As I read their reply, I don’t see that they addressed the fundamental point of my post, which is that people eating low carbohydrate diets don’t have the same anaerobic capacity as people eating higher carbohydrate diets (although not necessarily “high” carbohydrate diets) that allow for greater glycogen storage. As I noted in my original post, even scientists who advocate ketogenic diets (e.g. Phinney, 1) accept this as an established fact and have demonstrated it themselves in controlled studies on keto-adapted athletes.
Cynthia and David report that one of my links to a reference did not work, so they started off their rebuttal by searching PubMed for the article. In such cases, I suggest asking me to correct it, or provide another avenue, rather than picking another article that has Fournier as an author, and assuming, perhaps wrongly, as in this case, that you have the right article in your hands.
In my post, the dead link referred to this article:
Fournier et al, Post-exercise muscle glycogen repletion in the extreme: effect of food absence and active recovery, International Society of Sports Nutrition Symposium, June 18-19, 2005, Las Vegas NV, USA
This paper includes this quote to which I referred:
“In fact, we store just enough glycogen to sustain our energy demands for only a few hours of intense aerobic exercise (Gollnick et al., 1973; Ivy, 1991), and so little glycogen is stored in our muscles that close to a third to half of these stores can be depleted within a few minutes of a maximal sprint effort (Gollnick et al, 1973; Fairchild et al., 2003). As a result, active individuals are at increased risks of experiencing a fall in their ability to engage not only in intense aerobic exercise (Ivy, 1991), but also in short sprint effort under situations eliciting fight or flight responses (Balsom et al., 1999; Fournier et al., 2002).”
Fournier et al here point out that even individuals on a mixed diet can experience declines in either intense aerobic or anaerobic (including fight or flight) performance due to glycogen depletion. It is reliably reproducible in experiment, so no one doubts it. I took this as the basis of my argument that human ancestors who did use tubers for starch intake would have had a selective advantage over those who did not, by having superior performance both in hunting related activities and in escape from predators.
Cynthia and David don't believe that glycogen depletes so quickly as claimed by Fournier et al. Let's take a look.
How rapidly does glycogen deplete?
Cynthia and David contend that the statement that close to a third to half of glycogen stores can deplete within a few minutes of a maximal sprint effort is “an exaggeration.” I disagree. Fournier et al make this statement based on research on glycogen depletion in man, some of which Lyle McDonald discusses in his book The Ketogenic Diet: A Complete Guide for the Dieter and Practitioner (Morris Publishing, 1998, pp. 120-123).
McDonald notes that researchers have collected data on glycogen levels under different conditions, including ketogenic diets, which I will now summarize:
• Supercompensated glycogen levels reach 175 mm/kg in trained athletes on high carbohydrate diets.
• Athletes on mixed diets have levels of 110-130 mmol/kg.
• Normal individuals on mixed diets have 80-100 mmol/kg.
• Normal individuals on ketogenic diets and doing no anaerobic training have 70 mmol/kg.
• Exercise performance will be impaired at 40 mmol/kg
• Exhaustion occurs at 15-25 mmol/kg.
• Protein gets converted to fuel during exercise when glycogen falls to 40 mmol/kg or below.
As McDonald points out, researchers in two studies (2, 4) have determined the rate at which glycogen gets consumed during such efforts. At 70% of maximum weight, both studies found a glycogen depletion rate of 0.35 mmol/kg/second of work performed. Translated to seconds:
• 30 second effort, 10 mmol/kg depleted
• 40 second effort, 14 mmol/kg depleted
• 50 second effort, 17 mmol/kg depleted
• 60 second effort, 21 mmol/kg depleted
• 70 second effort, 24 mmol/kg depleted
• 80 second effort, 28 mmol/kg depleted
• 90 second effort, 31 mmol/kg depleted
So, with this data you can see how an intense effort could deplete one-third to one-half of stored glycogen, depending on starting stores. If starting stores are 80 mmol/kg, and you engage in a 90 second lifting effort at 70% of maximum resistance, this will deplete 31 of 80 mmol, or 39% of glycogen, i.e. one-third to one-half.
Can recycled lactate replenish glycogen?
If an individual consumes no carbohydrate following glycogen-depleting exercise, a small amount of glycogen will get resynthesized from lactate. Now for some more numbers (McDonald cites Pascoe and Gladden, 2):
• Production of 1 mmol of glycogen consumes 2 mmol of lactate.
• Only about 20% of the lactate generated during anaerobic activity like weight training (bison lifting) can get converted back to glycogen.
• Lactate levels in muscle during intense anaerobic activity typically reach only 10-15 mmol, with a maximum of 21 mmol.
So, at 2 mmol of lactate per 1 mmol glycogen and an efficiency of only 20%, the lactate recycling would reconstitute only at most 2 mmol/kg of glycogen, an insignificant amount compared to original stores.
Low carbohydrate dieting does not make this process more efficient. One study looked at the rate of resynthesis of glycogen following resistance training absent carbohydrate intake, and found a rate of 1.9 mmol/kg/hr, with a total (maximum) regeneration of 4 mmol/kg (2).
I referred to the following carcass-carting episode as an example of anaerobic activity fueled by glycogen:
“In 1805, the Lewis and Clark expedition witnessed an Indian bison kill ….A small herd was stampeded over a cliff into a deep, broad ravine. As the bison fell one on top of the other, dazed and injured, hunters killed those on top with spears; the others were crushed and suffocated underneath. The ravine was twelve feet wide and eight feet deep; most of the bulls weighed over a ton, yet a team of five Indian hunters pulled nearly all the bison out of the ravine onto level ground for butchering.” (3)
About this Cynthia and David say:
“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.”
First, this was not “a” bison carcass, it was a small herd. Next, each bison weighs 1500 or more pounds, the bulls over a ton, and only five men completed the task. The carcasses were hauled out of the ravine intact, for butchering on level ground. If all members of the team participated in lifting each carcass, this means each man had to deadlift and carry up out of a hole at least 300 and at times 400 or more pounds.
Cynthia and David say that this would be completed “primarily using aerobic metabolism.” I see it differently. Let me use a more contemporary example. Although a strength training routine consisting of 15 hard sets of 30-60 seconds each may involve rests of 3-5 minutes between sets, and aerobic metabolism would dominate during the rest periods, I would not say—and I don’t believe any exercise physiologist would argue-- that a strength training routine is “primarily” fueled by aerobic metabolism just because "on average” the level of effort could be sustained “over hours” by the insertion of rest periods.
The activity of interest here consists of lifting bison, not of the rest periods between lifts, and the question is, does this lifting deplete glycogen or not? The answer is, yes it does, regardless of rest between efforts.
Cynthia and David “suggest” that this “would not necessarily require a lot of glycogen…” Let's take a look.
As an experienced lifter, I believe that I can reasonably assume that the men lifting those bison out of the ravine were lifting not more than 70% of their maximum capacity, because they most likely would not have been able to repeat 10 or more such lift-and-haul operations (10 sets of the same movement) in one session if the resistance had been higher than 80% of their maximum.
OK, now let us generously assume the herd consisted of only 10 animals, and moving each animal out of the hole required only 30 seconds of intense effort (doubtful given the task, but roughly equivalent to a 5 to 8 repetition set of deadlifting). The result would be a depletion of 100 mmol/kg of glycogen. That seems like a lot to me, given that normal glycogen stores on a mixed diet amount to not more than 100 mmol/kg, and stores on a ketogenic diet amout to only 70 mmol/kg.
Now above I noted that research has demonstrated that in the absence of post-effort carbohydrate ingestion, lactate recyling only replenishes a maximum of 4 mmol/kg. So you hunt on an empty stomach, fasted for more than 16 hours, which already depletes your glycogen by 50%. Then you help lift 10 bison—your portion amounting to at least 300 pounds--out of a ravine, which would deplete something like 100 mmol/kg of glycogen. You then rely on lactate recycling to “replenish” your stores, and you end up with 4 mmol/kg—way below the exhaustion and impaired performance level. You can see that you will definitely have need for some substrate other than recycled lactate for replenishing glycogen.
Even if I cut the depletion estimate in half, we still have a scenario in which 50 mmol/kg gets depleted, leaving a person with normal stores (due to a mixed diet) at a level of 50 mmol/kg, and a person on a ketogenic diet with only 20 mmol/kg—still below the level of exhaustion. And the lactate recycling still only producees 4 mmol/kg, nowhere near enough to replenish even a third of the original stores.
The need for a substrate
Absent dietary carbohydrate, the only way out of this would consist of converting either endogenous (lean tissue) or exogenous (dietary protein) amino acids into glycogen, at a rate of 1 g protein for each 0.7 g of resulting glycogen. This is where my calculations in Primal Potatoes, part 2, come in.
Cynthia and David state “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.” I did not see anywhere in their discussion any mention of the substrate needed for replenishing glycogen. It does not magically replenish itself out of thin air. Cells have to have glucose to make glycogen, and the glucose has to come from something else: dietary glucose, dietary protein, body protein, or lactate. I just showed that lactate can’t supply enough glycogen to replenish what would get spent in this type of effort. Therefore, the body will use dietary or body protein for the task, in the absence of dietary carbohydrate, because it will replenish glycogen at the expense of muscle mass, since it is definitely more important to be able to run from a predator than to have an abundance of muscle.
Gorging on potatoes?
Cynthia and David say that even if this bison lifting would deplete glycogen, this “would not necessitate gorging on potatoes or other carb food to replenish glycogen stores.” I would like to know where in any post I have advocated “gorging on potatoes or other carb food,” or stated that our ancestors did this?
In my original post, I based all my calculations on replenishing only one-third of maximum glycogen stores (i.e. about 133 g), not on filling glycogen stores to the maximum. I agree with them that keeping the stores somewhat empty has advantages—that is why I calculated for refilling only one-third. To replenish one hundred thirty-three grams of glycogen would require only 133 g of dietary starch, only 532 calories as starch, 26% of a 2000 calorie diet. If gotten entirely from sweet potatoes, you would consume 16 ounces of sweet potato. Since most people consume three to five pounds (48 to 80 ounces) of food daily anyways, I would not classify this as “gorging on potatoes.”
Advantages of dietary carbohydrate
Cynthia and David take issue with my suggested advantages of using tubers. I suggested that consumption of tubers would “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.” They seem to think I expressed a “misconception” that eating less carbohydrate means eating more protein, not more fat. Well, besides the fact that eating very little carbohydrate does most certainly increase protein requirements (see below), they missed my point, which is that if you eat tubers, your total requirement for meat (the reason I used “protein/meat”) will reduce because you will now be using a plant food to supply some of your calories and glucose and to dilute protein.
In connection with this, I suggest reading “Energy Source, Protein Metabolism, and Hunter-Gatherer Subsistence Strategies,” in which Speth and Spielman point out that observers recorded recent aboriginal hunters in temperate, subarctic, and arctic habitats having difficulty meeting caloric requirements in late winter and early spring due to the decline in fat stores on ungulants making only lean meat available (5). Very likely Paleolithic hunters had similar difficulties.
Native hunters would at those times abandon a kill consisting of lean meat, despite feeling hungry and having invested considerable energy in the hunt of it, because they knew protein poisoning could occur. If these hunters had a plant source of carbohydrate (or fat), they would not have had to abandon their lean kills, which would have improved the efficiency of their hunting (i.e. less waste). It seems clear to me that this would confer an adaptive advantage. After all, would it not be better not to have to waste hunting effort (energy) on useless meat (because too lean), and would not having enough food confer an advantage over starvation?
Hunter-gatherers certainly thought so—and they weren’t averse to eating carbohydrate instead of fat in lean times. As Speth and Spielman note, “Hunter-gatherer exchange of meat with horticultural populations in return for carbohydrates is documented for many areas of the world” (5).
I also offered that having carbohydrate in the diet would reduce the burden on the liver for ammonia detoxification. They say “this is nonsense.” Well, I happen to believe that the burden on the liver will in fact vary according to the amount of protein consumed. I find it difficult to understand why anyone would call this nonsense. If I make an organ do more work, doesn’t that increase the burden upon it? Let me put it another way: If I make you do more work, doesn’t that increase your burden?
Cynthia and David say “Protein poisoning is just not a serious risk” and state that “protein consumption tends to be self-limiting at levels well below anything that would present any significant burden to the liver.” How then do they explain this report from Randolph B. Marcy in the winter of 1857-1858 , quoted by Speth and Spielman:
“We tried the meat of horse, colt, and mules, all of which were in a starved condition, and of course not very tender, juicy, or nutritious. We consumed the enormous amount of from five to six pounds of this meat per man daily, but continued to grow weak and thin, until, at the expiration of twelve days, we were able to perform but little labor, and were continually craving for fat meat.”(5)
Five to six pounds of meat supplies 560 to 672 g of protein daily, an amount that provides more nitrogen than the liver can convert to urea in a day (6). Since Marcy and his team got weak and thin on it, this illustrates that man can consume protein at levels that can burden the liver. If not so, no one would have ever experienced “rabbit starvation” and protein poisoning as referred to by Stefansson (quoted in Speth and Spielman):
“If you are transferred suddenly from a diet normal in fat to one consisting wholly of rabbit you eat bigger and bigger meals for the first few days until at the end of about a week you are eating in pounds three or four times as much as you were at the beginning of the week. By that time you are showing both signs of starvation and of protein poisoning. You eat numerous meals; you feel hungry at the end of each; you are in discomfort through distention of the stomach with much food and you begin to feel a vague restlessness. Diarrhoea will start in from a week to 10 days and will not be relieved unless you secure fat. Death will result after several weeks” (5)
In short, protein poisoning presents a serious risk, well known to aboriginal hunters, who would abandon lean meat to avoid it, despite having spent an enormous amount of energy hunting it down while starving.
Cynthia and David also claim that my statement that eating tubers would make it easier for a hunter to maintain and increase lean mass in response to the stresses of high intensity activity, with a lower dietary protein requirement, is “False!”
I guess they have never heard of the very well-established protein-sparing effects of dietary carbohydrate. Adding carbohydrate to a carbohydrate-free or very low carbohydrate diet reduces the amount of protein required for maintenance of lean mass, by supplying an alternative source of glucose. Absent dietary glucose, the liver generates glucose for maintaining normal blood glucose levels by gluconeogenesis, which is the conversion of amino acids into glucose. If you supply glucose directly, the liver will reduce gluconeogenesis, which reduces the use and need for dietary protein as a glucose source. This in turn means that the individual can maintain lean mass on less dietary protein. Simply put, the less dietary carbohydrate you ingest, the more protein you must ingest (enough for maintenance of lean mass plus some for generating variable amounts of glucose).
Low carb doesn't work magic
Let me repeat, low carb diets do not work magic. They do not enable the body to create blood glucose or glycogen out of thin air. They do not entirely eliminate the need for glucose, they just shift the individual from use of dietary glucose to endogenously produced glucose generated by gluconeogenesis (the reason for the high blood glucose they find after runs). They do not magically increase the efficiency of recycling of lactate into glycogen. They do not make it possible to consume unlimited calories without gain of body mass. They do not cause body fat to evaporate independent of energy expenditure. They do not eliminate the need to ingest essential micronutrients. They operate under all the same physical and biochemical laws as high carbohydrate diets.
On another topic, Cynthia and David state: “And carbohydrate consumption always causes blood insulin levels to spike, which has a whole series of negative consequences.” I don’t know if they have read “An insulin index of foods: The insulin demand generated by 1000 kJ portions of common foods” (7). This project demonstrated that protein-rich foods also cause insulin levels to rise, due to insulin also having a function of clearing amino acids from the blood stream. The insulin scores for beef and fish exceed those for several high carbohydrate foods (white pasta, brown pasta, porridge) and are comparable to others (brown rice, whole grain bread). While in general it is true that limiting carbohydrate reduces insulin responses, I would caution anyone against stating broadly that “carbohydrate consumption always causes blood insulin levels to spike,” without specifying what type of carbohydrate. Since dietary protein also causes release of insulin in amounts comparable to some carbohydrate sources, I suggest taking care not to assert that only carbohydrate causes insulin "spikes."
As another relevant aside, short-term, high intensity exercise also causes a “spike” in blood glucose levels along with an increase of insulin levels to 60 microU/ml, a 2-fold increase over resting values (2). Does this spike have “a whole series of negative consequences”? No. This spike has the function of promoting conversion of blood glucose into glycogen, an essential function for preserving fight or flight capacity. Not all spikes of insulin cause the sky to fall.
Finally, I suggest distinguishing between temporary spikes in insulin, and chronic hyperinsulinemia. The undesired effects of insulin arise from chronic hyperinsulinemia, not temporary rises in insulin levels, so long as those rises quickly subside.
To end, I will quote Speth and Spielman:
“The greater protein-sparing capacity of carbohydrate under conditions of marginal calorie or protein intake may also help to explain why hunter-gatherers in the early Holocene began to invest time and energy cultivating plants, despite the meager returns many of these cultigens
would have provided in their early stages of domestication.”
Not to belabor the obvious, but the Paleolithic lifestyle of hunting big game and tossing any animals with low body fat met up against ecological constraints that made it unsustainable. In response, I suggest that it appears that our ancestors looked for an option, and they discovered that carbohydrate could replace fat as a method of diluting protein, with superior results.
1. Phinney SD. Ketogenic diets and physical performance. Nutrition & Metabolism 2004, 1:2.
2. Pascoe DD and Gladden LB. Muscle glycogen resynthesis after short term, high intensity exercise and resistance exercise. Sports Med (1996) 21:98-118.
3. Eaton SB, Konner M, Shostak M. The Paleolithic Prescription. New York: Harper& Row, 1988.
4. Robergs RA et al. Muscle glycogenolysis during different intensities of weight-resistance exercise. J Appl Physiology (1991) 70:1700-1706.
5. Speth JD and Spielman KA. Energy Source, Protein Metabolism, and Hunter-Gatherer Subsistence Strategies. J Anthro Archaeo 2, 1-31 (1983).
6. Rudman et al, Maximal Rates of Excretion and Synthesis of Urea in Normal and Cirrhotic Subjects, J Clin Invest. 1973 September; 52(9): 2241–2249.
7. Holt SHA, Brand-Miller J, Petocz P. An insulin index of foods: The insulin demand generated by 1000 kJ portions of common foods. Am J Clin Nutr 1997:66:1264-76.