It is interesting to note from the careful observations published from the Bellevue study that Stafansson ate relatively modestly of protein, deriving between 80–85% of his dietary energy from fat and only 15–20% from protein [9]. This was, and still remains, at odds with the popular conception that the Inuit ate a high protein diet, whereas in reality it appears to have been a high fat diet with a moderate intake of protein. In his writings, Stefansson notes that the Inuit were careful to limit their intake of lean meat, giving excess lean meat to their dogs and reserving the higher fat portions for human consumption.
(...)
Given the uncertainties of this study caused by the subject's weight loss and potential for improved technique with multiple tests, the current author undertook a second study [please see the full article for the description of the first study] under the mentorship of Dr. Bruce Bistrian at MIT in Cambridge MA [14,15]. The diet employed in this followup study was patterned after that consumed by Stefansson during his year in the Bellevue study (and thus presumably close to that traditionally consumed by the Inuit) with the intention that the subjects would be in ketosis without weight loss.
This second study utilized competitive bicycle racers as subjects, confined to a metabolic ward for 5 weeks. In the first week, subjects ate a weight maintenance (eucaloric) diet providing 67% of non-protein energy as carbohydrate, during which time baseline performance studies were performed. This was followed by 4 weeks of a eucaloric ketogenic diet (EKD) providing 83% of energy as fat, 15% as protein, and less than 3% as carbohydrate. The meat, fish, and poultry that provided this diets protein, also provided 1.5 g/d of potassium and was prepared to contain 2 g/d of sodium. These inherent minerals were supplemented daily with an additional 1 g of potassium as bicarbonate, 3 grams of sodium as bouillon, 600 mg of calcium, 300 mg of magnesium, and a standard multivitamin.
The bicyclist subjects of this study noted a modest decline in their energy level while on training rides during the first week of the Inuit diet, after which subjective performance was reasonably restored except for their sprint capability, which remained constrained during the period of carbohydrate restriction. On average, subjects lost 0.7 kg in the first week of the EKD, after which their weight remained stable. Total body potassium (by 40K counting) revealed a 2% reduction in the first 2 weeks (commensurate with the muscle glycogen depletion documented by biopsy), after which it remained stable in the 4th week of the EKD. These results are consistent with the observed reduction in body glycogen stores but otherwise excellent preservation of lean body mass during the EKD.
The results of physical performance testing are presented in Table 2. What is remarkable about these data is the lack of change in aerobic performance parameters across the 4-week adaptation period of the EKD. The endurance exercise test on the cycle ergometer was performed at 65% of VO2max, which translates in these highly trained athletes into a rate of energy expenditure of 960 kcal/hr. At this high level of energy expenditure, it is notable that the second test was performed at a mean respiratory quotient of 0.72, indicating that virtually all of the substrate for this high energy output was coming from fat. This is consistent with measures before and after exercise of muscle glycogen and blood glucose oxidation (data not shown), which revealed marked reductions in the use of these carbohydrate-derived substrates after adaptation to the EKD.
Examining the results of these two ketogenic diet performance studies together indicates that both groups experienced a lag in performance across the first week or two of carbohydrate restriction, after which both peak aerobic power and sub-maximal (60–70% of VO2max) endurance performance were fully restored. In both studies, one with untrained subjects and the other with highly trained athletes who maintained their training throughout the study, there was no loss of VO2max despite the virtual absence of dietary carbohydrate for 4–6 weeks. This whole-body measure of oxidative metabolism could not be maintained unless there was excellent preservation of the full complement of functional tissues including skeletal muscle (and mitochondrial) mass, circulating red cell mass, and cardiopulmonary functions.
(...)
Resolving the performance paradox
There are three factors that can help us explain the paradox presented by studies showing superior performance with high carbohydrate diets versus the present author's two studies noted above.
Adaptation
The most obvious of these is the time allotted (or not) for keto-adaptation. In this context, the prescient observation of Schwatka (that adaptation to "a diet of reindeer meat" takes 2–3 weeks) says it all. None of the comparative low-carbohydrate versus high-carbohydrate studies done in support of the carbohydrate loading hypothesis sustained the low carbohydrate diet for more than 2 weeks [5], and most (including the classic report of Christensen and Hansen [2]) maintained their low-carbohydrate diets for 7 days or less.
There are to date no studies that carefully examine the optimum length of this keto-adapataion period, but it is clearly longer than one week and likely well advanced within 3–4 weeks. The process does not appear to happen any faster in highly trained athletes than in overweight or untrained individuals. This adaptation process also appears to require consistent adherence to carbohydrate restriction, as people who intermittently consume carbohydrates while attempting a ketogenic diet report subjectively reduced exercise tolerance.
Sodium and potassium
The second factor differentiating the author's studies from many others is optimized mineral nutriture, which has benefits for both cardiovascular reserve in the short term and preservation of lean body mass and function over longer time periods. The Inuit people lived much of the year on coastal ice (which is partially desalinated sea water), and much of their food consisted of soup made with meat in a broth from this brackish source of water. When they went inland to hunt, they traditionally added caribou blood (also a rich source of sodium) to their soup. With these empirically derived techniques, the Inuit culture had adapted the available resources to optimize their intakes of both sodium and potassium.
When meat is baked, roasted, or broiled; or when it is boiled but the broth discarded, potassium initially present in the meat is lost, making it more difficult to maintain potassium balance in the absence of fruits and vegetables. Because our research subjects were accustomed to eating meat, fish, and poultry prepared as something other than soup, we chose to give them most of their sodium separately as bouillon and a modest additional supplement of potassium as potassium bicarbonate. With these supplements maintaining daily intakes for sodium at 3–5 g/d and total potassium at 2–3 g/d, our adult subjects were able to effectively maintain their circulatory reserve (ie, allowing vasodilatation during submaximal exercise) and effective nitrogen balance with functional tissue preservation.
An example of what happens when these mineral considerations are not heeded can be found in a study prominently published in 1980 [18]. This was a study designed to evaluate the relative value of "protein only" versus "protein plus carbohydrate" in the preservation of lean tissue during a weight loss diet. The protein only diet consisted solely of boiled turkey (taken without the broth), whereas the protein plus carbohydrate consisted of an equal number of calories provided as turkey plus grape juice. Monitored for 4 weeks in a metabolic ward, the subjects taking the protein plus carbohydrate did fairly well at maintaining lean body mass (measured by nitrogen balance), whereas those taking the protein only experienced a progressive loss of body nitrogen.
A clue to what was happening in this "Turkey Study" could be found in the potassium balance data provided in this report. Normally, nitrogen and potassium gains or losses are closely correlated, as they both are contained in lean tissue. Interestingly, the authors noted that the protein only diet subjects were losing nitrogen but gaining potassium. As noted in a rebuttal letter published soon after this report [19], this anomaly occurred because the authors assumed the potassium intake of their subjects based upon handbook values for raw turkey, not recognizing that half of this potassium was being discarded in the unconsumed broth. Deprived of this potassium (and also limited in their salt intake), these subjects were unable to benefit from the dietary protein provided and lost lean tissue. Also worthy of note, although this study was effectively refuted by a well-designed metabolic ward study published 3 years later [20], this "Turkey Study" continues to be quoted as an example of the limitations of low carbohydrate weight loss diets.
Protein dose
The third dietary factor potentially affecting physical performance is adjusting protein intake to bring it within the optimum therapeutic window for human metabolism. The studies noted herein [13-15,20] demonstrate effective preservation of lean body mass and physical performance when protein is in the range of 1.2 – 1.7 g/kg reference body weight daily, provided in the context of adequate minerals. Picking the mid-range value of 1.5 g/kg-d, for adults with reference weights ranging from 60–80 kg, this translates into total daily protein intakes 90 to 120 g/d. This number is also consistent with the protein intake reported in the Bellevue study [9]. When expressed in the context of total daily energy expenditures of 2000–3000 kcal/d, about 15% of ones daily energy expenditure (or intake if the diet is eucaloric) needs to be provided as protein.
The effects of reducing daily protein intake to below 1.2 g/kg reference weight during a ketogenic diet include progressive loss of functional lean tissue and thus loss of physical performance, as demonstrated by Davis et al [21]. In this study, subjects given protein at 1.1 g/kg-d experienced a significant reduction in VO2max over a 3 month period on a ketogenic diet, whereas subjects given 1.5 g/kg-d maintained VO2max.
At the other end of the spectrum, higher protein intakes have the potential for negative side-effects if intake of this nutrient exceeds 25% of daily energy expenditure. One concern with higher levels of protein intake is the suppression of ketogenesis relative to an equi-caloric amount of fat (assuming that ketones are a beneficial adaptation to whole body fuel homeostasis). In addition, Stefansson describes a malady known by the Inuit as rabbit malaise [8]. This problem would occur in the early spring when very lean rabbits were the only available game, when people might be tempted to eat too much protein in the absence of an alternative source of dietary fat. The symptoms were reported to occur within a week, and included headache and lassitude. Such symptoms are not uncommon among people who casually undertake a "low carbohydrate, high protein" diet.
Conclusions
Both observational and prospectively designed studies support the conclusion that submaximal endurance performance can be sustained despite the virtual exclusion of carbohydrate from the human diet. Clearly this result does not automatically follow the casual implementation of dietary carbohydrate restriction, however, as careful attention to time for keto-adaptation, mineral nutriture, and constraint of the daily protein dose is required. Contradictory results in the scientific literature can be explained by the lack of attention to these lessons learned (and for the most part now forgotten) by the cultures that traditionally lived by hunting. Therapeutic use of ketogenic diets should not require constraint of most forms of physical labor or recreational activity, with the one caveat that anaerobic (ie, weight lifting or sprint) performance is limited by the low muscle glycogen levels induced by a ketogenic diet, and this would strongly discourage its use under most conditions of competitive athletics.
