production, and multiple cell types of the immune system.

12Some investigators report that carbohydrate supplementation during prolonged and intensive exercise interferes with the activation of signalling proteins that promote endurance training adaptation in skeletal muscle (Hawley & Morton, 2014). The literature is not consistent in this area, however (Akerstrom et al. 2009), and more research is needed to determine if athletes can train harder and adapt better with glucose ingestion, while experiencing reduced inflammation.

3.2 Antioxidants

13Multiple studies have focused on large-dose antioxidant supplements, and no consistent countermeasure benefit has been measured (Davison & Gleeson, 2006; Gleeson et al. 2004; Nieman et al. 2002, 2004). Heavy exertion causes oxidative stress, lipid peroxidation, and protein oxidation (McAnulty et al. 2011). Exercise-induced oxidative stress and immune dysfunction may be linked, but data support is largely lacking (Nieman, 2009). The proposed benefits of antioxidant supplementation in attenuating oxidative stress and immune dysfunction during exercise remain unsubstantiated (Nieman, 2008, 2009).

14For example, most well-designed studies do not support that vitamin C supplementation modulates immune responses following heavy exertion (Davison & Gleeson, 2005, 2006; Nieman et al. 2002). Studies of South African ultramarathon runners demonstrated that vitamin C (but not E or beta-carotene) supplementation (about 600 mg/day for three weeks) was related to fewer reports of URTI symptoms, but this has not been a consistent finding (Peters et al. 1993).

15Most studies also indicate that vitamin E supplementation is not an effective strategy for countering the inflammatory, oxidative stress, and immune response to intensive and prolonged exercise. Two months of vitamin E supplementation at a dose of 800 IU/day α-tocopherol did not counter increases in plasma cytokines, perturbations in other measures of immunity, or oxidative stress in triathletes competing in the Kona Triathlon World Championship race event (Nieman et al. 2004). Triathletes in the vitamin E compared to placebo group actually experienced greater lipid peroxidation and increases in plasma levels of several cytokines following the race event (see Figure 3).

Figure 3 (A, B): Plasma IL-6 and F 2-isoprostane responses in elite triathletes ingesting vitamin E or placebo (800 IU/day for 2 months) prior to the Kona Ironman World Championship (interaction effects, all P<0.06) (data from Nieman et al. 2004).

Figure 3 (A, B): Plasma IL-6 and F 2-isoprostane responses in elite triathletes ingesting vitamin E or placebo (800 IU/day for 2 months) prior to the Kona Ironman World Championship (interaction effects, all P&lt;0.06) (data from Nieman et al. 2004).

16In general, antioxidant supplementation for athletes during heavy exertion cannot be recommended based on current evidence. The majority of investigations have failed to show that ingestion of antioxidants such as vitamins E and C have meaningful effects on exercise-induced inflammation, muscle damage, increases in plasma cytokines, and immune perturbations. Large-dose vitamin E supplementation can actually exacerbate oxidative stress and inflammation during prolonged exercise in the heat. Other vitamins have not been investigated sufficiently, but one study conducted during a 16-week winter training period showed that low vitamin D status in endurance athletes was related to increased URTI prevalence and altered immune function (He et al. 2013).

3.3 Glutamine

17Glutamine supplements are not recommended because the best studies show no benefits when compared to placebo, perhaps due to abundant storage pools within the body that cannot be sufficiently depleted by exercise (Gleeson, 2007, 2008; Krzywkowski et al. 2001).

18Glutamine is an important fuel for lymphocytes and monocytes as supported by in vitro experiments showing that stepwise depletion of glutamine has a direct effect in lowering proliferation rates of T and B lymphocytes. Glutamine is an important component of currently available enteral immune-modulating formulas for patients that are critically ill or have experienced trauma or surgery.

19Reduced plasma glutamine levels have been observed in response to intense and prolonged exertion, and exercise immunologists have tested the value of glutamine ingestion as a countermeasure to exercise-induced immune dysfunction (Krzywkowski et al. 2001). The majority of studies, however, do not support that exercise-induced reductions in plasma glutamine levels cause impaired immunity and diminished host protection against viruses in athletes. For example, in a crossover, placebo-controlled study of eight men, glutamine supplementation abolished the post-exercise decrease in plasma glutamine concentration but still had no influence relative to placebo on exercise-induced decreases in T and natural killer cell function (Rohde, MacLean, & Pedersen, 1998).

20One problem with the glutamine hypothesis is that plasma concentrations following exercise do not decrease below threshold levels that are detrimental to lymphocyte function as demonstrated by in vitro experiments. In other words, even marathon-type exertion does not deplete the body of glutamine to a degree sufficient to negatively diminish lymphocyte function.

3.4 Beta-glucan

21The growing realization that extra vitamins, minerals, and glutamine do not provide countermeasure benefits for healthy and well-fed athletes during heavy training has shifted the focus to other types of nutritional components. β-glucans are polysaccharides found in the bran of oat and barley cereal grains, the cell wall of baker’s yeast, certain types of fungi, and many kinds of mushrooms. Rodent studies indicate that oat β-glucan supplements offset the increased risk of infection associated with exercise stress through augmentation of macrophage and neutrophil function, but these results were not upheld in a study of human cyclists (Murphy et al. 2009; Nieman et al. 2008). Some studies with athletes suggest that mushroom β-glucan may exert beneficial effects (Bergendiova, Tibenska, & Majtan, 2011).

22A wide variety of β-glucans exist that vary in macromolecular structure, solubility, molecular weight, and biological activity. Most β-glucans from yeast, fungi, and mushrooms consist of D-glucose linked in the β-(1→3) position with β-(1→6) linkage with glucose side branches. Oat and barley β-glucans have a mixed β-(1→3) and β-(1→4) linkage. Humans lack small intestine enzymes to separate the glucose molecules of β-glucans, and they pass to the large intestine undigested. Oat and barley β-glucan is a fermentable, viscous fibre that decreases LDL-cholesterol by partially blocking enterohepatic recirculation of cholesterol and bile acids. Consumption of oat and barley products with at least 3 g of β-glucan soluble fibre per day is effective in lowering blood total and LDL cholesterol.

23Receptors of β-glucans have been identified on a wide variety of cell types including macrophages, dendritic cells, natural killer cells, neutrophils, some types of T cells, epithelial cells, vascular endothelial cells, and fibroblasts (Murphy et al. 2009; Murphy, Davis, & Carmichael, 2010). Thus despite the lack of enzymatic breakdown in the small intestine, the widespread distribution of β-glucan receptors throughout the body suggests some degree or unique method of absorption. Studies with rodents indicate that the bioavailability of β-glucans is about 4 to 5%, and that soluble glucans can translocate from the gastrointestinal (GI) tract to the systemic circulation. Although the exact pathway is still undetermined, current evidence suggests that β-glucans interact with a variety of GI cells including mucosal dendritic and epithelial cells. GI mucosal dendritic cells may sample or interact with soluble β-glucans via projections across the epithelium and then migrate via afferent lymphatics to the mesenteric lymph nodes where immune modulation is initiated. GI macrophages may also engulf β-glucans, shuttle them to reticuloendothelial tissues and the bone marrow, and then degrade and secrete small β-glucan fragments that bind to receptors on bone marrow granulocytes. A subpopulation of intestinal epithelial cells and gut-associated lymphoid tissue (GALT) cells appears capable of actively binding and internalizing β-glucans, which then leads to small but significant increase in blood β-glucan levels.

24Growing evidence from studies conducted with rodents, fish, poultry, and swine indicates that oral β-glucan ingestion stimulates innate immune defenses and antitumor responses, and increases resistance to a wide variety of infections (Murphy et al. 2009; Murphy, Davis, & Carmichael, 2010). β-glucans may activate macrophages and neutrophils directly, stimulating their phagocytic, cytotoxic, and antimicrobial activities through several types of cellular receptors including Dectin-1, lactosylceramide, Toll-like receptors 2 and 6, scavenger receptors, and the type 3 complement receptor (CR3).

25Rodent studies indicate that oat β-glucan supplements offset the increased risk of infection associated with exercise stress through augmentation of macrophage and neutrophil function (Davis, et al. 2004; Murphy et al. 2009; Murphy, Davis, & Carmichael, 2010). In one study with mice, ingestion of oat β-glucan for 10 days before intranasal inoculation of herpes simplex virus-1 (HSV-1) countered the increase in morbidity and mortality, and the decrease in macrophage antiviral resistance, following exhaustive 140-minute exercise bouts over three consecutive days (Davis, et al. 2004). In a follow-up study, these investigators showed that ten days of oat β-glucan by mice blocked the increased susceptibility to morbidity and mortality following HSV-1 inoculation and three consecutive days of running to volitional fatigue on rodent treadmills (Murphy et al. 2009). Depletion of lung macrophages using clodronate negated the beneficial effects of β-glucan, indicating that these immune cells are at least partially involved.

26A similar study with human athletes, however, failed to confirm these results (Nieman et al. 2008). Trained male cyclists were randomized to β-glucan or placebo groups and under double-blind procedures received oat β-glucan (5.6 grams/day) or placebo for two weeks prior to and during a 3-day period in which subjects cycled for 3 h/day at high intensity. URTI symptoms were monitored for two weeks before and two weeks after the 3-day period of intensified exercise. Blood samples were taken before and after 14 days of β-glucan supplementation (chronic immunity) and immediately after the last bout of exercise and 14-hours of recovery (acute immunity), and were assayed for a wide variety of immune function measures including natural killer and T cells, granulocytes, and plasma cytokine levels. None of these immune measures differed between β-glucan and placebo groups, and URTI incidence did not differ during the 31 days of monitoring. These data indicate that oat β-glucan supplementation does not alter chronic immune function or acute exercise-induced immune perturbations during a period of intensified exercise training.

27A three-month supplementation study with 50 athletes indicated that oyster mushroom β-glucan reduced URTI incidence and had a favourable effect on phagocytosis relative to placebo (Bergendiova, Tibenska, & Majtan, 2011). Although mechanisms were not explored in this study, the β-(1,3/1,6)-D-glucan from the Pleurotus ostreatus (oyster mushroom) appears to travel through the digestive system and stimulate GALT immune cells with surface specific receptors Dectin-1 and CR3 (and is more effective than beta-(1,3/1,4)-D-glucan). Other studies with baker’s yeast β-(1,3/1,6)-Dglucan indicate reductions in URTI rates among marathon runners and those participating in intense exercise stress, and improvement in mucosal immunity postexercise (McFarlin et al. 2013). In general, the data on β-(1,3/1,6)-D-glucan supplementation among athletes are interesting, and future research will help sort out the optimal dosing regimen and potential adjuvants.

3.5 Other advanced supplements

28In vitro/cell culture, animal, and epidemiological research indicate that advanced supplements such as probiotics, bovine colostrum, flavonoids and polyphenols such as quercetin, resveratrol, curcumin, and epigallicatechin-3-gallate (EGCG), N-3 polyunsaturated fatty acids (N-3 PUFAs or fish oil), herbal supplements, and unique plant extracts (e.g. green tea extract, blackcurrant extract, tomato extract with lycopene, anthocyanin-rich extract from bilberry, polyphenol-rich pomegranate fruit extract) have potential benefits for athletes (Bakker et al. 2010; Lyall et al. 2009; Nieman, 2010; Nieman et al. 2009b, 2010a).

29Human research testing efficacy in athletes has just begun for many types of advanced nutritional supplements. Limited data from athletes are non-supportive or mixed for use of N-3 PUFAs (Nieman et al. 2009b), probiotics (West et al. 2009; Gleeson et al. 2012), bovine colostrums (Carol, 2011; Davison & Diment, 2010; Shing et al. 2009), ginseng (Senchina et al. 2009), or echinacea (Senchina et al. 2009). (See Table 1 for a summary).

30N-3 PUFAs, for example, decrease the production of inflammatory eicosanoids, cytokines, and reactive oxygen species, and have immunomodulatory activities. Some investigators promote that the majority of athletes need 1 to 2 g marine n-3 PUFAs per day to counter excessive oxygen radical formation, inflammation, and trauma from high-intensity exercise and the high n-6 PUFA levels of the Western diet. However, a double-blinded, placebo-controlled study with trained cyclists demonstrated that six weeks' supplementation with 2.4 g/day eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) did not alter measures of inflammation and immunity before and after three days of prolonged and intensive exercise (Nieman et al. 2009b). Other studies also indicate that DHA supplementation does not influence neutrophil responses to acute or chronic exercise training (Martorell et al. 2014).

31Bovine colostrum includes immune, growth and antimicrobial factors, and supplementation theoretically may promote exercise performance and help maintain immune function during intense exercise (Shing, Hunter, & Stevenson, 2009). Studies are mixed, however, and the optimal dosing paradigm is still being explored (Jones et al. 2014). Carol et al. (2011) had subjects consume 25 g/d freeze-dried bovine colostrum for ten days, but found no influence relative to skim milk powder placebo on exercise-induced immune changes.

32An evolving hypothesis is that the immune system is so diverse that a mixture of these advanced supplements within a carbohydrate beverage will probably perform better than one supplement by itself (Bakker et al. 2010; Nieman et al. 2009a). In other words, the “pharma” approach of using large doses of a single nutritional component is not as effective as a “cocktail” strategy for nutritional supplements. A secondary hypothesis is that the primary immune target of nutrient supplements should be the non-specific, innate arm of the immune system to enhance immunosurveillance against a wide variety of pathogens in athletes. If the nutritional supplement improves natural killer cell, macrophage, and granulocyte function before and/or after heavy exertion, then risk of infection is more effectively countered than when the target is the slower-moving adaptive immune components (Nieman, 2008; Nieman et al. 2007, 2009a).

3.6 Flavonoids

33Phytochemicals are chemicals produced by plants, and include tannins, lignins, and flavonoids. The largest and best studied polyphenols are the flavonoids, with more than 6000 identified and classified into at least six subgroups: flavonols, flavones, flavanones, flavanols (and their oligomers, proanthocyanidins), anthocyanidins, and isoflavonoids. Flavonoids are widely distributed in plants and function as plant pigments, signalling molecules, and defenders against infection and injury.

34Many flavonoids possess strong anti-inflammatory, anti-viral, antioxidant, anti-obesity, and anticarcinogenic properties when studied in vitro using large doses of the purified form. Inflammation and oxidative stress are key mechanisms in the pathogenesis of certain disease states, supporting the proposed strategy of increased flavonoid intake for prevention of cancer, diabetes mellitus, and cardiovascular disease. However, results from randomized, double-blinded studies in humans with large doses of purified flavonoids such as quercetin have been disappointing (Nieman, 2010). Flavonoids vary widely in bioavailability, and most are poorly absorbed, undergo active efflux and are extensively conjugated and metabolically transformed, all of which can affect their bioactive capacities (Harwood, et al. 2007). Despite low bioavailability of the parent flavonoid, some of the in vivo metabolites may accumulate in tissues and produce bioactive influences, but conclusive human data are lacking. For example, animal data indicate that quercetin metabolites accumulate in the vascular tissue and there act as complementary antioxidants, with plasma albumin facilitating the translocation of quercetin metabolites to the vascular target.

35There is a growing realization that bioactive influences of individual flavonoids are potentiated when mixed with other flavonoids (e.g. the flavonol quercetin with the flavanol epigallocatechin 3-gallate or EGCG) or included in a cocktail or extract of other polyphenols and nutrients (Lila, 2007). Two or more flavonoids ingested together may increase bioavailability and decrease elimination via competitive inhibition of glucuronide and sulfate conjugation in both the intestine and liver, and by inhibiting efflux transporters such as P-glycoprotein, breast cancer resistance protein (BCRP), and multidrug resistance protein 2 (MRP2).

36The health-protective effects of plant foods are not produced by a single component but rather complex mixtures of interacting molecules. The polyphenols and natural components provide a multifaceted defensive strategy for both plants and humans. Thus the “pharma” approach of using large doses of a single bioactive molecule is seldom successful in the application of nutrition to human health and performance. Additionally, a metabolomics or nutrigenomics approach is needed to improve the capacity of investigators to capture the complex and subtle influences of flavonoid supplements or flavonoid-rich extracts, foods and beverages on whole-body metabolism and physiology (Bakker et al. 2010).

37The physiologic effects of dietary polyphenols such as quercetin, EGCG, curcumin, lycopene, resveratrol, luteolin, and tiliroside are of great current interest to exercise immunologists due to their antioxidative, anti-inflammatory, antipathogenic, cardioprotective, anticarcinogenic, and mitochondrial stimulatory activities (Nieman, 2008, 2010).

38Flavonoids such as quercetin, EGCG, and isoflavones, or flavonoid-rich plant extracts are being tested by an increasing number of investigative teams as performance aids and countermeasures to exercise-induced inflammation, delayed onset of muscle soreness (DOMS), oxidative stress, immune dysfunction, and URTI (Nieman, et al. 2010a). Most studies have focused on the ability of flavonoid-rich tea, fruit, and vegetable extracts to counter oxidative stress, and the majority indicates an effective response. The second most common outcome measure is related to inflammation and DOMS, and again, most studies support protective effects when flavonoid mixtures or plant extracts are ingested prior to demanding bouts of exercise. Results are mixed for performance outcomes, and few studies have included immune and URTI measures. In one large study of 277 marathon runners, 3-weeks pre-race and 2-weeks post-race ingestion of nonalcoholic beer with polyphenols was linked to a significant reduction in URTI incidence and post-race inflammation (Scherr et al. 2012).

39A large proportion of ingested plant polyphenols reach the colon, and there is a growing realization that the metabolites created from colonic bacterial degradation can be reabsorbed and exert bioactive effects, especially following exercise when gut permeability is increased (Nieman et al. 2013). Future research should focus on the gutderived phenolic signature measured following polyphenolic supplementation and exercise, especially at the tissue level.

40For any particular flavonoid or plant extract studied within an exercise context, few papers are available, and research designs vary widely in regards to the supplementation dose and regimen, the mode of exercise stress, and outcome measures. The flavonoid supplementation period varies from 15 minutes to 60 days prior to an exercise challenge, with most studies clustered between 7 and 21 days. Nonetheless, the data in general support that flavonoid-rich plant extracts and unique flavonoid-nutrient mixtures (e.g. quercetin with green tea extract and fish oil, or isoflavones with lycopene) help counter exercise-induced oxidative stress and inflammation/DOMS. The serum of athletes using blueberry and green tea polyphenol supplements compared to placebo mitigates the tendency of viruses to replicate following intensified training periods (Ahmed et al. 2014) (Figure 4).

Figure 4: Viral replication responses in runners ingesting a blueberry and green tea supplement for two weeks prior to engaging in a three-day period of intensified exercise (2.5 h running per day). These data provide evidence that the serum of endurance athletes ingesting polyphenol supplements for two weeks contains antiviral properties that allow cells to resist virus infections following strenuous exercise.

Figure 4: Viral replication responses in runners ingesting a blueberry and green tea supplement for two weeks prior to engaging in a three-day period of intensified exercise (2.5 h running per day). These data provide evidence that the serum of endurance athletes ingesting polyphenol supplements for two weeks contains antiviral properties that allow cells to resist virus infections following strenuous exercise.

41More exercise-related research has been conducted with quercetin than any other flavonoid (Nieman, 2010; Nieman et al. 2007, 2009, 2010a, 2010b). In one of the earliest studies with exercise-stressed cyclists, supplementation with pure quercetin (1000 mg/day) over a five-week period reduced illness rates but did not counter post-exercise inflammation, oxidative stress, or immune dysfunction (Nieman et al. 2007). In a follow-up study using a similar design, quercetin supplementation combined with green tea extract, isoquercetin, and fish oil did cause a sizeable reduction in exerciseinduced inflammation and oxidative stress, with chronic augmentation of innate immune function (Nieman et al. 2009a) [see Figure 5]. Quercetin’s role as a performance aid has been tested by several research teams with mixed results, but a recent meta-analysis indicates a small but significant 3% performance enhancement (Kessler, Millard-Stafford, & Warren, 2011; Nieman et al. 2010b). Animal studies support a role for quercetin as an exercise mimetic for mitochondrial biogenesis, and one study with untrained human subjects indicated a modest enhancement in skeletal muscle mitochondrial density and endurance performance, but far below what was reported in mice (Nieman et al. 2010b).

Figure 5: C-reactive protein before and after two weeks supplementation with a mixture of quercetin, isoquercetin, EGCG-enriched green tea extract, fish oil, vitamin C, and niacin, and then immediately after and 14-hours after 3-days of intensified exercise (3 h/day, 57% Wattsmax) (data from Nieman et al. 2009).

Figure 5: C-reactive protein before and after two weeks supplementation with a mixture of quercetin, isoquercetin, EGCG-enriched green tea extract, fish oil, vitamin C, and niacin, and then immediately after and 14-hours after 3-days of intensified exercise (3 h/day, 57% Wattsmax) (data from Nieman et al. 2009).

4. Conclusion and future research

42Athletes must train hard for competition and are interested in strategies to keep their immune systems robust and illness rates low despite the physiologic stress they experience. The ultimate goal is to provide athletes with a sports drink or supplement bar containing carbohydrate and a cocktail of advanced supplements that will lower infection risk, exert significant and measurable influences on their innate immune systems, and attenuate exercise-induced oxidative stress and inflammation. The athlete can combine this strategy with other approaches that help maintain immunity and health.

43Carbohydrate beverage supplementation (˜60 g sugar/hour) during prolonged and intensive exercise has a strong effect in lowering plasma levels of cortisol, epinephrine and inflammatory immune responses including blood neutrophil and monocyte counts, and cytokines. Flavonoid-rich extracts when consumed just before or chronically for days or weeks before heavy exertion partially counter post-exercise inflammation and oxidative stress, and help counter the ability of viruses to replicate post-exercise. Research is needed to better define optimal dosing regimens and whether unique flavonoid mixtures that include several of the most bioactive flavonoids across different subgroups amplify these influences, while also bolstering immunity and operating as exercise mimetics for mitochondrial biogenesis.

44Antioxidant, N-3 PUFAs, and glutamine supplements do not counter exercise-induced immune dysfunction, and vitamin E may actually compound the oxidative stress and inflammation experienced by the endurance athlete. More research is needed for mushroom and yeast β-glucan, probiotics, and bovine colostrum. Additional research will broaden our understanding of the effects of these advanced supplements and others in providing immune benefits to athletes during physiologic stress.

Bibliographie

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Table des illustrations

Titre Figure 1: Plasma IL-6 response to varying exercise workloads. Data taken from a wide range of studies from Nieman’s lab.
URL http://books.openedition.org/insep/docannexe/image/1823/img-1.jpg
Fichier image/jpeg, 68k
Titre Figure 2 (A, B, C): Comparison of cortisol, epinephrine, and IL-6 responses to 2-hour exercise in cyclists consuming carbohydrate or placebo beverages (1 l/h, 6% carbohydrate) (data from Nieman et al. 2006). Interaction effects, all P<0.05.
URL http://books.openedition.org/insep/docannexe/image/1823/img-2.jpg
Fichier image/jpeg, 172k
Titre Figure 3 (A, B): Plasma IL-6 and F 2-isoprostane responses in elite triathletes ingesting vitamin E or placebo (800 IU/day for 2 months) prior to the Kona Ironman World Championship (interaction effects, all P<0.06) (data from Nieman et al. 2004).
URL http://books.openedition.org/insep/docannexe/image/1823/img-3.jpg
Fichier image/jpeg, 36k
Titre Figure 4: Viral replication responses in runners ingesting a blueberry and green tea supplement for two weeks prior to engaging in a three-day period of intensified exercise (2.5 h running per day). These data provide evidence that the serum of endurance athletes ingesting polyphenol supplements for two weeks contains antiviral properties that allow cells to resist virus infections following strenuous exercise.
URL http://books.openedition.org/insep/docannexe/image/1823/img-4.jpg
Fichier image/jpeg, 28k
Titre Figure 5: C-reactive protein before and after two weeks supplementation with a mixture of quercetin, isoquercetin, EGCG-enriched green tea extract, fish oil, vitamin C, and niacin, and then immediately after and 14-hours after 3-days of intensified exercise (3 h/day, 57% Wattsmax) (data from Nieman et al. 2009).
URL http://books.openedition.org/insep/docannexe/image/1823/img-5.jpg
Fichier image/jpeg, 28k

Auteur

PhD. Human Performance Laboratory, Appalachian State University and the North Carolina Research Campus, 600 Laureate Way, Kannapolis, NC 28081; Phone: 828-773-0056; E-mail: niemandc@appstate.edu

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