Peri-Workout BCAA + Glutamine + Citrulline Consumption Blunts Muscle & Fat Loss Compared to Powerade Placebo

"Shed the fat, keep the muscle!" That's a promise you will find not literally, but analogously in every ad for BCAAs, but do they actually do that? Help you shed fat and retain muscle? Scientific prove to support this claim is, as of yet, missing.

With BCAAs it is just as it is with 99.9% of the supplements: Ads and product labels are full of scientifically unproven claims. One of these unproven claims is that the consumption of branched-chain amino acids would protect you from losing muscle while you're dieting ... the problem with this notion is - as sound as it may seem in view of the mTOR promoting effects of leucine, there's no study which would prove that guzzling BCAAs all day will in promote fat and blunt lean mass losses when you're cutting.... or I should say "as of now, there was no study...", right? After all, there's this new study by Dudgeon et al.'s the abstract of which tells us that "BCAA supplementation in trained individuals performing resistance training while on a hypocaloric diet can maintain lean mass and preserve skeletal muscle performance while losing fat mass" (Dudgeon. 2015).

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As we are going to see after taking a look at the design and results of Dudgeon's single-blind study in seventeen resistance-trained males (21–28 years of age) on hypocaloric diets, this is yet a potentially misleading conclusion. Not because it was wrong, but rather because it omits an observation that could be of paramount importance to dieters who have the free choice between the two treatments, the subjects of the study were randomly assigned to, namely...

• 14g of Xtend (BCAA) before after workouts or
• 14 g Powerade (CHO) before and after workouts

The supplements were consumed for a total study time of 8 weeks during which all subjects trained four times per week according to a standardized workout program and consumed a diet that was programmed (but not controlled) to contain roughly 35% less energy than the subjects required on workout days and approximately 10% less energy than required on off-days.

In the strict sense, this is actually no "BCAA study": Some of you may already have realized that the "BCAA supplement" the scientists used, i.e. Scivation XTend, is not really a "BCAA only" supplement. Next to only 7 grams of BCAAs per 14g of powder the subjects ingested before and after the workout, it also contains 1 g citrulline and 2.5 g glutamine and obviously a hell lot of flavorings, fillers and what not. Now, while the latter are not of any importance, both of the former have been heralded as muscle protectors, as well, with citrulline probably having the more convincing scientific data to back it up (it appears to act similar to leucine, by the way | Moinard. 2007; Faure. 2012; Ventura. 2013) outside of scenarios with extremely high glucocorticoid levels where glutamine unquestionably helps (Hickson. 1995 & 1997; Salehian. 2006). It is thus in my humble opinion at least highly imprecise to conclude that the provision of 2x7g of BCAA ameliorated the the fat to muscle loss ratio during the 8-week study.

Now you may be rightly asking yourselves why I am so vague with respect to the energy deficit. Well, everything we learn from the full text of the study is that all subjects were "provided an individualized caloric restricted diet based on individual data (body mass, body composition, resting metabolic rate, etc.)" (Dudgeon. 2015) - a diet the scientists describe as follows:

Table 1: W/ the Harris-Benedict equation you calculate the basal metabolic rate and multiply it with a factor (multiplier) that describes your activity level best to arrive at the "real" estimated energy requirements.

"The caloric-restricted diet was designed as an 8 week “cut diet” for reducing body fat, and used a modified carbohydrate-restricted diet approach (percent of total calories for workout days were 30 % carbohydrates, 35 % protein and 35 % fat and for off days were 25 % carbohydrates, 40 % protein and 35 % fat). Each individual’s daily caloric and macronutrient intake was determined using the Harris Benedict formula with an activity factor of 1.35 (lightly active individual engaging in light exercise 1–3 days/week) for workout days and 1.125 (sedentary individual) for off days" (Dudgeon. 2015).

Since the Harris-Benedict formula is only a really rough estimate of how much energy you actually need, my previous estimations of the energy deficit are as "accurate" as I can possibly be. The 1604kcal that are printed in red bold letters on top of the exemplary meal plan in Figure 2, however, suggest that the deficit on the off days was significantly larger. After all, the subjects' mean weight was >80kg and their daily energy requirements should thus be at least 2,000kcal - even on off days (and the table in which the macronutrient composition is listed actually says that the mean intake was 2046 and 2264kcal/day for the BCAA and CHO group respectively).

Table 2: Sample dietary card for a subject during an off, non-workout, day (Dudgeon. 2015).

In view of the fact that the response I got from the authors to an email in which I asked about the exact kcal deficit only referred me to the previously cited passage about the activity factors, I guess it is futile to further speculate about the energy deficit, of which I would still like to add that it was probably higher in the heavier and taller BCAA group. Why? Well, the BCAA group had plans with 2456 and 2046 kcal on workout and off days, the CHO group on the other hand were fed 2717 and 2264 kcal... Whatever, let's get to the more relevant, but not less confusing changes in body weight, lean mass and fat mass the researchers report for the BCAA and CHO groups:

Figure 1: Pre and post absolute mean body weight, body fat and lean body mass values before and after the 8-week intervention; * p < 0.05 for the difference within groups (no difference between groups | Dudgeon. 2015)

-0.1 kg and -2.3 kg of body weight, +0.4 kg and -0.9 kg of lean mass and 0.6 kg and 1.4 kg fat mass in the BCAA and CHO groups respectively - that's in line with the previously cited conclusion. The BCAA supplement blunted the small loss of lean mass in the CHO group, but if we look at the complete dataset, a somewhat different image emerges; one in which the two classic markers of body composition, namely the relative amount of body fat (aka "body fat percentage") and the lean mass as percentage of the total mass changed in a way that favors CHO over BCAA supplements:

Figure 2: Pre vs. post values for body fat % and lean mass %, the two parameters you would classically use to assess body composition (instead of absolute lean and fat mass); pre-to-post change on top of the post-bars (Dudgeon. 2015).

Now, I am not saying that the consumption of the BCAA (+citrulline + glutamine) supplement did not blunt the loss of lean mass - it obviously did. What I want you to keep in mind, though, is the fact that the consumption of 14g of BCAAs before and after workouts appears to suffocated any dieting efforts - after all, the subjects lost a practically irrelevant (and for whatever reason allegedly statistical significant) amount of 600g body fat; that's in contrast to the 1.4 kg of fat mass the subjects in the control group lost; and that's a practically relevant insight, even if this fat loss was allegedly statistically non-significant, because  it implies that BCAAs practically blunt fat loss.

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So what do we make of this study? Well, first of all, I would like to come back to something fundamental: This is yet another BCCA study that did not make the practically most relevant comparison of BCAAs and cheap (whey) protein protein supplements, in which BCAAs have hitherto always failed. In my humble opinion that's a problem, after all having a carbohydrate supplement as control in a dieting study is nice, but eventually not relevant for the average trainee who is probably not really considering extra-carbs when he's dieting.  What a real trainee would have been interested in, is whether BCAAs can prevent muscle catabolism to a significantly greater degree than the cheap whey protein he's using anyway...

... and maybe, whether the latter has a similar negative effect on fat loss as the BCAAs in the study at hand - which leads me to the actual take home message of the study, which is, as usually, not as straight forward as the conclusion of the abstract suggested. When all is said and done, the study at hand does after all suggest that someone who is approaching the single-digit body-fat zone, where every gram of muscle that is not lost counts, could benefit from the apparent lean mass protective effects of BCAA the scientists observed in the study at hand. It does yet also indicate that someone who's "making weight" for a competition should take a second look at the data in Figure 1 + 2 and acknowledge that taking a BCAA supplement may be the reason he will fail to achieve his weight loss goal. You don't believe that? Well, let's do some scientifically not exactly kosher extrapolations: If you manage to lose 10 kg in 10 weeks without BCAAs, for example, the data from the study at hand suggests that your weight loss "on BCAAs" over the course of those 10 weeks would be as meager as 434 grams ... whether that's in fact the case (I doubt it ;-) will have to be studied in future studies, just like the effect of BCAAs, citrulline and glutamine, alone and whether using your regular whey protein before and after the workout wouldn't have the exact same, or even better effects | Comment on Facebook!

References:

• Dudgeon, WD; Page Kelly, E; Scheett TP. "In a single-blind, matched group design: branched-chain amino acid supplementation and resistance training maintains lean body mass during a caloric restricted diet." Journal of the International Society of Sports Nutrition  (2016) 13:1.
• Faure, Cécile, et al. "Leucine and citrulline modulate muscle function in malnourished aged rats." Amino acids 42.4 (2012): 1425-1433.
• Moinard, Christophe, and Luc Cynober. "Citrulline: a new player in the control of nitrogen homeostasis." The Journal of nutrition 137.6 (2007): 1621S-1625S.
• Hickson, R. C., S. M. Czerwinski, and L. E. Wegrzyn. "Glutamine prevents downregulation of myosin heavy chain synthesis and muscle atrophy from glucocorticoids." American Journal of Physiology-Endocrinology and Metabolism 268.4 (1995): E730-E734.
• Hickson, Robert C., et al. "Protective effect of glutamine from glucocorticoid-induced muscle atrophy occurs without alterations in circulating insulin-like growth factor (IGF)-I and IGF-binding protein levels." Experimental Biology and Medicine 216.1 (1997): 65-71.
• Salehian, Behrouz, et al. "The effect of glutamine on prevention of glucocorticoid-induced skeletal muscle atrophy is associated with myostatin suppression." Metabolism 55.9 (2006): 1239-1247.
• Ventura, G., et al. "Effect of citrulline on muscle functions during moderate dietary restriction in healthy adult rats." Amino acids 45.5 (2013): 1123-1131.

Glutamine, the Anti-Obesity Gut-Tenant Modulator for the Obese and Potential Anti-Ammonia Benefits for Athletes

The health impact of the vast gene pool in our guts has long been underrated.

You will probably remember my previous articles on glutamine - articles that draw an overall very mixed picture of the usefulness of this gluconeogenic amino acid.

If you have been around "forever", you may yet also remember that there's one thing glutamine appears to do that no-one actually has on the radar, when he or she's browsing the storefronts of his or her favorite supplement vendor: Improvements in insulin sensitivity as those I've written about for the first time in 2010 and downstream anti-diabesity effects as they've been demonstrated more recently by Mansour et al. (2014) in a quite impressive 6 week study, in the course of which "3x30g/day Markedly Improved Cardiovascular Risk Factors & Body Comp in 6 Weeks" (reread the full article).

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Now, back in the day, I was not really able to explain how "exactly", the  most abundant amino acid in the body was able to induce significant decreases in body fat even though the subjects were not dieting. With the publication of the results of a recent study from the State University of Campinas in Brazil, however, the evidence that these benefits may be a consequence of the modulatory effects of glutamine on the (pro-inflammatory) microbiome of obese individiuals are accumulating.

In said pilot study, Alessandra Zanin Zambom de Souza and her colleagues aimed to "determine whether oral supplementation with L-glutamine (GLN) modifies the gut microbiota composition in overweight and obese adults" (de Souza. 2015).

"In this double-blind, 14-d study, participants [thirty-three overweight and obese adults, ages between 23 and 59 y and body mass index between 25.03 and 47.12 kg/m²] were randomly divided into two groups: glutamine (GLN) and alanine (ALA). We used alanine as control to give the volunteers the same amount of calories. Participants received a kit containing small packs with 15 g of amino acid (GLN or ALA) each, with varying artificial flavors, to be diluted in 200 mL of water at the time of intake. Participants were instructed to take two packs at any convenient time of the day, totaling 30 g/d of amino acid, while maintaining their usual diets and physical activities" (de Souza. 2015).

After 14 d of supplementation, adults in the GLN group exhibited statistically significant differences in the Firmicutes and Actinobacteria phyla compared with those in the ALA group.

Figure 1: Gut microbiota profile. Data were collected before and after 14 d of supplementation with ALA: alanine (n = 12) or GLN: glutamine (n = 21); Relative percentage of major phyla found in the gut microbiota of participants in (A) ALA group and in (B) GLN group at baseline and day 14. Major phyla found were Actinobacteria (black), Bacteroidetes (dark gray), Firmicutes (gray), Proteobacteria (light gray), and others (white | de Souza. 2015).

At first, this change may appear to be pretty arbitrary, but in conjunction with the previously cited results of the Mansour study (reread it) and the existing evidence suggesting that the ratio of Firmicutes to Bacteroidetes, a good biomarker for obesity (Ley. 2005 & 2006 | Ley et al. (2006), for example found a linear increase in bacteriode abundance with weight loss), the observed decrease in the F:B ratio from from 0.85 to 0.57 in the glutamine group may in fact provide a mechanistic explanation for the previously observed medium-term benefits of high-dose glutamine supplementation in the obese. Benefits that may be augmented by the recently proven and probably mechanistically related ability of glutamine to attenuate oxidative stress and the proinflammatory responses as they would occur, when endotoxins from the gut make it into your blood stream (Cruzat. 2014) - something you may, by the way, also expect to see if you are a green or black tea connoisseur of which Henning et al. have recently been able to show that it induces similarly positive changes in the firmicute to bacteroides ratio as glutamine (Henning. 2015).

Figure 2: Rating of perceived exertion (RPE) versus CSF ammonia following exercise with (open symbols) or without glucose supplementation (grey/red symbols) RPE values represent the individual scores during the last 15 min of the prolonged cycle trial (Nybo. 2005).

And what about ahletes? In view of the fact that studies indicate that exercise can keep the number of potentially proinflammatory gut tenants like Dialister, Dorea, Pseudobutyrivibrio, and Veillonella (all firmicutes) at bay, anyway (Choi. 2013), you may argue that this is not that relevant for athletes. The proven ability of glutamine to counter the fatiguing exercise-induced increase in ammonia (Bassini-Cameron. 2008), however, makes glutamine a potential valuable dietary supplement specifically for those athletes who consume a high protein diet that may - as a consequence of the use of protein as energy source - lead to potentially performance decreasing increases in ammonia (Nybo. 2005) which also passes the blood brain barrier and "might possibly result in the observable central nervous system symptoms of dysfunction which accompany exhaustion such as ataxia, mental confusion and syncope [partial loss of consciousness]" (Banister. 1983).

In that, it is yet allegedly debatable, whether other amino acids like citrulline which has been shown to significantly improve the clearance of ammonia from the blood stream (Takeda. 2011) wouldn't be the better choice in terms of their ability to block the accumulation of ammonio during workouts. Reductions in gut permeability or reductions of the number of pro-inflammatory Firmicute and Actinobacteria, however, have not been reported for citrulline, which is why one may have to reconsider the lack of convincing evidence of acute beneficial effects of glutamine supplementation on exercise performance (Gleeson. 2008) in view of the previously shown ability of glutamine to serve as alternative or adjunct to glucose during longer workouts and the more recent evidence of its benefits on the digestive tract | Comment on Facebook! 

References:

• Banister, E. W., et al. "The time course of ammonia and lactate accumulation in blood during bicycle exercise." European Journal of Applied Physiology and Occupational Physiology 51.2 (1983): 195-202.
• Bassini-Cameron, Adriana, et al. "Glutamine protects against increases in blood ammonia in football players in an exercise intensity-dependent way." British journal of sports medicine 42.4 (2008): 260-266.
• Choi, Jeong June, et al. "Exercise attenuates PCB-induced changes in the mouse gut microbiome." Environmental health perspectives 121.6 (2013): 725-730.
• Cruzat, Vinicius Fernandes, et al. "Oral free and dipeptide forms of glutamine supplementation attenuate oxidative stress and inflammation induced by endotoxemia." Nutrition 30.5 (2014): 602-611.
• de Souza, Alessandra Zanin Zambom, et al. "Oral Supplementation with L-Glutamine Alters Gut Microbiota of Obese and Overweight Human Adults: A Pilot Study." Nutrition (2015).
• Gleeson, Michael. "Dosing and efficacy of glutamine supplementation in human exercise and sport training." The Journal of nutrition 138.10 (2008): 2045S-2049S.
• Henning, Susanne, et al. "Effect of Green and Black Tea Extracts on Intestinal Microbiota and Body Composition in Mice Fed a High Fat/High Sucrose/Western Diet." The FASEB Journal 29.1 Supplement (2015): 924-27.
• Ley, Ruth E., et al. "Obesity alters gut microbial ecology." Proceedings of the National Academy of Sciences of the United States of America 102.31 (2005): 11070-11075.
• Ley, Ruth E., et al. "Microbial ecology: human gut microbes associated with obesity." Nature 444.7122 (2006): 1022-1023.
• Mansour, Asieh, et al. "Effect of glutamine supplementation on cardiovascular risk factors in patients with type 2 diabetes." Nutrition (2014).
• Nybo, Lars, et al. "Cerebral ammonia uptake and accumulation during prolonged exercise in humans." The Journal of physiology 563.1 (2005): 285-290.
• Takeda, Kohei, et al. "Effects of citrulline supplementation on fatigue and exercise performance in mice." Journal of nutritional science and vitaminology 57.3 (2011): 246-250.
• Turnbaugh, Peter J., et al. "A core gut microbiome in obese and lean twins." nature 457.7228 (2009): 480-484.

Whey + Casein - A Superior Post-Workout Shake in Theory (Fast + Slow) and Practice (Results of a 10-Week Study)

Casein & whey - Many companies sell both. For a good reason!

It appears to be logical. By combining whey and casein in your post-workout shake you would have the protein synthesis triggering spike of amino acids from the whey and the long-lasting pro-anabolic hyperaminoacidemia (=elevated amino acid levels in the blood) from casein. Can you ask for more?

Yes, you can! You can ask for scientific evidence that this is actually superior to say spiking your whey protein with additional pro-anabolic BCAAs (Atherton. 2010; Blomstrand. 2001) and allegedly recovery boosting glutamine (Sharp. 2010).

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Luckily, Kerksick, et al. did exactly this study in 2006, already. It's quite interesting that it is rarely cited, which is why I think it's worth its own SuppVersity post despite the fact that it's already 9 years old. Ah... well, and of course it's also worth being cited because it's a 12-week (10 weeks training time) resistance training + supplementation study that does not fool us to believe that whey + BCAA may be superior, because the researchers failed to measure the actual muscle gains in a long(er) term study.

Table 1: Overview of the resistance training protocol the subjects followed for 10 weeks after
an acclimatization phase of 2 weeks (Kerksick. 2005).

As the authors point out, "the purpose of this study was to examine the effects of whey protein supplementation on body composition, muscular strength, muscular endurance, and anaerobic capacity during 10 weeks of resistance training" (Kerksick. 2006). Thirty-six resistance-trained males (31.0 +/-  8.0 years, 179.1 +/- 8.0 cm, 84.0 +/- 12.9 kg, 17.8 6.6%) followed a 4 days-per-week split body part resistance training program for 10 weeks.

No, adding BCAAs to your intra-workout will not increase your gains: The previously cited study by Blomstrand et al. (2001) does not just show that the ingestion of BCAAs post-workout can increase protein synthesis. It does also prove that doing the same intra-workout may be tasty, but not productive.

Table 2: As you can see, the supplements were isocaloric. Differences in the energy intake from the supplement, which had be consumed as quickly as possible, but ideally within 2 hours, following the workouts on training days and in the morning ( 9:00 AM) of nontraining days, can thus not explain the different study outcomes (Kerksick. 2006)

Three groups of supplements were randomly assigned, prior to the beginning of the exercise program, in a double-blind manner to all subjects (see Table 1 for details):

• 48 g per day (g·d 1) carbohydrate placebo (P), 
• 40 g per day of whey protein + 8 g per day of casein (WC), or 
• 40 g per day of whey protein + 3 g per day branched-chain amino acids + 5 g L-glutamine (WBG). 

At 0, 5, and 10 weeks, subjects were tested for fasting blood samples, body mass, body composition using dual-energy x-ray absorptiometry (DEXA), 1 repetition maximum (1RM) bench and leg press, 80% 1RM maximal repetitions to fatigue for bench press and leg press, and 30-second Wingate anaerobic capacity tests.

Now what's most interesting for us, obviously are additional effects of the supplements on the body composition of the study participants - despite identical total energy and protein intakes (2.1g/kg body weight both the WBG and WC groups).

Figure 1: Changes in lean and fat mass over the course of the 10-week training period (Kerksick. 2006).

An effect of which the data in Figure 1 tells you that it was the most significant for the WC group. Ok, after the 5-weeks mark the gains stagnated, but in the whey + amino acid group, the subjects even lost the lean mass they'd gained. Quite interesting, by the way, because this coincided with a reduction in volume and an increase in weight... so could it be that training in the higher rep ranges is eventually more anabolic? Well, to prove that we would have to do another study.

Protein Requirements of Dieting Strength Athletes: More is Better Only in the Presence of Adequate Carb & Fat Intake. Optimal Muscle Retention With 2-3g/kg Lean Body Mass | more

What this study shows, is not that training in a higher rep range of 10 reps per set is more anabolic than training in the 6-8 range. What the study at hand shows is that the combination of plain whey and casein proteins is vastly superior to the funky "BCAA-powered" and "glutamine enhanced" protein powders you will see in the stores and in shiny advertisments.

And let's be honest, in view of the way the fast and slow digesting proteins facilitate long-lasting elevations of amino acids in the blood (=hyperaminoacidemia), the results of this study are not exactly surprising | Comment on Facebook!

References:

• Atherton, Philip J., et al. "Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells." Amino acids 38.5 (2010): 1533-1539.
• Blomstrand, Eva, and Bengt Saltin. "BCAA intake affects protein metabolism in muscle after but not during exercise in humans." American Journal of Physiology-Endocrinology And Metabolism 281.2 (2001): E365-E374.
• Chad M., et al. "The effects of protein and amino acid supplementation on performance and training adaptations during ten weeks of resistance training." The Journal of Strength & Conditioning Research 20.3 (2006): 643-653.
• Sharp, Carwyn PM, and David R. Pearson. "Amino acid supplements and recovery from high-intensity resistance training." The Journal of Strength & Conditioning Research 24.4 (2010): 1125-1130.

The A to Z of Effective & Less Effective Immuno-Nutrients to Prevent and Combat Respiratory Tract & Other Infections

Teddy bears are like vitamin C and zinc. They can help you when you are already sick, but what are supplements athletes and gymrats take in advance to survive the flu season without getting sick at all?

Specifically during the winter time, hard working athlete and manic gymrats can be particularly susceptible to all sorts of infections. To help you having to work out with a handkerchief in your hand all winter long, I have compiled a non-comprehensive list of supplements that may help you to maintain and even improve your immune defenses and thus to survive the cold and dark winter times without catching a cold or even the flu.

In their recent review in the Journal of the International Society of Sports Nutrition Vinicius Fernandes Cruzat, Maurício Krause and Philip Newsholme reviewed the extensive literature on nutritional supplements that act as immuno-nutrients, may to reduce immunosuppression and excessive inflammation in hard-training athletes and gymrats like yourself (or yourself in 2015 ;-)

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In said paper, the researchers from the CHIRI Biosciences Research Precinct at the Curtin University in Perth and the Laboratory of Cellular Physiology at the Federal University of Rio Grande do Sul in Porto Alegre focus what they call the "key immuno-nutrients" L-glutamine, L-arginine, branched chain amino acids (BCAA) and whey protein. Now this would not be the SuppVersity if I didn't go beyond this list and added a few more or less promising extra supplements to the list. Before we get to any of those extras, let's briefly recap what Cruzat et al. (2014) found:

"Although a balanced diet with high quality and sufficient quantity of nutrients is essential, there is growing evidence that some non-synthetic supplements can assist optimal nutrition. In fact, the use of nutritional supplements especially the provision of amino acids, has grown year-on-year. [...]

The use of proteins and amino acids for supplementation deserves special attention, since these molecules are critical for anti-oxidant and fuel provision, participating in the whole-body energy homeostasis, growth, development, recovery and immune responses.

As Cruzat et al. point out, the key targets for immunonutrition may include provision of key metabolites for immune cells per se. In other words: Immuno-nutrients feed the immune system and don't suppress but optimize the multi-layered immunte response consisting of

• the inflammatory response and cytokine release, 
• the production of chaperone proteins such as the heat shock proteins (HSPs), 
• changes in the redox balance (including glutathione, GSH metabolism), and 
• the protection of skeletal muscle mass (see Figure 1). 

Thus your reasons to consume immuno-nutrients go well beyond warding off the common cold and encompass (a) performance improvements, (b) the general strengthening of the immune system and (c) the shortening of the exercise recovery period (Nieper. 2005).

Figure 1: Biphasic immuno-inflammatory response to severe exercise and the possible immunonutrition role. Immuno-inflammatory response induced by severe exercise or heavy periods of training and the proposed role of specific nutrients with immune benefits, also called immunonutrition (Cruzat. 2014).

In that, the most widely used supplements are vitamins and minerals. Reliable evidence for their immuno-protective effects, however is scarce and the results are ambigious:

• Vitamin C: South African ultramarathon runners did demonstrate that vitamin C (but not E or beta-carotene) supplementation (about 600 mg day7 1 for 3 weeks) was related to fewer reports of upper respiratory tract infections (URTI) symptoms (Peters 1983, 1990, 1993, 1996; Peters-Futre, 1997).
  
  

  

  Classic ROS-scavengers like vitamin C are not just ineffective, when it comes to countering the increased susceptibility to infection they have also been shown to hamper the adaptational response to exercise | read more.

  These beneficial effects have yet not been replicated by other research teams. Himmelstein, Robergs, Koehler, Lewis and Qualls (1998), for example, reported no alteration in URTI incidence among 44 marathon runners and 48 sedentary individuals randomly assigned to a 2 month regimen of 1000 mg /day of vitamin C or placebo. And in view of the fact that most randomized, placebo-controlled studies have been unable to demonstrate that vitamin C supplements modulate immune responses following heavy exertion (Nieman et al., 1997b, 2002b; Nieman, Peters, Henson, Nevines, & Thompson, 2000b), it should be clear that vitamin C must not be counted among the highly effective immune nutrients. 

Zinc + C, not protetive, but effective? While the evidence supplementing with a combination of vitamin C and zinc would protect you from upper respiratory tract infections (URTIs) is scarce, there are studies like Maggini et al. (2012) which indicate that the provision of a combination of 1000 mg vitamin C plus 10 mg zinc in patients with the common cold will lead to a nonsignificant reduction of rhinorrhoea duration (range 9 – 27%) was seen. Moreover, a pooled analyses of the two studies Maggini et al. conducted shows that "vitamin C plus zinc was significantly more efficient than placebo at reducing rhinorrhoea over 5 days of treatment" (Maggini. 2012). Furthermore, symptom relief was quicker and the product was well tolerated. Despite the fact that the subjects in these experiments were ordinary people, upping your zinc and vitamin C intake, when you've already caught a cold may help you to recover faster and thus get back to the grind earlier.

• Vitamin E: As Niemann et al. point out in their review of the efficacy of various immuno-nutrients, vitamin E functions primarily as a non-specific, chain-breaking antioxidant that prevents the propagation of lipid peroxidation. The vitamin is a peroxyl radical scavenger and protects polyunsaturated fatty acids within membrane phospholipids and in plasma lipoproteins.
  
  The effect of vitamin E supplementation on the inflammatory and immune response to intensive and prolonged exercise is largely unstudied and equivocal. Cannon et al. (1991) found that vitamin E supplementation of 800 IU/day for 48 days attenuated endotoxin-induced IL-6 secretion from mononuclear cells for 12 days after running downhill on an inclined treadmill. Singh et al. (1999) showed no effect of vitamin E supplementation (4 days, 800 IU/day) on the increase in plasma IL-6 following a 98 min treadmill run at 65 – 70% V_ O2max to exhaustion. Petersen et al. (2002) reported no influence of vitamin E and C supplementation (500 mg and 400 mg, respectively, for 14 days before and 7 days after) on the plasma cytokine response to a 5% downhill 90 min treadmill run at 75% VO2max.
  
  

  

  Figure 2: Chronic supplementation with 800 IU of vitamin E (as alpha-tocopherol) has significant negative effects on markers of lipid oxidation and inflammation in triathletes (Nieman. 2004).

  A 2004 study in the course of which triathletes competing in the Kona Triathlon World Championship race event received 800 IU/day of a-tocopherol for two months does even indicate that vitamin E can increase the degree of exercise induced lipid peroxidation and the amount of several cytokines in the blood following a triathlon.Against that background and in view of the previously cited ambiguous results, Niemann et al. (2006) rightly conclude that "vitamin E supplementation to counter immune suppression and oxidative stress in endurance athletes cannot be recommended" (Niemann. 2006).
• Vitamin D: For vitamin D a slightly different image emerges. It appears to be indisputable that athletes with low vitamin D levels are at higher risk of upper-respiratory tract infections - specifically during winter times (He. 2013).
  
  The results of clinical trials investigating the benefits of vitamin D supplementation, however, are less unambiguous. In non-athletes, the monthly administration of 100 000 IU of vitamin D did not reduce the incidence or severity of URTIs; and that despite the fact that the supplement brought the 25OHD levels of the healthy subjects up, significantly (Murdoch. 2012). A meta analysis by Bergman et al. (2013), however indicates that "vitamin D has a protective effect against RTI, and dosing once-daily seems most effective".
  
  

  

  Figure 3: Length of time to viral infection related to initial serum concentration of 25-hydroxyvitamin D.
  Shown are the results of the pharmacodynamic model relating 25-hydroxyvitamin D to length of time before a viral respiratory tract infection (Bergman. 2013)

  Bergamn et al. do yet also point out that "[d]ue to heterogeneity of included studies and possible publication bias in the field, these results should be interpreted with caution" (Bergman. 2013). Against that background it may be a good idea to at least make sure that you are in the "normal range" for vitamin D - irrespective of the fact that low levels may rather be a marker than a trigger of an increased susceptibility to infections that results from uncontrolled inflammation (vitamin D as a negative acute phase reactant | cf. Waldron. 2013).

Next to vitamins, many studies have described the use of proteins, such as whey for supplements or isolated amino acids like glutamine (Kreider. 2008; Cury-Boaventura. 2008).

Simply eating enough: It may sound funny, but in the end it's not surprising that a lack of readily usable energy makes you more susceptible to infections. Firstly, a general calorie restriction is often related to an insufficient intake of important micronutrients (Pendergast. 2002). And even if the intake of all micronutrients is adequate. Important immune factors such as glutamine are (ab-)used as a substrate to produce glucose in the liver and are thus no longer available to "feed" your immune cells. Accordingly it should not surprise you that Niemann and Bishop highlight in their review of "nutritional strategies to counter stress on the immune system in athletes" that the existing data indicates that "physiological stress to some aspects of the immune system is reduced when athletes use carbohydrate during intense exertion lasting 90 min or more" and their own experiments suggest that this means "that athletes using carbohydrate beverages during competitive events will lower their risk of sickness afterwards" (Nieman. 2006).

Figure 4: Mechanisms involving whey proteins as a source of different immunonutrients. (Cruzat. 2014).

In their previously cited review, Cruzat et al. included a nice graphical overview (Figure 4) of the mechanisms by which complete proteins and peptides and their individual amino acids effect the immune system of hard training athletes.

As you can see in Figure 4, Cruzat et al. put a particular emphasis on whey protein - for good reasons.

Firstly, whey contains all the "good" amino acids of which previous studies indicate that they may have direct beneficial effects on the immune system:

• Glutamine: As Cruzat et al. point out, "L-glutamine is probably the most widely recognized immuno-nutrient since it can be used as an oxidizable fuel, a substrate for nucleotide synthesis, a modulator of intermediary metabolism of amino acids, HSP expression and a component of GSH-mediated antioxidant defense" (see Figure 5 | Cruzat. 2014).
  
  Put simply glutamine is the food your immune cells thrive on. Accordingly scientists, athletes and coaches have speculated ever since the early 1990s that supplemental glutamine should be able to prevent the exercise induced immune impairments.
  
  

  

  Figure 6: 5g of glutamine per day led to significant reductions in the occurrance of infections in marathon, ultra-marathon, mid distance runners and rowers (Castell. 1996a).

  Why? Well, exercise depletes the amount of circulating glutamine and will thus "steal" the fodder your immune cells need to survive and function (Wernerman. 2008).
  
  And in fact, there are studies that support the logical conclusion that the repletion of the glutamine that has been burned as alternative fuel during a workout with 0.1 g/kg body weight ameliorates the exercise induced reduction of lymphocytes, and could thus eventually reduce the risk of URTI’s (Castell. 1997).
  
  In that, I deliberately used the conditional, because subsequent studies with fixed (20–30 g/day) or variable (0.3 - 0.5 g/kg body wt) doses of glutamine did not report similar outcomes (Castell. 1996b; Krzywkowski. 2001; Hiscock. 2002). Accordingly, Castell et al. write in their contribution to the BMJ A-Z Supplement review (ed. Newsholme. 2011):
  

  "Overall, there is no consensus or unifying concept to explain the efficacy of exogenous provision of glutamine alone on performance in athletes, although in combination with carbohydrate or other amino acids, significant improvements have been reported." (Newsholme. 2011)

  In other words: Benefits can't be guaranteed, but specifically when glutamine is ingested in amounts of at least 20g/day in addition to carbohydrates and protein supplements it appears as if it could be a useful dietary supplement for hard-training athletes.

Where are all the other supplements gone? As I wrote in the introduction, this list is not supposed to be comprehensive. Furthermore, agents like quercetin, beta-glucan, curcumin or astragalus may be backed by animal studies, their efficacy in human beings does yet warrant further testing - specifically in athletes (Nieman. 2006). Other supplements such as the often-used herb Echinacea purpurea have been shown to fail to stimulate the nonspecific immune response and may be useful only when you are already sick or if the preperations are administered intravenously (Schwarz. 2002).

• Arginine: No, this is not a mistake. L-arginine is in fact the #2 on the list of supplemental immune modulators for hard-training athletes. Needless to say that it's not arginine itself, but rather Nitric Oxide (NO) which acts as a mediator of inflammation and immune system activation in the human body (Krause. 2011 & 2012).
  
  As a SuppVersity reader, you know that arginine has little ergogenic effect. It has beneficial effects in diabetics and may offer benefits for people who want to control their blood pressure. As a immuno-modulator, however it is similarly ineffective as it is as an ergogenic. Benefits can only be expected if the blood levels of arginine are depleted and that is - even with heavy exercise - usually not the case.

Whey protein, however, is more than the sum of its amino acid parts. Yes, whey can contain up to 26% of BCAA, plus L-arginine, L-lysine, L-glutamine.

Figure 7: Effect of maltodextrin (filled square) and maltodextrin plus hydrolyzed whey protein enriched with glutamine dipeptide (filled triangle) supplementation on exercise-induced loss of membrane integrity and depolarized mitochondria in lymphocytes and neutrophils, which are essential for the response against viral infections, such as upper respiratory tract infections (URTI), in athletes after intense training (Cury-Boaventura. 2008).

Whey does yet also contain a range of powerful proteins / peptides, namely betalactoglobulin, alpha-lactalbumin, bovine serum albumin, lactoferrin, immunoglobulins (e.g. IgA), lactoperoxidase enzymes, glycomacropeptides, as well as vitamins such as vitamin D, and minerals such as Ca2+, of these...

• lactoferrin and lactoferricin, demonstrate direct anti-microbial activity and may thus protect you from infections,
• lysosome, lactoperoxidase and diverse globulins and peptides in whey provide a synergistic protective “cocktail” activity against viral and bacterial organisms (Ha. 2003), and
• sulphur-containing amino acids, such cysteine and taurine attenuate the reduction of intracellular GSH concentration induced by intensive exercise (Lands. 1999). 

For all three of them, it is yet not fully established to which extend they contribute to the proven immune-modulating effects of whey (note: the levels of these agents will be higher in concentrates compared to isolates, due to the increased number of processing steps). It is in fact likely that Cruzat et al. (2014) are right, when they say that its the cocktail of amino acids, proteins, peptides and other micro- and macronutrients, vitamins and minerals in whey protein that acts via direct and indirect pathways (e.g. via optimizing the redox status / GSH) on the immune function of athletes.

Bottom line: While there is good evidence for vitamin D supplementation (1,000-2,000IU/day in individuals with low levels and / or hard-working athletes during the winter months) and high doses of glutamine in hard working athletes. There is little doubt that the amino acid + protein + peptide coctail in whey proteins is the "goto supplement" you would choose if you wanted to use only one of the supplements discussed in this article.

Whey Beyond Brawn: 10+ Things You Probably Didn't Know Whey & Peptides That Form During its Digestion Can Do | learn more.

In that, a reasonable dosage suggestion would be similar to that for maximal muscle hypetrophy and range from 20-60g per day - with the higher dosage being consumed in 2-3 servings evenly spread accross the day. Furthermore, studies like the one by Cury-Boaventura et al. (2008) indicate that, during periods of intense training, it may be useful to add glutamine. Either in large amounts of 10-20g per day (5-10g on top of each serving of whey) or, as it was the case in said study, as a dipeptide which has a higher chance of making it past the splachnic bed and not ending up as "fuel" for your organs and or glyconeogenic substrate in the liver.

And yes, if you've already caught a cold, 1 gram (in divided doses) of the the good old vitamin C (if you want to along with 5-15mg of zinc) is useful, as well - along with plenty of rest and sleep, of course ;-) Comment on Facebook!

References:

• Cury-Boaventura, Maria Fernanda, et al. "Effects of exercise on leukocyte death: prevention by hydrolyzed whey protein enriched with glutamine dipeptide." European journal of applied physiology 103.3 (2008): 289-294.
• Bergman, Peter, et al. "Vitamin D and respiratory tract infections: a systematic review and meta-analysis of randomized controlled trials." PloS one 8.6 (2013): e65835. 
• Castell, L. M., E. A. Newsholme, and J. R. Poortmans. "Does glutamine have a role in reducing infections in athletes?." European journal of applied physiology and occupational physiology 73.5 (1996a): 488-490.
• Castell, L. M., et al. "Some aspects of the acute phase response after a marathon race, and the effects of glutamine supplementation." European journal of applied physiology and occupational physiology 75.1 (1996b): 47-53.
• Castell, Linda M., and Eric A. Newsholme. "The effects of oral glutamine supplementation on athletes after prolonged, exhaustive exercise." Nutrition 13.7 (1997): 738-742. 
• Cruzat, Vinicius F., et al. "Amino acid supplementation and impact on immune function in the context of exercise." Journal of the International Society of Sports Nutrition 201.4 (2014): 11:61.
• Cury-Boaventura, Maria Fernanda, et al. "Effects of exercise on leukocyte death: prevention by hydrolyzed whey protein enriched with glutamine dipeptide." European journal of applied physiology 103.3 (2008): 289-294.
• Ha, Ewan, and Michael B. Zemel. "Functional properties of whey, whey components, and essential amino acids: mechanisms underlying health benefits for active people (review)." The Journal of nutritional biochemistry 14.5 (2003): 251-258.
• He, Cheng-Shiun, et al. "Influence of vitamin D status on respiratory infection incidence and immune function during 4 months of winter training in endurance sport athletes." Exerc Immunol Rev 19 (2013): 86-101. 
• Hiscock, Natalie, and Bente Klarlund Pedersen. "Exercise-induced immunodepression–plasma glutamine is not the link." Journal of Applied Physiology 93.3 (2002): 813-822. 
• Lands, L. C., V. L. Grey, and A. A. Smountas. "Effect of supplementation with a cysteine donor on muscular performance." Journal of Applied Physiology 87.4 (1999): 1381-1385.
• Krause, Mauricio S., et al. "L-arginine is essential for pancreatic β-cell functional integrity, metabolism and defense from inflammatory challenge." Journal of endocrinology 211.1 (2011): 87-97.
• Krause, Mauricio, et al. "Differential nitric oxide levels in the blood and skeletal muscle of type 2 diabetic subjects may be consequence of adiposity: a preliminary study." Metabolism 61.11 (2012): 1528-1537.
• Kreider, Richard B., et al. "Effects of ingesting protein with various forms of carbohydrate following resistance-exercise on substrate availability and markers of anabolism, catabolism, and immunity." Journal of the International Society of Sports Nutrition 4.1 (2007): 1-11.
• Maggini, S., S. Beveridge, and M. Suter. "A combination of high-dose vitamin C plus zinc for the common cold." Journal of International Medical Research 40.1 (2012): 28-42.
• Murdoch, David R., et al. "Effect of Vitamin D3 Supplementation on Upper Respiratory Tract Infections in Healthy AdultsThe VIDARIS Randomized Controlled TrialVitamin D3 and Upper Respiratory Tract Infections." Jama 308.13 (2012): 1333-1339.
• Newsholme, Philip, et al. "BJSM reviews: A to Z of nutritional supplements: dietary supplements, sports nutrition foods and ergogenic aids for health and performance—Part 18." British journal of sports medicine 45.3 (2011): 230-232.
• Nieman, David C., et al. "Vitamin E and immunity after the Kona triathlon world championship." Medicine and science in sports and exercise 36 (2004): 1328-1335.
• Nieman, David C., and Nicolette C. Bishop. "Nutritional strategies to counter stress to the immune system in athletes, with special reference to football." Journal of sports sciences 24.07 (2006): 763-772.
• Nieper, A. "Nutritional supplement practices in UK junior national track and field athletes." British journal of sports medicine 39.9 (2005): 645-649. 
• Pendergast, David R. "Effect of dietary intake on immune function in athletes." Sports medicine 32.5 (2002): 323-337.
• Schwarz, Eveline, et al. "Oral administration of freshly expressed juice of Echinacea purpurea herbs fail to stimulate the nonspecific immune response in healthy young men: results of a double-blind, placebo-controlled crossover study." Journal of Immunotherapy 25.5 (2002): 413-420.
• Waldron, Jenna Louise, et al. "Vitamin D: a negative acute phase reactant." Journal of clinical pathology (2013): jclinpath-2012. 
• Wernerman, Jan. "Clinical use of glutamine supplementation." The Journal of nutrition 138.10 (2008): 2040S-2044S.

Glutamine or BCAA, Which is the Better Fatique Buffer? 18g GLU Suprisingly Effective, 9.5g BCAAs (Un-)Surprisingly Useless as Blood Fatigue Factors & Cytokine Buffers

Rowing is an excellent cardio exercise for wanna be bodyuilders, by the way!

I am not really a fan of glutamine, but unlike BCAAs that are still hyped all over the Internet, the conditionally essential amino acid which is the most abundant of all amino acids in human blood is at least not falsely heralded as a potent catabolic, anabolic, weight loss adjuvant and what not, any longer.

Against that background I have to admit that I am not exactly unhappy to tell you that Ga Hee Koo, Jin Hee Woo, Sung Whun Kang, and Ki Ok Sjin who work at the Dong-A University and the Republic of Korea Airforce Academy, have recently observed that BCAAs have absolutely no, glutamine at least a minimal impact on the blood fatigue factor response of juvenile athletes in response to a 2,000 m all out rowing challenge w/ placebo, BCAA or glutamine supps.

Learn more about amino acid and BCAA supplements at the SuppVersity

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In the corresponding experiment, the scientists from the College of Sports Science at the Dong-A University had five male juvenile elite rowing athletes perform the same 2,000m rowing test at maximal intensity after having received a placebo, BCAA, or glutamine for 7 days before
the test. The specific supplementation regimen included:

• BCAA (Spomax, Seoul, Republic of Korea) was given three times a day (25% valine, 50% leucine, 25% isoleucine, 3.15 g/day).
• L-glutamine (Optimum Nutrition, Aurora, IL, USA, 6 g/day) was given three times a day.

Blood samples were collected from the antecubital vein on the day of testing while resting before the test, immediately at the end of test, and 30 min after the test. All tests were conducted with a 1-week interval to eliminate the potential effects from potentially longer-lasting effects of the previously administered supplement.

Which parameters did the researchers test and why? Koo et al. tested lactate, the accumulation of which will eventually impair ATP synthesis and lead to muscular fatigue. They tested the accumulation and clearance of ammonia, which can trigger central fatigue, when the levels increase rapidly during high intensity exercise. And they tested creatine kinase (CK) which is a classic marker of muscle damage and IL-8 and IL-15, two cytokines that will be elevated, when the activity of the immune system is not sufficient to deal with exercise induced stressors.

The actual test was conducted with an indoor rowing machine (Concept², Morrisville, VT, USA) two times each for supplementation with the placebo, BCAA, and glutamine. All the subjects performed a 2,000 m (Olympic single scull race) race at their own individual maximum paces (42–45 pace for 0m~250m, 40 pace for 250m~500m, 36–38 pace for 500m~1,500 m, and over 42 pace for 1,500 m~2,000 m)

Figure 1: Serum markers of fatigue and muscle damage, expressed relative to placebo (Koo. 2014)

There were no significant differences in lactate levels; a significant phopshorus-sparing effect from BCAAs (small effect size) and glutamine (large effect size) of which the scientists believe that it was mediated by the use of the amino acids to maintain adequate muscular ATP levels; and there was a non-significantly elevated level of ammonia in the glutamine group (some arginine could help clear those | learn more) that returned to normal 30 min after the test.

The dosages are not the same! That's unfair! No, it's not necessarily unfair, but it would still have been better to test 18g of glutamine vs. 18g of BCAAs. There is after all one thing both have in common: They both can be used as workout fuel in the muscle, so the advantage of glutamine may have become smaller (maybe even non-significant), if both had been administered at the same amounts.

The creatine kinase levels (a marker of muscle damage) and the levels of interleukin-8 and interleukin-15, however, were significantly lower in the glutamine than they were in either the BCAA or placebo group. This is a result of which the authors of the study believe that, it may...

"[...]represent the effects of energy supplementation from glutamine supply, which activated as a fuel in the muscle and as a nitrogen precursor for nucleotide synthesis" (Koo. 2014). 

An alternative explanation would be that glutamine (probably via its connection to glutathione; see Roth. 2002) had a direct protive effect on the skeletal muscle tissue during the workouts.

Figure 2: Serum levels of inflammatory cytokines expressed relative to placebo (Koo. 2014)

This hypothesis would also be supported by the changes in interleukin expression. i.e. the blunted increase of interleukin-8. IL-8 is an inflammatory cytokine that serves as a chemical signal which attracts neutrophils at the site of inflammation. The corresponding increase in IL-15, which was likewise reduced in response to sub-chronic glutamine supplementation, on the other hand, indicates a reduced production (not activity!) of natural killer cells.

Table 1: Intense exercise is not the only condition / disease that's associated  with low blood glutamine levels (Roth. 2002)

In that, it is crucial to understand that the authors (imho reasonably) believe that the increase in IL-8 & IL-15 is a compensatory mechanism which is initiated to counter the reduced immune function that occurs, when the amount of glutamine in the blood and skeletal tissue drops. We do after all know for sure that the this will result in a significant decrease in the cell proliferation rate of lymphocytes, the amount of antioxidants, peptides, amino sugars related to cell resistance against apoptotic processes, purines, as well as the synthesis of key molecules such as pyrimidines which are all involved in redox reactions (Roth. 2002).

Whether supplementation is warranted with low(er) intensity exercise, as well, is however questionable. Previous research by Ostrowski et al. (2001), who had their subjects exercise at significantly lower intensities, did not find comparable increases in IL-8. This difference is probably due to a comparably lower amount of exercise induced stress that corresponds to the reduced intensity. In this context it's also worth mentioning that Fischer et al. (2006) report that the blood chemokine concentrations would increase little or remain stagnant unless a sufficient muscle mass is mobilized and maintained at a certain level of intensity sufficiently... now, everyone who has ever done an all-out rowing time trial will confirm: This is (a) intense and will (b) involve almost every muscle in your body.

If maximal muscle hypertrophy, not performance increases in all-out (aerobic) exercise and protecting your immune function is your goal, buy some whey + casein and stay away from glutamine & BCAAs unless you insist on wasting money on hitherto unproven promises of strength & size gains | learn more

Bottom line: In contrast to BCAAs which will "only" blunt the increase in debilitating phosphorus in the blood,  "glutamine supplementation could be helpful for enhancement of immune function and the defensive inflammatory reaction after exercise." (Koo. 2014)

The results of the study at hand do thus confirm an older piece of broscience, i.e. the importance and efficiency of adequate amounts of glutamine (15g or more per day!) for recovery and immune function. They do yet also put another question mark behind the ergogenic potential of brach-chained amino acids about which I have written repeatedly in previous articles here at the SuppVersity (in other contexts, BCAAs may well be superior to glutamine, but long-term studies to prove any of the claimed benefits are missing, as well).

Whether the results from the study at hand warrant the consumption of 18g of glutamine per day for all of us, is still questionable. If you are in a phase of your training that requires a lot of all-out exercise and already feel that your immune defenses are dwindling, it probably won't hurt to buy a cheap 500g bag of glutamine from the bulk supplier you trust. Don't expect instant results of illusive tingles as you'll get them with certain other supplements. If there are benefits they will only be visible over time and will include faster / more complete recovery, reduced rates of infection and overall fatigue. Eventually, these would help you to make faster gains in strength and size, though | Comment on Facebook.

References:

• Fischer, Christian P. "Interleukin-6 in acute exercise and training: what is the biological relevance." Exerc Immunol Rev 12.6-33 (2006): 41.
• Koo, Ga Hee, et al. "Effects of Supplementation with BCAA and L-glutamine on Blood Fatigue Factors and Cytokines in Juvenile Athletes Submitted to Maximal Intensity Rowing Performance." Journal of Physical Therapy Science 26.8 (2014): 1241-1246.
• Ostrowski, Kenneth, et al. "Chemokines are elevated in plasma after strenuous exercise in humans." European journal of applied physiology 84.3 (2001): 244-245.
• Roth, Erich, et al. "Regulative potential of glutamine—relation to glutathione metabolism." Nutrition 18.3 (2002): 217-221.