The “Science” behind “Bonking”

It has long been “common knowledge” that endurance exercise is fuel-limited. This is most familiar to general populations as a commonly observed limitation on foot races that says that you will run out of energy, “hit the wall,” or “bonk” at around 20 miles. For common race distances, the effect is most frequently observed in the marathon (26.2 miles). The standard explanation is that you can only store a limited amount of carbohydrate fuel in the form of muscle and liver glycogen, and that you will bonk when the supplies run out. Management of the “problem” is variously accomplished by “carb-loading” before the race to super-fill (“super-compensate”) the glycogen stores, and by various refueling strategies during the race (which support a large industry that provides special drinks, gels, bars, and the like).

At the same time, there is a growing body of evidence that there is no reason to depend on stored carbohydrate fuel which is limited in quantity if you can mobilize your fat stores as a source of fuel. The problem seems to be that anyone who is accustomed (adapted) to eating a high-carbohydrate diet tends to preferentially burn carbohydrates as fuel and does not utilize the energy available from fat in a way that spares carbohydrate use during endurance exercise. These are the so-called “sugar burners” as compared to “fat burners.”

There are a few possible strategies to enhance fat burning. The most commonly discussed strategy is to train at slower, more aerobic paces, to train the body to optimize using fat as fuel. This approach was discussed by Alan Couzens. Although carbohydrate was also restricted, the main emphasis was on low intensity training, with pretty amazing results from the combined approach.

A second strategy, perhaps even simpler, is to change to a low-carbohydrate diet. Maintaining glycogen supplies in a partially depleted state encourages the development of aerobic apparatus via the action of AMP Kinase (increased mitochondria and associated fat burning enzymes such as carnitine palmitoyltransferase, necessary to help transport fatty acids across the mitochondrial membrane). People with deficiencies of carnitine palmitoyltransferase are unable to utilize fat for fuel efficiently, and can even suffer damaged muscles and rhabdomyelosis resulting in kidney failure. There is also evidence that people suffering from obesity and diabetes may have impaired mitochondrial function, which inhibits their fat burning and at least partially explains the origins of their condition. Similarly, a deficiency of carnitine can result in impaired mitochondrial function and even lead to symptoms of metabolic syndrome.

There is an adaptation period of a few weeks to lowering carbohydrate intake during which the appropriate metabolic pathways and aerobic enzymes and cofactors are up-regulated to better utilize fat as a substrate, allowing blood glucose levels during exercise to be more easily maintained. As Alan Couzens explains, lower carb intake should result in a 20% increase in fat burning in a few weeks. Numerous scientific studies bear this out. A recent study, for example, concludes that a high fat diet increased the rate of whole-body and muscle fat oxidation while reducing the rate of muscle glycogenolysis during submaximal exercise, even after restoring high carbohydrate intake. In this study, a high fat diet was followed for up to two weeks (which we know is just long enough to see significant adaptation), during which usual training was followed. A high carbohydrate diet was restored for the last few days along with a taper before racing. The athletes were able to maintain the increased fat oxidation even after reinstating high carbohydrate intake.

There is at least one supplement (Vespa) which is alleged to improve fat-burning during exercise. There is also some evidence that, all else being equal, the athlete that has the most efficient fat-burning ability can consistently beat the athlete with the higher raw power output (higher VO_{2 max}) in endurance competition.

An article in Running Times last year discussed the strategy of carb cutting to increase endurance, though the article suggests mainly forgoing carb supplementation on training runs, not going low carb in the training diet. The Ethiopian runners again are cited as evidence that a high carb diet is necessary to fuel runs, and there is speculation that they are somehow training themselves not to use glycogen as the predominant fuel by not consuming carbs while actually training. This conclusion seems unlikely to us, since it is well known that exercise causes an increase in blood sugar (due to action of epinephrine and glucagon), effectively mimicking the result of taking in supplemental carbohydrate while exercising. A marathoner does not “hit the wall” until they have run ~20 miles at race pace anyway, a condition not likely encountered during routine training runs for most of us.

Despite all that is known about “the wall,” people persist in believing that a high carbohydrate diet is necessary if you hope to be a good runner. A high carbohydrate diet may work well for Ethiopian runners, who are known for running prodigious mileage and training three times per day. At this training intensity, we seriously doubt their glycogen stores are ever completely full, and they may effectively be training in a perpetually glycogen depleted state, which would upregulate the same enzyme systems that occurs in the low carbohydrate condition. Perhaps what they are mainly training is the rapid replenishment of glycogen stores. However, for most of us amateur or older runners, we’re only fooling ourselves if we think we need to fuel exercise with a high carb diet. David does quite well on very minimal carbs (less than 50 g/day), while Cynthia prefers closer to 100 g/day. Since we generally only run once per day and even then usually less than 10 miles, there is no reason to consume any more carbs to fuel our exercise habits.

David has been a low-carb runner for more than two years now, keeping carbohydrate consumption low before, during, and after endurance exercise. While he won’t brag about his speed and has no plans to challenge any course records, he consistently finds that he has even energy levels and rapid post-event recovery with minimal muscle aches and pains. Fat fueling works for him! However, until very recently, while he refueled less often than is typical, he did routinely refuel using protein and fat for any event of more than 3–4 hours.

He was prompted to revisit the issue when he heard about a recent study (“Metabolic Factors Limiting Performance in Marathon Runners”) by Ben Rapoport when he had his fifteen minutes of fame on NPR in October 2010. Ben was attempting to model bonking in the context of marathon runners. David subsequently exchanged e-mail with Ben whose initial reaction was to interpret David’s personal experience as simply confirming Ben’s model, arguing that fat-fueling works, and that you don’t bonk as long as you run sufficiently slowly. David pointed out some flaws in Ben’s interpretation of the scientific data he analyzed and challenged him to define a performance that David might personally be able to achieve that he might consider sufficient to disprove his model, but he never responded to the challenge. We summarize here both a couple of the criticisms of Ben’s model and analysis and some more recent personal experience and experiments.

A key part of the experimental data that Ben used in building his model came from Romijn AJ, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, et al. (1993) “Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration,” Am J Physiol 265: E380–E391. That paper shows (in Fig. 8) the relative amount of particular substrates which are used in short-term exercise at three different intensities. The subject’s dietary habits were not identified, and any changes that might take place over more than a few minutes were ignored. The data show that more intense efforts use primarily muscle glycogen as fuel. They do not show the pathways that feed the muscle glycogen. Glycogen and glucose are rapidly interconverted, and over longer periods of exercise, new supplies of glucose are made by the liver. The liver, in turn, is capable of using any available fuel source via gluconeogenesis to keep blood glucose levels up. These fuel sources include ingested carbohydrates, protein, and fat as well as lactate, glycerol from liver and adipose tissue fat stores, and even body protein stores such as in muscle tissue. Which source predominates depends on availability. Some of the necessary up- and down-regulation of different metabolic pathways can take place on a short time scale to respond to instantaneous demand for fuel from the muscles and other bodily functions. However, there are also some key adjustments that respond more to average demand and supply to deal with changing diet, exercise demand, starvation, and the like, and these are events that tend to have time constants measured in days or weeks, not minutes or hours. The adaptation processes may be numerous and complex (or at least, we fully admit that we don’t understand all of them) and likely include adaptations in the skeletal muscles as well as in the liver. However, we think it is clear that the data extracted from Romijn do not actually show the underlying consumed fuel source for various levels of endurance exercise, and the data cannot reasonably be extrapolated to model and predict bonking.

One factor which Ben cites in favor of the importance of carbohydrate and fueling is the relative stoichiometry of oxygen consumption for each substrate. He states that carbohydrate oxidation typically generates approximately 120 kcal per mole of respired oxygen, whereas fatty acid oxidation typically generates only approximately 100 kcal per mole of oxygen. We would argue that this, while probably correct, is irrelevant in that the difference is relatively small, and the availability of oxygen is never a limiting factor at a typical aerobic marathon pace. There is always an excess of oxygen available. In any case, regardless of the underlying fuel used to generate blood glucose/glycogen, the immediate muscle activity (except for very short term bursts of power) is fueled by glucose.

Notwithstanding the possible flaws, Ben’s model does make predictions as to whether one is likely to bonk in a marathon. In particular, he has provided a calculator for the marathon. Putting in the best estimates David has for his personal situation, the calculator predicts that he should not bonk for finishing times over about 3 hrs. Since he can only sustain a 3-hour marathon pace for about 1 mile or so, he may never be able to really challenge the model experimentally using himself as a test subject.

However, David was inspired to test his need for refueling during running, and now has a significant number of test results that, if not sufficient to explicitly challenge Ben’s model, are at least startling to many people. For some time now, David routinely runs training runs of up to 4–5 hrs without refueling (water alone). This is still true when he runs with his son at faster speeds who typically chooses to refuel using at least a couple of energy bars or gels. David first pushed the envelope a bit on what was supposed to be a planned 18-mile run that stretched to about 26 miles when the route was blocked by an impassable rain-swollen river crossing. That run extended over about 7 hours including some significant rest breaks, so it was not at a strenuous pace, although it did include some significant elevation change. David consumed only water. The next experience was a 50K (31-mile), mostly flat run, again at a very modest pace, finishing in 6:50, again on water alone. Two weeks later, he completed a much more strenuous 50K on rough rocky trails with about 6000 ft of elevation gain (and loss) in 7:28 on water alone. In all three of these runs, David started with a breakfast of a two-egg cheese omelet and bacon about two hours beforehand. He felt some minor hunger around normal lunch time, but otherwise did not experience any significant fluctuations in energy level, and he certainly did not bonk. His overall weight was down about 3–4 lbs at the end of the day compared to the beginning, but looking at beginning-of-day weights across several days, any weight change was pretty much lost in the noise. Of course, it only takes about a pound of fat to fuel a 50K run, anyway. Another week later David ran yet another moderately hilly 50K event which was slower (8:04) due to snowy trail conditions. Due to a late start (10 am), he chose to eat a little at around the 6-hour mark, mostly because it was a long time since breakfast. However, the ability to do three 50K runs in four weekends, certainly confirms that post-event recovery was rapid.

So what’s the take-away message from all this? It’s interesting to compare our reaction and the experiments that David decided to try to others. Greg Crowther also blogged on Ben’s article. Greg’s big concern was inter- and intra-personal variability, and he questioned the validity of extrapolating from some sort of average measurement of performance to the needs of one individual on one particular day. He didn’t ask (as we did) if too many runners are needlessly afraid of bonking but rather, “if ingesting extra carbohydrates before and during a marathon might help you avoid ‘hitting the wall,’ why wouldn’t you do it? Especially after investing all of that time and effort in training, traveling to the race, etc.?” Hey, we’ll even go further: if ingesting fuel (whether carbohydrate, protein, or fat) during a race might help you maintain a faster pace for whatever reason and for whatever limited portion of the race, even it’s just a placebo effect (or tricking your Central Governor), then by all means go for it! But we also stand by our basic conclusions that (1) carbohydrates are simply not necessary before, during, or after endurance exercise, (2) they’re probably not even particularly beneficial, at least if you are suitably adapted to efficient fat-burning (and may be harmful to your long-term health) and not logging very high miles at high intensity, and (3) unless you’re able and motivated to run, say, an entire marathon at a high percentage of your VO_{2 max}, consuming much of any food immediately before, during, or after the event is entirely optional. Moreover, there may be some benefit to having the stomach completely empty while racing, in order to avoid stomach upset, intestinal discomfort/diarrhea or nausea when running at high intensity. (David does continue to believe in significant protein consumption sometime in the 12 hours or so following strenuous exercise as an aid to muscle repair and recovery, but the timing of even that refueling does not appear to be nearly as critical as some authors suggest.) David will probably resume modest consumption of fat and protein on longer events, just because he’s not big on skipping meals entirely, anyway, but it’s reassuring to know that he can easily keep going without any fuel if for any reason he needs to.

Primal Potatoes—a Contrary View

In a recent blog entry “Primal Potatoes, Part 2” the author tries to make the case that humans are evolutionarily adapted to include starchy foods such as tubers in their diets, and that there would be survival advantage in keeping glycogen stores higher using these sources of starch. We don’t disagree with all of the conclusions he ends up with, but we think that a lot of the “evidence” used is factually incorrect or misleading. Here’s our take:

There is no doubt that the human digestive system has broad adaptability. The fact that humans are “omnivores” who can digest most everything that any animals eat except straight cellulosic materials (grasses and dietary fiber) clearly provides a survival advantage in that it allows humans to survive for at least short periods on whatever food source is available. It does not follow, however, that the ability of humans to digest starches means that they provided a real performance advantage in hunting and/or survival activities and would have been a required part of our diet. Rather, it seems to us that humans are well-adapted to depend predominantly on aerobic exercise (fat-burning) which can be sustained for many hours even in a fasting state if necessary, using the generous fat storage capacity available. Humans have an auxiliary system able to use the much more limited glycogen (carbohydrate) energy stores for primarily short bursts of intense exercise (30 seconds or less at a time) or to supplement for higher intensities than can be sustained by fat burning alone. This auxiliary system is further adapted to replenish/restore itself fairly quickly, again, even without the aid of carbohydrate consumption. While it is possible to create situations in athletic training and competition where the rate of depletion can be faster than can be replenished in steady-state (especially for athletes who normally depend on carbohydrates for much of their calories), it does not follow that such rapid depletion followed by rapid replenishment using dietary carbohydrate sources, was ever important or necessary in evolutionary terms. Note, for example, that athletes in many sports routinely use “reps” or “intervals” of intense activity separated by recovery periods, typically with no consumption of food or drink during the recovery periods. To the extent that fuel stores are being restored during these recovery periods, the process does not depend on any particular external source of calories.

In effect, the body is so effective at conserving and recycling its limited stores of carbohydrate fuels that large dietary replenishment would not have been required to satisfy the needs of hunting and survival activities.

An article by Fournier was cited in “Primal Potatoes, Part 2” to support statements that “whereas typical glycogen stores will support an intense aerobic exercise for a few hours, a single maximal sprint effort will deplete one-third to one-half of glycogen stores,” and “humans can replenish glycogen stores without dietary carbohydrate, and even while fasting.” However, the article link did not work. A PubMed search found this article which appears to match the cited reference. The article describes experiments on rats which were made to engage in moderate exercise (swimming for 30 min with a weight attached to their tails), followed by a 3 min “sprint” (when a much heavier weight was attached to their tails). The main point of the article was to determine if the lactate produced during the sprint was the predominant source of carbon incorporated into newly synthesized glycogen. If you look at Fig. 1, you’ll see that the preceding “moderate” exercise depleted glycogen by at least 50% before the “sprint,” which then further depleted glycogen (down to ~25%). The researchers concluded that the lactate only provided ~50% of the newly synthesized glycogen, which actually is not surprising given that the previous glycogen depleting activity had already reduced the amount of glycogen available, and presumably any lactate that was or could have been produced and therefore recycled into new glycogen had already been oxidized completely and was no longer available. In short, the cited article does not support the first statement, which appears to be an exaggeration. There was no study showing that a single maximal sprint would deplete one third to one half of stored glycogen. Rather, the already ~50% depleted glycogen stores were further depleted by the “sprint,” showing only that the higher intensity the effort, the more rapidly the glycogen was depleted. A “single maximal sprint effort” as we understand it would most certainly not deplete a large fraction of glycogen stores. It may feel like it, but that feeling is not due to glycogen depletion per se, but rather due to acidification due to lactate and carbonic acid accumulation.

There is some confusion as to the meaning of the word “sprint” and how different available fuel sources are used by humans in sprint versus endurance events. True “sprints” (short bursts of maximal effort) do not even depend on glycolysis, which is too slow. There is a third energy storage and release system based on local stores of ATP and phosphocreatine. These are typically sufficient for about 7 sec of peak power output, and are rapidly regenerated during any rest periods using energy from aerobic glycolysis or fat metabolism. (See, for example, Noakes, Lore of Running, p 154.) But even a 100 m sprint by a world-class runner takes longer than 7 sec, and some energy must then come from glycolysis. Perhaps a single clean-and-jerk or other 1 rep maximum weight lift can be completed using primarily this sort of burst of maximal energy, but even a typical set of 10–15 reps in weight training takes longer.

Most people probably think of a “sprint” as something roughly equivalent to a 100 m or maybe as much as a 200 m maximum-speed run. Such efforts typically take about 10–30 sec to complete and, while not possible using only the local ATP and phosphocreatine stores, the effort can be completed mostly anaerobically, fueled by local glycogen stores. The 30-second maximum for this kind of effort is probably limited by the acidification resulting from the rapid production of lactate. What glycogen has been depleted can regenerate rapidly when the maximal effort ends. “Recovery” for a repeat of a similar effort largely consists of clearing enough of the accumulated lactate to relieve the sensation of “burning” in the muscles. Fuel depletion is not a major issue.

Three minutes of a “sprint swim” (or an 800 m run or a flight from a predator) is a much more complex sort of “maximal effort.” It is not a sprint as usually defined for humans. It is a “middle distance” that cannot be completed purely anaerobically. Even an 800 m run (2 min of effort for good runners) is considered an endurance event (requiring stamina), and much of the speed can be developed using aerobic training, though a maximal effort of this length will utilize primarily glycolysis and generate a lot of lactate temporarily. (See http://www.lydiardfoundation.org/news/pdfs/Snellcourirenglish.pdf.)

Clearly the maximum power output that can be maintained for a few seconds cannot be maintained even for 30 sec. A several minute effort is still in the range where a human is capable of power output that exceeds levels that can be sustained for much longer periods of time. The relative contributions of the available metabolic paths to energy generation for an maximal effort of a few minutes can vary widely depending on the individual, the level of normal activity, training or conditioning, dietary habits and adaptations, and the level of actual effort relative to the individual’s maximum capabilities over that distance or time. Anaerobic metabolism of glucose from glycogen is certainly one of the possible contributors. In fact, the limit to how fast any one individual can go for, say 3 min of “maximal effort” is probably still set by acidification caused by lactate accumulation (and carbonic acid from CO₂ produced) due to anaerobic glucose metabolism. As the anaerobic metabolism of glucose is very inefficient and would rapidly deplete stores, additional more efficient metabolic pathways will be tapped, most notably aerobic metabolism of fat and glucose. Another important contribution comes from the aerobic metabolism of the lactate (produced from anaerobic metabolism of glucose mentioned above). If lactate is being overproduced, some of its carbon will be further metabolized in the heart and muscles and converted to CO₂ through the citric acid cycle, and eventually breathed out, with most of the potential ATP from the glucose being realized eventually, even if not in the muscle of origin. At modest production rates, much of the lactate can be used aerobically and directly as fuel by the muscles, and is a preferred fuel of slow twitch and heart muscle. In addition to possibly being used by other muscles, this lactate is also taken up by the liver and converted back into glucose and then glycogen, and thus recycled. In short, it takes a lot more than a 3-minute burst of effort to substantially deplete glycogen stores. In fact, calculations show that the glycogen stores of a well-trained runner are sufficient to last for approximately 2 hours if glycogen is the exclusive fuel (and, incidentally, stored fat would last for about 59 hours [estimates based on glycogen and fat stores present in lean elite athletes]).

Thus, it is simply not true that there would be an urgent need to fully replenish severely depleted glycogen stores after a single episode of high-energy activity. The glycogen stores would not be significantly depleted (e.g., >50%); any of several available replenishment mechanisms would be sufficient to provide necessary restoration; and there is, in any case, no urgent need to provide complete restoration within 24 hours anyway.

This renders meaningless all of speculation in the post about the large amount of protein that would need to be consumed to replace the allegedly depleted glycogen. Let’s consider first, how the body actually uses its glycogen stores. Many authors tend to focus on how much total glycogen can be stored in muscles, how much activity that amount will support, and how much time is required to replace and completely refill the muscle glycogen stores. This way of thinking may be relevant when trying to achieve peak athletic performance for a particular competitive event, but this artificial effort would not be relevant to “normal” life and evolutionary pressures. In "normal" life, maximal effort may be required on occasion, but would be punctuated with adequate rest periods to allow recovery and maintenance of energy stores. Glycogen available to any given muscle for short intense effort is only that stored locally in that muscle—you can’t steal from other muscles. Similarly, once stored in the muscles, it remains there until used—it is not depleted beyond a certain level that is protected and maintained even after extensive exercise.

Even after an exhausting race, a person can still increase their efforts and sprint to the finish. A critical detail to remember is that lactate produced from glycolysis can be used to regenerate glucose and then glycogen, as well as enter the citric acid cycle and be used aerobically. Hence lactate is recyclable—glucose can be used anaerobically for a brief intense effort, then rapidly regenerated from lactate once there is a rest period. Under conditions of carbohydrate restriction or partial glycogen depletion, the body simply intensifies the recycling effort and favors use of fat for most energy needs. Only during periods of long and repeated exhaustive glycogen depletion would glycogen levels be dangerously low, and then the body would attempt to reserve them for emergencies, decreasing intensity of activity to levels supported by fat metabolism.

That said, the amount of glycogen storage for any given muscle is also “trainable” in that the amount of glycogen stored increases with increased use. A well-trained athlete may be able to top out his muscle glycogen stores at as much as three to four times that of a sedentary individual. And presumably, a paleolithic hunter is more similar to a modern athlete than to a couch potato. Further, the “normal” steady state condition for an active individual is probably not with glycogen stores full, but more like half full. This seems to be the condition measured for endurance athletes in steady state (i.e., several hours into a many-hour event or in everyday training. See Noakes, Lore of Running pages 101–102 and references therein). It may take a day or more of resting and relatively high carb eating to fully replenish glycogen stores to maximum capacity, but the half-full steady state can be maintained more or less indefinitely, and is fully capable of supporting most any activity that is needed. Further, at least for individuals adapted to fuel their activity primarily on fat, this steady state can be maintained with little or no carbohydrate consumption, and at levels of protein consumption that are modest compared to any levels that might overwhelm the kidneys.

A further point is that it is possible that this “half full” condition is optimal for health, in that muscles that are not topped out with glycogen are still hungry for more glucose, that is, they still express glucose transporters on their surface that are actively scavenging for glucose. This constant glucose uptake by hungry muscles would tend to keep blood glucose levels low, optimize insulin sensitivity and thereby keep insulin levels low, compared to the condition of the over-fed over-carbed SAD consumers. (See http://ajpendo.physiology.org/cgi/reprint/285/4/E729.)

As soon as liver glycogen starts to decrease, gluconeogenesis kicks in, and if adapted to fat burning, gluconeogenesis enzymes may be up-regulated. One can sustain aerobic activity (presumably using glycogen stores in addition to fat stores) for many hours and still have no measurable depletion of blood glucose levels! In fact, we routinely observe the opposite (elevated blood glucose after hours of running). Glycogen stores can thus be regularly replenished (at least partially- enough to call on in emergencies) as needed even during prolonged aerobic exercise, even when fasting, to support the needs of occasional anaerobic activity. As already noted, data indicates that trained athletes can maintain a steady state level of average glycogen stores that are approximately 50% of their maximum capacity. Put another way, during prolonged periods of inactivity, a trained athlete can store ahead approximately twice the “normal” levels of glycogen stores. (Note that even the “normal” levels are about twice those measured in sedentary humans.)

In the example given of hauling a buffalo carcass out of a ravine, this activity may involve some anaerobic activity, but it will necessarily stretch over an extended period of time and be completed primarily using aerobic metabolism. There may be brief bursts of high intensity effort as needed, and there may even be bursts of extreme effort for particular heavy lifting tasks, but on average the task will necessarily be completed with levels of effort that can be sustained over hours not minutes. We suggest that hauling out a buffalo carcass would not necessarily require a lot of glycogen, and even if it did, would not necessitate gorging on potatoes or other carb food to replenish glycogen stores. Perhaps the one situation outside of athletic competition that could force someone to put out maximum effort for as long as possible (and thus seriously deplete glycogen stores) is a fight (or flight) for life. These events presumably don’t occur in close succession, so the primary evolutionary adaptation would be to provide the capacity to sustain the necessary fight or flight long enough to survive the immediate crisis. An ability to fully recharge is not necessary and would not confer much less of a survival advantage.

In fact, it is often argued that the key characteristic of humans that makes them surprisingly competitive in the predator vs. prey world compared to animals that are nominally bigger, stronger, and faster is that humans don’t depend on their peak power output capabilities but instead on their ability to maintain lesser levels of output for very long times (as, for example, in a “persistence” hunt, where they literally outlast and outrun their nominally faster prey).

Other purported advantages of eating tubers cited in “Primal Potatoes, Part 2”:

1. Lower dietary protein/meat requirement, reducing the pressure for success in hunting large animals, and making it possible to feed more people (offspring) with each kill.

This seems to be a common misconception! Eating less carbohydrate means eating more fat, not more protein. And the hunting of large animals provides increased fat relative to smaller animal sources of protein. It is difficult to eat large amounts of protein, and most people find it almost impossible to eat too much protein. It is true, however, that tubers are easier to store for extended periods than meat (and meat fat) which must be more carefully prepared for long term storage, especially in warmer climates. Agriculture does enable more concentrated population centers and was probably a major driving force for the increasing urbanization of the world. However, it is not at all clear that the sort of monoculture version of agriculture that has come to dominate how we feed large populations is a positive step. In fact it is becoming increasingly recognized that we may be destroying the planet faster with mass agriculture than we ever did by overhunting.

2. Less burden on the liver for ammonia detoxification.

This is nonsense. Again, protein consumption tends to be self-limiting at levels well below anything that would present any significant burden to the liver (or kidneys).

3. Easier to avoid protein poisoning while at the same time maintaining greater glycogen stores.

Again nonsense. Protein poisoning is just not a serious risk. And it is not difficult to maintain more than adequate glycogen stores with very low carbohydrate consumption because glycogen stores do not need to be 100% full in order to provide adequate auxilliary anaerobic energy production.

4. Easier to maintain and increase lean mass in response to the stresses of high intensity activity, with a lower dietary protein requirement.

False! As anyone who has seriously tried a low-carbohydrate diet knows, it is much easier to maintain lean body mass without increasing excess fat storage if carbohydrates are minimized in favor of fats. And carbohydrate consumption always causes blood insulin levels to spike, which has a whole series of negative consequences. Arguably, from a public health point of view, the widespread adoption of higher-carbohydrate diets was the single worst event in human history that is the major cause of most of the so-called “diseases of civilization.” Building lean mass (muscle) is usually easier with adequate protein consumption. The key to maintaining it is to (1) make sure that you maintain sufficient nutrition so as not to catabolize too much of your own protein (which the body will do if other fuel sources are limited) and (2) to consume enough protein for muscle building and rebuilding/repair. (See for example http://www.bodybuilding.com/fun/md92.htm and references cited therein, which provides evidence that excessive carbohydrate consumption post-exercise actually inhibits optimal muscle growth and repair.)

5. Reduced pressure to hunt only the fattest animals by use of carbohydrate instead of fat to dilute the protein content of the diet; which greatly enlarges the pool of potential prey, increasing dramatically the amount of energy available for harvest.

Fat is good anyway! You should always be hunting for your fat needs as well as your protein needs. You just don’t need that much total protein. But you do need some protein, and high quality protein (i.e., the so called “essential” amino acids) is hard to get in sufficient quantity from non-animal sources.

In summary, while we certainly believe that humans likely ate tubers and other starchy vegetables (and eventually the New World potato) when they could be found, we see no evidence that that behavior conveyed any sort of evolutionary advantage beyond survival in times of limited food availability.

In Praise of the Little Muscles

The more I learn about how animal bodies achieve motion, the more impressed I am by the mechanical engineering that has been achieved by Mother Nature through some millions of years of evolution. Prosthetic limbs and robot arms that have been built to date by humans can’t come close to duplicating Nature’s exquisite designs. For example, I recently saw the latest personal robotics research coming out of Willow Garage. They’re doing interesting work, though as someone who has watched robotics research from the sidelines for 30 years or so, it’s clear that real progress is still slow, and we’re still a long way from giving Nature any serious competition, either from a physical performance point of view or from a computational intelligence point of view.

As someone who has never really studied anatomy in any detail, I also never fully appreciated just how many muscles are engaged in simple motions, what it takes to use and control them properly, and just how important some of those little muscles that we tend to ignore can be. There’s nothing like an injury to a minor muscle to teach you what their importance and function are.

My first experience with a “minor” muscle injury was some years ago. I tore my right piriformis muscle doing a lunge while fencing. (Look up all the muscles mentioned here at Get Body Smart.)

The Piriformis is a little muscle under the Gluteus Maximus that is used for leg rotation at the hip. I knew I’d done something bad at the time, but I didn’t have much in the way of acute pain and mostly just ignored the injury. Some months later I was experiencing chronic but vague hip discomfort and a sense of looseness in the joint. A good physical therapist was able to diagnose the problem from my assortment of vague symptoms, and having diagnosed the problem (the muscle at that point was seriously knotted), it was a straightforward, if slow, process to undo the damage and get the muscle back to normal function.

Apparently, there aren’t a lot of nerves in these small muscles compared to the major skeletal power muscles, and one can’t necessarily feel the damage unless you find the muscle and start to really knead it—something that can be hard to do for a muscle that is hidden behind something much bigger. It took a year or so of regular rubbing (the corner of a countertop or table
worked great!) before the muscle stopped acting up from time to time.

I had a similar experience with the upper part of my right Soleus muscle. In that case the injured muscle was hidden underneath the big calf muscle (the Gastrocnemius). The Soleus contributes to flexing the foot, and thus is commonly stressed by running.

Again, I was experiencing vague calf pain while not having any obvious pain in the big muscles. Once identified, Soleus muscle damage can be easily massaged by lying on one’s back and resting the lower leg on the opposite bent knee. Move the lower leg back and forth over the knee with the Gastrocnemius fully relaxed, and you should easily be able to find any tender or knotted
areas. Even though I don’t have any particular damage problems with this muscle now, I still find it a useful post-run massage to do—the Soleus muscles often take a beating on a long hard run. Also, while I generally subscribe to the theory that warming up slowly is far more important than stretching (which can be downright counter productive, promoting rather than preventing injury), I do find it useful to stretch the Soleus muscles by flexing the foot up with the leg straight (which also stretches the Achilles tendon and attached structures).

My most recent experience was the most dramatic yet. It introduced me to yet another lesser-known muscle that I had been completely unaware of and left me unable to run for several weeks! After running many hundreds of trail miles over rough terrain with little more than routine sore muscles and the occasional minor bumps and scrapes, I managed to injure myself on the track! I was well warmed up and had just run a 7-minute mile (about as fast as I can go for that distance). After a lap or two of cooling down, I decided to sprint for 100 m or so. Mistake! I almost never really sprint, and I don’t really have well-developed sprinting muscles and technique. Again, I knew I’d hurt something, but I wasn’t quite sure what. A couple of days later, about seven miles into a twelve-mile trail run, I landed slightly wrong on the injured leg going downhill, and felt a sharp pain in my knee. After the acute pain subsided, I was suddenly unable to run at all, though I could still walk with minimal limping and was able to walk the rest of the way.

It turns out that the damaged muscle this time was the Popliteus. (And no, there was not any ligament or cartilage damage at this point.) This seeming unimportant muscle is located immediately behind the knee running diagonally across the leg from the outside (at the top) underneath the top of the Grastocnemius muscle. It’s pretty hard to find even when acutely injured, but it can be massaged (carefully! there are other sensitive structures nearby) if the Gastrocnemius is fully relaxed. The Popliteus muscle serves at least three important functions. First, though it has very little power being very small, it is the first muscle that fires when you bend your knee from a fully-extended position. Second, it helps hold the knee joint together. Third, it helps prevent you from “hyperextending” your knee (going past the normal maximum extension—straight leg). Lacking a normally functioning Popliteus muscle is surprising debilitating! The knee joint just doesn’t work right. Most joint motions involve multiple muscles that are fired in an exquisitely timed sequence to achieve the full action. The Popliteus fires first
for knee bending, and without it, your timing falls apart. The joint looseness and potential for hyperextension leave the joint cartilage vulnerable. My attempts to continue at least light running caused acute pain to develop at the medial meniscus, the main piece of cartilage padding the knee joint on the inside. The weak Popliteus muscle allowed excessive pinching of the
cartilage, especially on impact. In effect, the Popliteus muscle also plays a key role in the sequence of muscle firing that provides shock absorption as you land on your foot when running. This particular problem is peculiar to running; walking and bicycling were possible with little or no pain. (With most knee injuries, bicycling is painful, since it tends to put significant stress on the knee.) Of course, as with any injury, any limping or other change of gait, whether conscious or not, tends to stress other muscles that are compensating for the injured muscle in unusual ways. In this case, I got quite sore in the adductors in the opposite leg!

The good news is that, while recovery has been slow and I was unable to run much at all for a few weeks, no lasting damage occurred. I walked and bicycled more, and eased back into running with shorter, slower distances, being particularly cautious on the downhills. Ibuprofen and a simple knee brace also helped enable a little more activity sooner, and I managed not to lose too much conditioning. I also followed the recommendation to take a Glucosamine/Chondroitin supplement.

I also took advantage of the slower shorter distances to start to switch over to more “toe” running (landing on the ball of the foot rather than the heel). This reduced the impact on the medial meniscus, again allowing me to run more sooner, though it has required developing a slightly different set of running muscles. (You use parts of your Gastrocnemius muscles more for shock absorption when landing on the ball of your foot than you do when landing on your heel.) I’ve been experimenting with Vibram Five-Finger shoes, which I like a lot for running, and since these shoes have no padding whatsoever, landing on your heels
is not such a good idea, at least on rough surfaces, so I was already motivated to change my running style. But I’ll postpone a detailed report on these unusual shoes for another post.

Final notes: (1) If you’re wondering whether the new shoes caused or exacerbated the injury (I was wearing them when it happened), I can’t prove definitively that they didn’t, but I’m pretty convinced that there’s no connection. I’ve tried various shoes since and keep coming back the the Five Fingers as the shoes that cause the least stress post-injury, which is certainly suggestive that they couldn't have caused the injury in the first place. (2) I now know how to go about diagnosing problems like those described above without consulting medical professionals. There are, of course, a lot of good resources on the web that can help you sort through any specific problem. I started out this time with a Google search on “knee pain” and found a number of good diagnostic aids including a paper by Calmbach and Hutchins oriented at Family Physicians that helped me sort through what was plausible and what was not, and I am convinced that I have correctly described the injury. Of course, I have to add the usual sort of disclaimer that you shouldn’t “try this at home” and should always seek competent medical advice when needed. I just happen to have a certain tendency to do things myself anyway, and I’ve come to believe that, in many cases, I can do as well or better than any professionals I might try to hire to help me.

David

Third Time’s the Charm? Quicksilver 50K

Being disgusted and frustrated with missing cutoff times in two consecutive races, I couldn’t possibly take the hint, and instead signed up for another one! (against David’s better judgment). It seemed a shame to let all this hill training go to waste, so I convinced David that I was doing another with or without him, and luckily he decided to come too. This time it was the Quicksilver 50K in Almaden Quicksilver County Park in San Jose. We had some vague thoughts about moving up to the 50 mile after returning to the 50K point, which tacks on an out and back to get the extra miles. Supposedly, you can opt up to the 50 mile but not down from the 50 mile to the 50K. Not wanting to take another chance on missing cutoffs or just having a bad day with the heat, we signed up for the 50K with the possibility of continuing on. Turns out, 50K was quite enough on this sunbaked day, and I was happy enough to stop with that.

The picture (pre-race) below was swiped from Donald Buraglio’s site. (Thanks Donald!) David is #117 (currently ~187lbs, down from 220lbs a year and a half ago). Fifty mile winner Chikara Omine is #75. Jean Pommier and Mark Tanaka with backs to the camera. Many other folks I don’t recognize—apologies). For more pictures and a report on the full 50 mile race, see Donald’s post.

The race started at 6 am, before the sun’s rays began to heat us up. We climbed a few initial hills on a fire road, mostly walking where I was, then ran down the road again and off onto a wooded trail following a meandering stream. This section was shaded as the sun rose, and was full of lovely gentle inclines and downhills. At one point I jumped over the stream crossing rather than climbing carefully down and back out again, and strained something in my foot—I thought it was broken it hurt so much! but it gradually settled down. I need to remember that I’m not 20 anymore! We came out onto fire roads again and more uphills, longer though still gradual and runnable, and still mostly shaded and cool.

Reaching the first full aid station (Dam overlook), the sun had only just peaked over the hills. More fire roads with runnable ups and downs, mostly in the shade, and the second aid station was upon us, more brightly lit and exposed to the sun. These volunteers looked to be getting warm. By this point the runners were pretty spread out. A few people had gone out too fast and were slowing down, and I was able to pass a few folks. We came upon Sean Lang and Gordy directing traffic, and soon there was a long fast downhill section leading back to the dam overlook aid station. I tried to make up for my slowness on the uphills here, and to compensate for having to climb this hill again on the way back. This was now mile 19—my energy levels usually start to fade here, and that’s what happened this day as well.

The next section was not difficult and had a fair amount of downhill, but I was just hot, tired and thirsty, and even the downhills felt bad. It seemed to take forever to finish the 4 mile loop, then climb once more to the Dam overlook aid station. I filled up on fluids and wandered off sipping coke on lots of ice. The long downhill became the long uphill as we retraced our steps, and I managed to muster a run here, but it was intermittent. Finally, there was Sean and Gordy again, making sure we didn’t get lost, then a bit more climb and another long downhill to my last aid station. I was surprised to see I had caught someone, and was inspired to try harder this last section. Only 4 miles to go—how hard could it be? It turned out to be the most difficult part of the course! Soon we were climbing again, short steep hills I had read, but what I found were long steep hills almost impossible to climb at this point. My shin muscles were cramping and I had to walk on tip toe to keep the muscles from cramping worse. I felt a shiver and was sure heat stroke was near too. The hills just kept coming and coming until you forget you thought you’d be finished by now. Finally we came upon the final downhill dash (for those who still had their legs) and the finish.

At this point, there was no question about going out into that heat again. I had made the cutoff time for the 50-mile, but it was miserably hot out there on that trail, and the thought of crawling up those last few hills again in the heat was more than I could take. It turned out David had had enough too, and he brought me ice as soon as I crossed the finish line.

And what a spread at the finish! There was watermelon, strawberries, meats on the grill, salads, desserts. They even had a generator for power and a full sized refrigerator (now that's serious advance planning) with ice cream, and they filled ice cream requests to order (I had ice cream with strawberries). It was fun hanging out and enjoying the food with fellow racers. I got to visit with Barb Elia and Christina Brownson, and a whole bunch of other folks whose names I forgot in post-50K brain fog. I also got to run for a while with Janice O’Grady, one of the founders of the event who returned from Colorado to run it. I talked with Mark Tanaka for the first time (having one of his usual hectic race mornings), as well as Simon Mtuy and Jean Pommier. The 50-mile winner, Chikara Omine was amazingly approachable and gracious, though a superstar already at 26 years old. See Mark Tanaka’s interview. And I finally got to see Bev Anderson-Abbs in person rather than merely watch her shoot by (and even talked with her!). She looks like a consummate athlete—lithe and well muscled. Maybe someday…

I was able to keep my heart rate more consistent than at Diablo or Miwok, which could be a sign of some improvement in pacing. I typically start a race between 150 and 160 bpm, and hold that for a few hours, but the HR gradually drops for unknown reasons over time, down to the 140s, and when I’m really dragging or cold, into the 120–130s. It’s an interesting chicken and egg question—does heart rate decline because of fatigue, or does fatigue increase because of HR decline (the heart can’t deliver sufficient oxygen)? The hints I’ve gotten from questioning coaches is that as glycogen is depleted, there is less energy for anaerobic energy production, and the aerobic heart rate is much lower (see the Maffetone formula, that works out to about 135–140 bpm for someone my age and condition. For other lucky souls, it might be much higher and hence they can blow by me without even breathing hard). I’ve been looking through the research literature, but I still don’t understand the connection between exercise intensity, muscle glycogen reserves and heart rate, but presumably it has something to do with blood lactate levels. This time I also didn’t bother with Vespa, though I had tried it previous races. I think if anything, my energy levels were maintained better than usual, but that may have more to do with pacing and the course.

We decided to experiment more seriously with David’s carb-free race nutrition approach, and have him try and run at his own pace to see if he’d bonk with no carbs. So David started out faster and I didn’t see him the rest of the day until the finish. (and I was lonely…) I carried all kinds of food with me, most of which I never managed to eat. Funny how that always happens. I started out with a bottle of full strength Cytomax, but it got diluted as we went along with the watered down stuff. I forgot one of my water bottles, and so never had the ability to carry extra water—when it grew hot, that became a problem. I ended up eating a few gels, few bites of potato and cups of coke, and a couple ounces of roast beef that I brought along in my pocket. Maybe 500 calories in but ~3000 out (walking uses less than running, but 5500 feet of climbing must count for something).

I was happy to be 54th out of 75 finishers and 5th out of 7 in the 50–59 women (not completely back of the pack for a change) in this field that included 19 first ultra runners (many of whom were faster than me!)

David finished successfully without using any carbs in 32nd place overall (and 7th out of 12 in the 50–59 age-group men). He was running with a heart rate generally in the 150s, substantially above the mid 130s that he typically maintains at my pace, and well above his purely “aerobic” effort. Toward the end he reported distinctly slowing at the same heart rate, but that was probably due to a combination of increasing heat and steeper trails and calf cramps. (The hardest hills, both up and down, in this race are at the very end!) He said he couldn’t sit down to rest for about an hour after the race because his legs kept cramping! It was definitely hot there at the end, and I was glad I managed to keep the cramps at bay as well as I did.

The aftermath: the lung irritation and asthma from before Diablo finally disappeared for good (and hasn’t come back thankfully). My foot (that I thought might be broken) was tender and slightly swollen for a few weeks, though I kept running on it anyway, but mostly has settled down again (though the bones look thicker now—got stronger?). Some hot spots on the balls of the feet, but no blisters (thanks to Drymax socks!)

Carbohydrate Needs of the Endurance Athlete

There is increasing recognition among endurance athletes that at least some fat and protein consumption is beneficial for athletic activity extending beyond about 3 hours. Further, most athletes understand that increased protein consumption post-event is valuable for speeding recovery and reducing discomfort in the following day or two. But most still insist that you
absolutely need plenty of carbohydrates before, during, and after the activity to achieve peak performance, to avoid “crashing” or “bonking,” and to recover quickly. Aid stations are typically stocked almost exclusively with carbohydrates, especially sugars (jelly beans, cookies, M&Ms) and simple starches (potatoes, potato chips, pretzels, gels), with the addition of some limited fats and protein only in the longest events. I’d come to increasingly suspect that this advice is probably wrong, and especially wrong for anyone who has adopted a low-carbohydrate diet and made the physiological adaptation to fat-burning to fuel exercise. I can now add my own anecdotal experience.

I have been restricting my average carbohydrate intake to an estimated 20% or so of calories for about 10 months now. At the same time I have been increasing my exercise level and capability substantially, to the point where I have now completed several 50K running events and one 50-mile event. At first, running seemed harder without the usual high level of carbohydrate intake, but over a few weeks it got steadily easier until fairly suddenly it was much easier. I was able to run uphill again (which I hadn't been able to do for a while); I found my routine breathing rate during comfortable sustained running had slowed by at least a third; I could easily go longer without any food intake besides water.

Nevertheless, for my first 50K event, I consumed more like a 50% carbohydrate meal the night before, and consumed the usual assortment of provided aid station food, avoiding only the simple sugars. The running went well enough, though my weight jumped a few pounds the next day and took three or four days to return to “normal.”

Since then I have been steadily cutting back on carbohydrate supplementation during the run. I did the 50-miler on mostly protein and fat with only a modest amount of carbs thrown in. Then I tried a strict low-carb 50K run, using only a “protein shake” (my own brew of whey protein, soy protein, milk, cocoa, almond meal, and walnut oil) for the entire distance. It worked great! I had steady energy throughout the event (no ups and downs) and was still feeling strong at the end to the point where I did not participate in the post-event food and was happily running around on the beach where the event ended. (The day-after weight gain still occurred; apparently that's not a carbohydrate effect.) So my conclusion is that all this carbohydrate is not needed for successful endurance!

There’s still a question of peak performance. Do you need the carbs and the associated blood glucose spike to do your absolute best? Can you go faster with carbs than without? Does it matter if you’re planning short events (sprints, strength events, etc.) rather than longer endurance events? I don’t know, but I’m increasingly favoring the hypothesis that you don’t actually need much carbohydrate at all once your body is adapted to using fat as its primary fuel.

There are at least a handful of papers related to this topic. These papers all support the idea that only limited amounts of carbohydrates are necessary or even desirable for endurance athletes. See, for example:

Larson-Meyer et al., “Effect of dietary fat on serum and intramyocellular lipids and running performance,” Med Sci Sports Exerc. 2008 May;40(5):892–902 reports 3-day crossover trials of endurance trained runners with low fat (10% fat LFAT) or medium fat (35% fat MFAT), and concludes that “despite approximately 30% lower IMCL [intramyocellular lipids] 0.220±0.032% LFAT, 0.316±0.049% MFAT; P = 0.045) and approximately 22% higher muscle glycogen stores at the start of performance testing (P = 0.10), 10-km performance time was not significantly different following the two diet treatments.” Lipid profiles suggestive of cardiovascular disease were associated with the high-carbohydrate-low-fat diet, and the authors concluded that “even short-term consumption of a low-fat diet may unfavorably alter serum lipids, even in healthy, endurance-trained runners.” (Note that this study did not allow time for adaptation to the different diets, so glycogen and lipid levels in the muscle cells are due only to the acute diets tested);

Vogt et al., “Effects of dietary fat on muscle substrates, metabolism, and performance in athletes,” Med Sci Sports Exerc. 2003 Jun;35(6):952–60, which studied the effect on trained athetes of a high-fat (53% fat) or high-carbohydrate diets (17% fat) for 5 weeks in a randomized crossover design, found that maximal power and vO₂-max during an incremental exercise test to exhaustion were not different between the two diet periods, total work output during a 20-min all-out time trial (298±6 vs 297±7 W) on a bicycle ergometer as well as half-marathon running time (80 min 12 s ± 86 s vs 80 min 24 s ± 82 s) were not different between HF and LF. Blood lactate concentrations and respiratory exchange ratios (RER) were significantly lower after HF than after LF at rest and during all submaximal exercise loads. The authors concluded that “muscle glycogen stores were maintained after a 5-wk high-fat diet period whereas IMCL content was more than doubled. Endurance performance capacity was maintained at moderate to high-exercise intensities with a significantly larger contribution of lipids to total energy turnover”;

Lambert et al., “High-fat diet versus habitual diet prior to carbohydrate loading: effects of exercise metabolism and cycling performance,” Int J Sport Nutr Exerc Metab. 2001 Jun;11(2):209–25. No changes were observed in circulating glucose, lactate, free fatty acid (FFA), and b-hydroxybutyrate concentrations during exercise. However, mean serum glycerol concentrations were significantly higher [indicating mobilization of fat stores with glycerol release] in the HFD-CHO trial. The HFD-CHO diet increased total fat oxidation and reduced total CHO oxidation but did not alter plasma glucose oxidation during exercise. By contrast, the estimated rates of muscle glycogen and lactate oxidation were lower after the HFD-CHO diet. The HFD-CHO treatment was also associated with improved time trial times (29.5±2.9 min vs. 30.9±3.4 min)[150 min cycling at 70% vO₂-max followed by a 20 km time trial] for HFD-CHO and CTL-CHO. They conclude that “high-fat feeding for 10 days prior to CHO-loading was associated with an increased reliance on fat, a decreased reliance on muscle glycogen, and improved time trial performance after prolonged exercise”;

Leddy et al., “Effect of a high or a low fat diet on cardiovascular risk factors in male and female runners,” Med Sci Sports Exerc. 1997 Jan;29(1):17-25, which notes that “restricting fat intake may compromise endurance performance and that increasing fat intake may improve endurance performance,” and concludes that “a 42% fat diet maintained favorable CHD risk factors in female and male runners whereas a 16% fat diet lowered Apo A1 and HDL-C and raised the TC/HDL-C ratio”;

Horvath et al., “The effects of varying dietary fat on performance and metabolism in trained male and female runners,” J Am Coll Nutr. 2000 Feb;19(1):52–60, which concludes that “runners on a low fat diet consume fewer calories and have reduced endurance performance than on a medium or high fat diet [and] a high fat diet, providing sufficient total calories, does not compromise anaerobic power.”