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Yogurt & Co are good for athletes. But is this due to the bacteria?

As a regular here at the SuppVersity, you are well aware of the far-reaching effects of having the "right" or "wrong" bacteria in your tummy. The claim that having the "right" bacterial make-up in the gut could have beneficial effects on your performance in the gym or on the track is something you should not believe too credulously. If we had a study to prove these benefits, things would be different, though - a study like the one a group of researchers from the National Taiwan Sport University are about to publish in the scientific bible of resistance training, the Journal of Strength and Conditioning Research (Hsu. 2014).

In said study which is still available only as an accepted manuscript, Hsu et al. investigated the association of intestinal bacteria and exercise performance in specific pathogen-free (SPF), germ-free (GF), and Bacteroides fragilis (BF) gnotobiotic mice (animals in which only certain known strains of bacteria and other microorganisms are present).
To this ends, the scientist had the rodents swim to exhaustion to determine whether enteric bacteria alter antioxidant enzyme levels, exercise performance and physical fatigue. In addition, they tested the antioxidant enzyme activities, physical performance and anti-fatigue function after monocolonizing GF mice with B. fragilis (BF).

Figure 1: Time to exhaustion during exercise test and body composition of the miceaccording to the make-up of their gut microbiome; data expressed relative to group means (Hsu. 2014)

What they found was an increased time to exhaustion for the previously germ-free (GF) mice after theyd been colonized with B. fragilis (BF). Similar results were observed for the specific pathogen-free and Bacteroides fragilis gnotobiotic mice, who were also more enduring than the obesity resistant (Bäckhed. 2007) germ-free mice.
As any SuppVersity veteran would expect, the germ-free mice were leaner than the rest of the pack. At the same time, the "sterile" mice did yet also have a lower liver, muscle, brown adipose, and epididymal fat pad weight than the SPF and BF mice.

Figure 2: Selected markers of antioxidant status in serum and liver; expr. rel. to group means (Hsu. 2014)

The markers of antioxidant defenses, the scientists measured were highest in the lean + light germ-free mice and their specific pathogen-free cousins. Against that background its at least somewhat surprising that the performance differences are pretty significant.
References:

• Bäckhed, Fredrik, et al. "Mechanisms underlying the resistance to diet-induced obesity in germ-free mice." Proceedings of the National Academy of Sciences 104.3 (2007): 979-984.
• Cani, Patrice D., et al. "Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal." The American journal of clinical nutrition 90.5 (2009): 1236-1243.
• Cox, Amanda J., et al. "Oral administration of the probiotic Lactobacillus fermentum VRI-003 and mucosal immunity in endurance athletes." British Journal of Sports Medicine 44.4 (2010): 222-226. 
• DiMarco, N. M., et al. "A–Z of nutritional supplements: dietary supplements, sports nutrition foods and ergogenic aids for health and performance—Part 30." British journal of sports medicine 46.4 (2012): 299-300.
• Gleeson, Michael, et al. "Daily probiotics (Lactobacillus casei Shirota) reduction of infection incidence in athletes." (2011). 
• Hsu et al. "Effect of Intestinal Microbiota on Exercise Performance in Mice." Journal of Strength and Conditioning Research.  DOI: 10.1519/JSC.0000000000000644 | Publish Ahead of Print.
• Martarelli, Daniele, et al. "Effect of a probiotic intake on oxidant and antioxidant parameters in plasma of athletes during intense exercise training." Current microbiology 62.6 (2011): 1689-1696.
• West, Nicholas P., et al. "Lactobacillus fermentum (PCC®) supplementation and gastrointestinal and respiratory-tract illness symptoms: a randomised control trial in athletes." Nutrition journal 10.1 (2011): 30.

Believe it or not, but the question "low or high carb for breakfast" is non-sense, because there is no general answer. It depends on who is asking and what he is going to spend the rest of his day.

Before we can start reviewing the contemporary literature, we will have to define the term "breakfast" as the first meal in the day which is eaten in the AM. This definition differs from the "literal" one, Ive used in a previous article with the title "Circadian Rhythmicity - "Breakfast" or "Breaking the Fast"? Fasting as Zeitgeber & All About King, Prince & Pauper" (read it) and is thus in line with the mainstream idea of standing up, showering and... yes, you got it: having breakfast.

If you google "breakfast" and "obesity" youre served a colorful potpourri of "pro breakfast" articles which will inform you about "facts" like "Eating a big breakfast fights obesity and disease" (ScienceDaily), or "Breakfast Combats Obesity and Diabetes in Young People" (medscape).
Could all these "experts" be wrong? For the obedient average Joe this sounds crazy. Like one of those theories from your average Internet conspiracy theorist, but if you look at the actual evidence you have to admit:"A definitive conclusion can be made concerning the role of breakfast skipping in weight change." (McCrory. 2014)

The reasons for our cluelessness are manifold

There is for example a very good reason I anteceded this article with a definition of "breakfast". The latter is after all something you wont find in the average study, which could therefore consider eating a donut at 11am in as much as "breakfast", as it would discard having a protein shake immediately after you wake up as "not breakfast".

If we look at the actual "average Joe" (according to US National survey data), were getting into even more trouble. This guy was eating 2.76 meals in 1971–75, while he is now up to 2.96 in 1999–2002 (Kant. 2007).

In other words: Americans eat more frequently these days, but are still fatter

Obviously frequency alone doesnt tell us whether one of those "almost three" meals was actually the holy breakfast. I mean, if it wasnt its obvious the Americans became fatter and fatter - right (sarcasm)? The data we are interested in, is thus not the total number of meal (if you want to know more about that, take a look at "Many Small Meals Suck!" | go for it!). The data we are interested in is the data in Figure 1, the number of non-obedient US citizens who dont listen to the well-meant advice from the USDA and simply skip one of their holy meals.

Figure 1: Prevalence of skipping meals (breakfast, lunch, dinner) and snacking in the US, 2009–10 (McCory. 2014).

As McCorey highlights in a recent review (2014), their number rose. This seems to be a contradiction. I mean, if the number of meal skippers increases, shouldnt the number of meal (on average) decrease, when it in fact rose from 11% to 18%? Well, it should, if it was not for the snackers and grazers who either skip breakfast and snack all-day or are over-obediently grazin on 20+ small meals per day.

Figure 2: Prevalence of breakfast skipping among US men and women (USDA)

Whats interesting, is that we will find that the was a decrease in breakfast skippin from 2002 to 2009, of which I am pretty sure that it was (at least partly) mediated by headlines like the ones I quoted in the introduction to this article (USDA)

USDA shows a slight decrease in the prevalence of breakfast skippingin both men and women by about 4%. If not having breakfast was the root cause of the obesity epidemic, the average American should thus have lost a few pounds over the past decade - right?

Right! This should be the case if breakfast was the mythical "lean-maker" the "experts" want us to believe. The figures, i.e. the constantly increasing rate of obesity, dont disprove that (those who dont eat breakfast could simply gain even more weight), but they certainly put another "?" behind the statement that having breakfast has anti-obesogenic effects.

23% of males and 20% of females skip lunch!

Apropos "?", I am missing one, here! One behind the consequences of skipping lunch. With all the upheaval about skipping breakfast, people seem to have forgotten that lunch, not breakfast, was the most commonly skipped meal among most age groups in 2009–10. In most age groups, 23% of males and 20% of females are skipping this important (?) meal... and are - you bet - having an unhealthy snack later in the afternoon.
Anyway! This is the breakfast skipping research summary and no afford to dig up the two or three studies that dealt with skipping lunch explicitly. Lets thus, just for the time being, assume breakfast does in fact keep you lean. How on earth would eating some extra-food do that, when we all agree that the root cause of the obesity epidemic is after all the ravenousness of the average Westerner and the ways in which his / her diet multiplies these effects...oh, I guess the latter will lead us right to one of the answer to our question.

Proposed reasons for the anti-obesity effects of breakfast

I am not sure if I will be able to list all of them, but the following list of explanations that have been brought forward to explain the cross-sectionally observed negative association between body weight and breakfast eating is probably pretty comprehensive:

• skipping breakfast leads to lower satiety than if breakfast had been eaten, thus 
• overeating will ensue later in the day, which
• over time would result in weight gain

What? Yeah, in the end, this is all the "breakfastpromoters" have to tell you: Its an overcompensation for the energy missed at breakfast they blame the alleged fattening effects of not having breakfast on. As McCroy points out, in whats probably the most recent peer-reviewed analysis of the contemporary evidence, one could easily imagine another scenario

"in which breakfast skipping could result in no weight change over time, if breakfast skipping does not lead to overeating (i.e., if there is perfect compensation for the missed meal), or to weight loss if there is lack of compensation." (McCrory. 2014)

In his review McCory provides an enlightening overview of each of these possible scenarios, I dont want to keep from you. The“control” in this imaginary case study is a habitual breakfast eater with energy needs of 2000kcal/day, whose energy intake distribution across breakfast, lunch, snacks and dinner is 2000 kcal/day and therefore who is maintaining body weight.

Figure 3: Theoretical models illustrating different types of breakfast skippers vs. a habitual breakfast eater (McCrory. 2014).

There are potentially three types of habitual breakfast skippers: those with perfect compensation and maintain body weight, those who overcompensate and gain weight, and those who undercompensate and lose weight over time. In his consecutive review, in which McCrory considered only studies in adults (?18 years on average) and focusing primarily on experimental studies (short-term acute feeding trials or longer-term feeding trials) and longitudinal studies (prospective or retrospective, with the outcome of body weight change), the scientists from the Purdue University draws the following conclusions:

• Acute feeding studies on breakfast skipping effects on energy intake and appetite later in the day show equivocal results.
• Longer-term (2–3 weeks) randomized controlled trials do not show effects of breakfast skipping on weight change.
• In prospective studies with 3.7–10 years follow-up, individuals who consume breakfast more frequently gain less weight.

McCrory also points out that the lack of standardization is a major obstacle that makes it difficult, if not impossible to compare the results from different labs / different experimental setups.
References:

• Brown, Andrew W., Michelle M. Bohan Brown, and David B. Allison. "Belief beyond the evidence: using the proposed effect of breakfast on obesity to show 2 practices that distort scientific evidence." The American journal of clinical nutrition 98.5 (2013): 1298-1308.
• Kant, Ashima K., and Barry I. Graubard. "Secular trends in the association of socio-economic position with self-reported dietary attributes and biomarkers in the US population: National Health and Nutrition Examination Survey (NHANES) 1971–1975 to NHANES 1999–2002." Public health nutrition 10.02 (2007): 158-167.
• McCrory, Megan A. "Meal skipping and variables related to energy balance in adults: A brief review, with emphasis on the breakfast meal." Physiology & Behavior (2014).