High Protein Diets and Weight Loss/Fat Loss
Written by Dan Gwartney, MD
09 April 2007
Protein holds a principal position in the diets of bodybuilders. The primary source of amino acids, the building blocks necessary to promote muscle growth, protein is consumed in amounts well beyond the levels recommended by dieticians. Whereas the recommended dietary allowance (RDA) for protein is 0.8 grams per kilogram of bodyweight per day, most bodybuilders exceed this by a factor of three or more.1 Going by the RDA, a 100-kilo bodybuilder (220 pounds) need only consume 80 grams of protein. In practice, bodybuilders typically use the guideline of one gram per pound of bodyweight. Rather than being satisfied with 80 grams of protein, a bodybuilder might consume 220 grams or more.2
More than Just Muscle
However, there's more to protein than building muscle. The role of protein in weight loss/fat loss had traditionally been ignored, the belief being that it merely prevents the loss of lean muscle during periods of caloric deficit.3 Only recently has the popular success of the Atkins plan and other high-protein diets impressed upon the scientific community the need for further research into the role of protein in weight loss and fat loss.
While the South Beach and Atkins diets are clearly recognized as high protein (due to their emphasis on lowering carbohydrates), even more moderate programs, such as the Zone diet as created by Barry Sears, qualifies as a high protein diet. The typical American diet is roughly 12-18 percent protein (by calories); compare this to the 30 percent offered by the Zone diet or even higher percentage reached by other plans.1
Many bodybuilders will reach extremely high protein percentages during periods of carbohydrate depletion, especially when concentrated protein powders are used instead of meat, fish and dairy sources. The diet plans commonly describe two major functions for protein. One is to preserve lean muscle mass during weight loss. The second is to replace refined carbohydrates in the diet. By reducing refined carbohydrates, insulin levels may lower, with several beneficial results, including the following: improved insulin sensitivity, lower insulin levels, reduced water retention, immediate weight loss, lower blood pressure, improved fat loss, etc.
However, it's well understood that amino acids are bioactive compounds that either directly influence the metabolism and hormonal profile, or serve as precursors to bioactive molecules.4 It's possible that a higher level of protein in the diet may actually trigger processes that are responsible for some degree of the greater weight loss experienced. Academics and scientists have approached the high-protein diets with distaste, calling them fad diets, unproven, even dangerous. However, a sufficiently large body of science now exists that allows for an objective review of the effectiveness and possible mechanisms of action for high-protein diets.
An extensive review of high-protein diets was published in 2002 showing evidence for the safety and effectiveness of high-protein diets.5 Further studies have been published, allowing for a more complete evaluation of the safety and efficacy of high-protein diets. This review, published in the Journal of the American College of Nutrition, went a step beyond the question of whether or not high-protein diets work. It asked the next logical question: How?6 The authors, Drs. T. Halton and F. Hu of the Harvard School of Public Health, proposed three possible mechanisms of weight loss in high-protein diets. They performed this analysis by reviewing 50 weight loss diet studies comparing high- and low-protein diets under controlled conditions.
Three Mechanisms
The first of the three mechanisms proposed was an increase in dietary thermogenesis. Thermogenesis is the production of heat and is the method of weight loss of ephedra products.7 What makes thermogenesis so important to weight loss is that the body uses heat production as a means of wasting calories rather than storing them. Calories are units of energy and when applied in biological processes, drive the functions of the human body. When excess calories are consumed, they are stored either as fat or glycogen (a storage form of sugar). The body can modify how efficiently it burns calories by allowing some of the calories to be wasted as heat; this accounts for the weight loss effect of thermogenic agents.
There is also a thermic effect of food, meaning the amount of energy required to digest, absorb and dispose of consumed food. Carbohydrates and fat are easily digested and absorbed, and the end products are easily disposed of, as they are eventually broken down into water and carbon dioxide.8,9 Protein is a different matter. It requires a great deal of energy to digest proteins, and the absorption of the products of digestion (amino acids, oligopeptides) require active transport. Further, amino acids are disposed of as urea or ketones, or are converted into glucose (sugar). All these processes require energy, thus the thermic effect of protein is much higher than that of carbohydrates and fats. In fact, the thermic effect of each food type has been measured; carbohydrates and fat require between five to 15 percent of the calories consumed, whereas protein requires 20-35 percent.8 Obviously, if the net number of calories consumed is lower after accounting for the thermic effect of food, the calorie burden of food is less.
The thermic effect of protein appears to be dose dependent, meaning it creates a higher calorie demand with higher percentages of protein.8-13 As shown in one study, by increasing the protein content from 15 to 30 percent, the thermic effect was increased by approximately eight calories per hour.14 Thus, over a 24-hour period, almost 200 more calories were spent dealing with protein as opposed to carbohydrates or fat. Similar numbers have been reported in other studies.5,11,15 Regardless, the trend strongly suggests that increasing the percentage of protein in the diet can increase the thermic effect of food.6 This may account for enough of a difference to induce a weight loss of approximately four pounds per year. Not eye-popping numbers, but definitely worth considering as another worthy reason to keep protein intake high for a specialized population like bodybuilders.
The second proposal by Halton and Hu was that an increased protein load could decrease weight by increasing satiety. Satiety is the feeling of fullness, or a meal's ability to remove the hunger signal. Hunger involves powerful, primitive brain pathways and alterations of this signal are tied into many theories on treating obesity. Numerous studies have looked at the effect of different types of meals on reducing hunger and promoting satiety. For the sake of clarity, many of these studies exaggerate the difference, providing almost exclusively carbohydrate, fat or sugar meals. When provided with a high-protein meal, hunger is significantly reduced and the feeling of satiety remains for several hours as compared to carbohydrates and fat.16-21
Interestingly, the satiety effect of protein appears to have a lower threshold value. As opposed to the changes in thermic effect, which were noted at modest levels of protein, for a satiety effect to be consistently present following a meal for the duration recorded in these studies, the meal appears to need to consist of at least 40 percent protein.16-21 It's difficult to assess whether an absolute amount of protein need be present (for instance, a minimum of 15 grams) or if the type of protein influences this threshold number. For the time being, observations seem to suggest that meals need a substantial percentage of protein, at least 40 percent.
Lastly, the proposal of reduced subsequent energy intake was assessed. This means the effect of various levels of protein on later food consumption was investigated. At first, this sounds very similar to satiety, in that it seems logical that if hunger is reduced, less food is eaten later on. However, in some instances that's not the case. Once the effect of hunger suppression wears off, a rebound effect occurs. Later eating could compensate for the earlier reduced eating. Clearly, a temporary reduction in hunger that is later compensated for by overeating has little value in long-term weight loss.
Support from Other Studies
Again, reviewing the existing data from other studies supports this proposal. When provided with high-protein preloads (early meals), subsequent eating was significantly reduced. In one study, a meal of chicken (76 percent protein) decreased later eating by approximately 200 calories.16 Other studies showed similar or even more dramatic effect, with ad lib (buffet style) eating markedly reduced by nearly 400 calories.18,19,22-24 Again, as was noted in the satiety studies, there appears to be a threshold level necessary to consistently achieve a later suppression in later food consumption. It appears a minimal number of calories may be necessary in the high-protein meal (between 200 and 400) and a level greater than 30 percent protein.6 When such a meal is consumed, later food consumption appears to be reliably reduced in most subjects.
There were studies that did not agree with the three proposals, but given that different methods and conditions are considered, it appears the studies that were not in agreement often placed the subjects in conditions where free choice was not available and the environment was different from normal eating conditions.6
It was interesting to note that the authors also reviewed kidney function and cardiovascular disease risk associated with high-protein diets. Contrary to the popular warnings voiced by the media and nutritionists, there does not appear to be any need for caution in healthy individuals, though those with existing kidney disease do need to monitor their protein intake.2,5 Cardiovascular disease risks, as assessed by blood lipids (fat and cholesterol), are actually lower during high-protein diets. LDL (bad) cholesterol and blood fats are lower, while HDL (good) cholesterol increases; these are changes associated with lower risk of heart and blood vessel disease.25-27 Long-term studies correlating eating habits with health have shown people who eat moderate to high amounts of protein have less heart disease, while those who eat little animal protein are at greater risk of (hemorrhagic) stroke.28
Summing Up
In summary, this excellent review by Halton and Hu provides the bodybuilding community with further assurances that high-protein diets (relative to the U.S. RDA) are safe and effective. Going beyond a simple declaration of the effectiveness of such diets, the authors explored three possible mechanisms for the greater weight loss experienced during high- protein diets and found evidence supporting their hypotheses. It appears, though the usual caveat for further research was noted, that high-protein diets increase the amount of energy burned following a meal, more effectively reduce hunger and suppress later eating.
The cumulative effect of these three mechanisms may account for a difference of several hundred calories every day. This is a strong effect, greater than most pharmaceutical drugs. This review provides convincing evidence for all people looking to manage their weight to increase the percentage of protein in the diet. For the bodybuilder who already includes high percentages of protein in the diet for the purpose of preserving and building muscle mass, this is further support for a proven dietary regimen.
It would seem that science is nearly ready to accept what the bodybuilding community knows and has practiced for decades.
References
1. Smit E, Nieto FJ, et al. Estimates of animal and plant protein intake in US adults: results from the Third National Health and Nutrition Examination Survey, 1988-1991. J Am Diet Assoc, 1999 Jul;99(7):813-20.
2. Poortmans JR, Dellalieux O. Do regular high protein diets have potential health risks on kidney function in athletes? Int J Sport Nutr Exerc Metab, 2000;10:28-38.
3. Deibert P, Konig D, et al. Weight loss without losing muscle mass in pre-obese and obese subjects induced by a high soy protein diet. Int J Obes Relat Metab Disord, 2004 Oct;28(10):1349-52.
4. Ferranti P, Traisci MV, et al. Casein proteolysis in human milk: tracing the pattern of casein breakdown and the formation of potential bioactive peptides. J Dairy Res, 2004 Feb;71(1):74-87.
5. Eisenstein J, Roberts SB, et al. High-protein weight-loss diets: are they safe and do they work? A review of the experimental and epidemiologic data. Nutr Rev, 2002 Jul;60(7 Pt 1):189-200.
6. Halton TL, Hu FB. The effects of high protein diets on thermogenesis, satiety and weight loss: A critical review. J Am Coll Nutr, 2004;23(5):373-85.
7. Astrup A. Thermogenic drugs as a strategy for treatment of obesity. Endocrine, 2000 Oct;13(2):207-12.
8. Westerterp KR, Wilson SA, et al. Diet induced thermogenesis measured over 24h in a respiration chamber: effect of diet composition. Int J Obes Relat Metab Disord, 1999 Mar;23(3):287-92.
9. Nair KS, Halliday D, et al. Thermic response to isoenergetic protein, carbohydrate or fat meals in lean and obese subjects. Clin Sci, 1983 Sep;65(3):307-12.
10. Luscombe ND, Clifton PM, et al. Effect of a high protein, energy-restricted diet on weight loss ans energy expenditure after weight stabilization in hyperinsulinemic subjects. Int J Obes Relat Metab Disord, 2003 May;27(5):582-90.
11. Robinson SM, Jaccard C, et al. Protein turnover and thermogenesis in response to high-protein and high-carbohydrate feeding in men. Am J Clin Nutr, 1990 Jul;52(1):72-80.
12. Schutz Y, Bray G, et al. Postprandial thermogenesis at rest and during exercise in elderly men ingesting two levels of protein. J Am Coll Nutr, 1987 Dec;6(6):497-506.
13. Steiniger J, Karst H, et al. Diet-induced thermogenesis in man: thermic effect of single protein and carbohydrate test meals in lean and obese subjects. Ann Nutr Metab, 1987;31(2):117-25.
14. Johnston CS, Day CS, et al. Postprandial thermogenesis is increased 100% on a high-protein, low-fat diet in healthy, young women. J Am Coll Nutr, 2002 Feb;21(1):55-61.
15. Crovetti R, Porrini M, et al. The influence of thermic effect of food on satiety. Eur J Clin Nutr, 1998 Jul;52(7):482-8.
16. Johnson J, Vickers Z. Effects of flavor and macronutrient composition of food servings on liking, hunger and subsequent intake. Appetite, 1993;21:25-39.
17. Johnstone AM, Stubbs RJ, et al. Effect of overfeeding macronutrients on day to day food intake in man. Euro J Clin Nutr, 1996;50:418-30.
18. Poppitt SD, McCormack D, et al. Short term effects of macronutrient preloads on appetite and energy intake in lean women. Physiol Behav, 1998;64:279-85.
19. Rolls BJ, Hetherington M, et al. The specificity of satiety: The influence of foods of different macronutrient content on the development of satiety. Physiol Behav, 1988;43:145-53.
20. Stubbs RJ, Van Wyk MCW, et al. Breakfasts high in protein, fat or carbohydrate: effect on within-day appetite and energy balance. Euro J Clin Nutr, 1996;50:409-17.
21. Stubbs RJ, O'Reilly LM, et al. Description and evaluation of an experimental model to examine changes in selection between high protein, high carbohydrate and high fat foods in humans. Euro J Clin Nutr, 1999;53:13-21.
22. Porrini M, Crovetti R, et al. Evaluation of satiety sensations and food intake after different preloads. Appetite, 1995;25:17-30.
23. Barkeling B, Rossner S, et al. Effects of a high protein meal and a high carbohydrate meal on satiety measured by automated computerized monitoring of subsequent food intake, motivation to eat and food preferences. Int J Obes, 1990;14:743-51.
24. Booth DA, Chase A, et al. Relative effectiveness of protein in the late stages of appetite suppression in man. Physiol Behav, 1970;5:1299-1302.
25. Farnsworth E, Luscombe ND, et al. Effect of a high protein energy restricted diet on body composition, glycemic control and lipid concentrations in overweight and obese hyperinsulinemic men and women. Am J Clin Nutr, 2003;78:31-9.
26. Parker B, Noakes M, et al. Effect of a high protein, high monounsaturated fat weight loss diet on glycemic control and lipid levels in type-2 diabetes. Diabetes Care, 2002;25:425-30.
27. Wolfe BM. Potential role of raising dietary protein intake for reducing risk of atherosclerosis. Can J Cardiol, 1995;11(Suppl G):127g - 31g.
28. Iso H, Stampfer MJ, et al. Prospective study of fat and protein intake and risk of intraparenchymal hemorrhage in women. Circulation, 2001;103:856-63.
More than Just Muscle
However, there's more to protein than building muscle. The role of protein in weight loss/fat loss had traditionally been ignored, the belief being that it merely prevents the loss of lean muscle during periods of caloric deficit.3 Only recently has the popular success of the Atkins plan and other high-protein diets impressed upon the scientific community the need for further research into the role of protein in weight loss and fat loss.
While the South Beach and Atkins diets are clearly recognized as high protein (due to their emphasis on lowering carbohydrates), even more moderate programs, such as the Zone diet as created by Barry Sears, qualifies as a high protein diet. The typical American diet is roughly 12-18 percent protein (by calories); compare this to the 30 percent offered by the Zone diet or even higher percentage reached by other plans.1
Many bodybuilders will reach extremely high protein percentages during periods of carbohydrate depletion, especially when concentrated protein powders are used instead of meat, fish and dairy sources. The diet plans commonly describe two major functions for protein. One is to preserve lean muscle mass during weight loss. The second is to replace refined carbohydrates in the diet. By reducing refined carbohydrates, insulin levels may lower, with several beneficial results, including the following: improved insulin sensitivity, lower insulin levels, reduced water retention, immediate weight loss, lower blood pressure, improved fat loss, etc.
However, it's well understood that amino acids are bioactive compounds that either directly influence the metabolism and hormonal profile, or serve as precursors to bioactive molecules.4 It's possible that a higher level of protein in the diet may actually trigger processes that are responsible for some degree of the greater weight loss experienced. Academics and scientists have approached the high-protein diets with distaste, calling them fad diets, unproven, even dangerous. However, a sufficiently large body of science now exists that allows for an objective review of the effectiveness and possible mechanisms of action for high-protein diets.
An extensive review of high-protein diets was published in 2002 showing evidence for the safety and effectiveness of high-protein diets.5 Further studies have been published, allowing for a more complete evaluation of the safety and efficacy of high-protein diets. This review, published in the Journal of the American College of Nutrition, went a step beyond the question of whether or not high-protein diets work. It asked the next logical question: How?6 The authors, Drs. T. Halton and F. Hu of the Harvard School of Public Health, proposed three possible mechanisms of weight loss in high-protein diets. They performed this analysis by reviewing 50 weight loss diet studies comparing high- and low-protein diets under controlled conditions.
Three Mechanisms
The first of the three mechanisms proposed was an increase in dietary thermogenesis. Thermogenesis is the production of heat and is the method of weight loss of ephedra products.7 What makes thermogenesis so important to weight loss is that the body uses heat production as a means of wasting calories rather than storing them. Calories are units of energy and when applied in biological processes, drive the functions of the human body. When excess calories are consumed, they are stored either as fat or glycogen (a storage form of sugar). The body can modify how efficiently it burns calories by allowing some of the calories to be wasted as heat; this accounts for the weight loss effect of thermogenic agents.
There is also a thermic effect of food, meaning the amount of energy required to digest, absorb and dispose of consumed food. Carbohydrates and fat are easily digested and absorbed, and the end products are easily disposed of, as they are eventually broken down into water and carbon dioxide.8,9 Protein is a different matter. It requires a great deal of energy to digest proteins, and the absorption of the products of digestion (amino acids, oligopeptides) require active transport. Further, amino acids are disposed of as urea or ketones, or are converted into glucose (sugar). All these processes require energy, thus the thermic effect of protein is much higher than that of carbohydrates and fats. In fact, the thermic effect of each food type has been measured; carbohydrates and fat require between five to 15 percent of the calories consumed, whereas protein requires 20-35 percent.8 Obviously, if the net number of calories consumed is lower after accounting for the thermic effect of food, the calorie burden of food is less.
The thermic effect of protein appears to be dose dependent, meaning it creates a higher calorie demand with higher percentages of protein.8-13 As shown in one study, by increasing the protein content from 15 to 30 percent, the thermic effect was increased by approximately eight calories per hour.14 Thus, over a 24-hour period, almost 200 more calories were spent dealing with protein as opposed to carbohydrates or fat. Similar numbers have been reported in other studies.5,11,15 Regardless, the trend strongly suggests that increasing the percentage of protein in the diet can increase the thermic effect of food.6 This may account for enough of a difference to induce a weight loss of approximately four pounds per year. Not eye-popping numbers, but definitely worth considering as another worthy reason to keep protein intake high for a specialized population like bodybuilders.
The second proposal by Halton and Hu was that an increased protein load could decrease weight by increasing satiety. Satiety is the feeling of fullness, or a meal's ability to remove the hunger signal. Hunger involves powerful, primitive brain pathways and alterations of this signal are tied into many theories on treating obesity. Numerous studies have looked at the effect of different types of meals on reducing hunger and promoting satiety. For the sake of clarity, many of these studies exaggerate the difference, providing almost exclusively carbohydrate, fat or sugar meals. When provided with a high-protein meal, hunger is significantly reduced and the feeling of satiety remains for several hours as compared to carbohydrates and fat.16-21
Interestingly, the satiety effect of protein appears to have a lower threshold value. As opposed to the changes in thermic effect, which were noted at modest levels of protein, for a satiety effect to be consistently present following a meal for the duration recorded in these studies, the meal appears to need to consist of at least 40 percent protein.16-21 It's difficult to assess whether an absolute amount of protein need be present (for instance, a minimum of 15 grams) or if the type of protein influences this threshold number. For the time being, observations seem to suggest that meals need a substantial percentage of protein, at least 40 percent.
Lastly, the proposal of reduced subsequent energy intake was assessed. This means the effect of various levels of protein on later food consumption was investigated. At first, this sounds very similar to satiety, in that it seems logical that if hunger is reduced, less food is eaten later on. However, in some instances that's not the case. Once the effect of hunger suppression wears off, a rebound effect occurs. Later eating could compensate for the earlier reduced eating. Clearly, a temporary reduction in hunger that is later compensated for by overeating has little value in long-term weight loss.
Support from Other Studies
Again, reviewing the existing data from other studies supports this proposal. When provided with high-protein preloads (early meals), subsequent eating was significantly reduced. In one study, a meal of chicken (76 percent protein) decreased later eating by approximately 200 calories.16 Other studies showed similar or even more dramatic effect, with ad lib (buffet style) eating markedly reduced by nearly 400 calories.18,19,22-24 Again, as was noted in the satiety studies, there appears to be a threshold level necessary to consistently achieve a later suppression in later food consumption. It appears a minimal number of calories may be necessary in the high-protein meal (between 200 and 400) and a level greater than 30 percent protein.6 When such a meal is consumed, later food consumption appears to be reliably reduced in most subjects.
There were studies that did not agree with the three proposals, but given that different methods and conditions are considered, it appears the studies that were not in agreement often placed the subjects in conditions where free choice was not available and the environment was different from normal eating conditions.6
It was interesting to note that the authors also reviewed kidney function and cardiovascular disease risk associated with high-protein diets. Contrary to the popular warnings voiced by the media and nutritionists, there does not appear to be any need for caution in healthy individuals, though those with existing kidney disease do need to monitor their protein intake.2,5 Cardiovascular disease risks, as assessed by blood lipids (fat and cholesterol), are actually lower during high-protein diets. LDL (bad) cholesterol and blood fats are lower, while HDL (good) cholesterol increases; these are changes associated with lower risk of heart and blood vessel disease.25-27 Long-term studies correlating eating habits with health have shown people who eat moderate to high amounts of protein have less heart disease, while those who eat little animal protein are at greater risk of (hemorrhagic) stroke.28
Summing Up
In summary, this excellent review by Halton and Hu provides the bodybuilding community with further assurances that high-protein diets (relative to the U.S. RDA) are safe and effective. Going beyond a simple declaration of the effectiveness of such diets, the authors explored three possible mechanisms for the greater weight loss experienced during high- protein diets and found evidence supporting their hypotheses. It appears, though the usual caveat for further research was noted, that high-protein diets increase the amount of energy burned following a meal, more effectively reduce hunger and suppress later eating.
The cumulative effect of these three mechanisms may account for a difference of several hundred calories every day. This is a strong effect, greater than most pharmaceutical drugs. This review provides convincing evidence for all people looking to manage their weight to increase the percentage of protein in the diet. For the bodybuilder who already includes high percentages of protein in the diet for the purpose of preserving and building muscle mass, this is further support for a proven dietary regimen.
It would seem that science is nearly ready to accept what the bodybuilding community knows and has practiced for decades.
References
1. Smit E, Nieto FJ, et al. Estimates of animal and plant protein intake in US adults: results from the Third National Health and Nutrition Examination Survey, 1988-1991. J Am Diet Assoc, 1999 Jul;99(7):813-20.
2. Poortmans JR, Dellalieux O. Do regular high protein diets have potential health risks on kidney function in athletes? Int J Sport Nutr Exerc Metab, 2000;10:28-38.
3. Deibert P, Konig D, et al. Weight loss without losing muscle mass in pre-obese and obese subjects induced by a high soy protein diet. Int J Obes Relat Metab Disord, 2004 Oct;28(10):1349-52.
4. Ferranti P, Traisci MV, et al. Casein proteolysis in human milk: tracing the pattern of casein breakdown and the formation of potential bioactive peptides. J Dairy Res, 2004 Feb;71(1):74-87.
5. Eisenstein J, Roberts SB, et al. High-protein weight-loss diets: are they safe and do they work? A review of the experimental and epidemiologic data. Nutr Rev, 2002 Jul;60(7 Pt 1):189-200.
6. Halton TL, Hu FB. The effects of high protein diets on thermogenesis, satiety and weight loss: A critical review. J Am Coll Nutr, 2004;23(5):373-85.
7. Astrup A. Thermogenic drugs as a strategy for treatment of obesity. Endocrine, 2000 Oct;13(2):207-12.
8. Westerterp KR, Wilson SA, et al. Diet induced thermogenesis measured over 24h in a respiration chamber: effect of diet composition. Int J Obes Relat Metab Disord, 1999 Mar;23(3):287-92.
9. Nair KS, Halliday D, et al. Thermic response to isoenergetic protein, carbohydrate or fat meals in lean and obese subjects. Clin Sci, 1983 Sep;65(3):307-12.
10. Luscombe ND, Clifton PM, et al. Effect of a high protein, energy-restricted diet on weight loss ans energy expenditure after weight stabilization in hyperinsulinemic subjects. Int J Obes Relat Metab Disord, 2003 May;27(5):582-90.
11. Robinson SM, Jaccard C, et al. Protein turnover and thermogenesis in response to high-protein and high-carbohydrate feeding in men. Am J Clin Nutr, 1990 Jul;52(1):72-80.
12. Schutz Y, Bray G, et al. Postprandial thermogenesis at rest and during exercise in elderly men ingesting two levels of protein. J Am Coll Nutr, 1987 Dec;6(6):497-506.
13. Steiniger J, Karst H, et al. Diet-induced thermogenesis in man: thermic effect of single protein and carbohydrate test meals in lean and obese subjects. Ann Nutr Metab, 1987;31(2):117-25.
14. Johnston CS, Day CS, et al. Postprandial thermogenesis is increased 100% on a high-protein, low-fat diet in healthy, young women. J Am Coll Nutr, 2002 Feb;21(1):55-61.
15. Crovetti R, Porrini M, et al. The influence of thermic effect of food on satiety. Eur J Clin Nutr, 1998 Jul;52(7):482-8.
16. Johnson J, Vickers Z. Effects of flavor and macronutrient composition of food servings on liking, hunger and subsequent intake. Appetite, 1993;21:25-39.
17. Johnstone AM, Stubbs RJ, et al. Effect of overfeeding macronutrients on day to day food intake in man. Euro J Clin Nutr, 1996;50:418-30.
18. Poppitt SD, McCormack D, et al. Short term effects of macronutrient preloads on appetite and energy intake in lean women. Physiol Behav, 1998;64:279-85.
19. Rolls BJ, Hetherington M, et al. The specificity of satiety: The influence of foods of different macronutrient content on the development of satiety. Physiol Behav, 1988;43:145-53.
20. Stubbs RJ, Van Wyk MCW, et al. Breakfasts high in protein, fat or carbohydrate: effect on within-day appetite and energy balance. Euro J Clin Nutr, 1996;50:409-17.
21. Stubbs RJ, O'Reilly LM, et al. Description and evaluation of an experimental model to examine changes in selection between high protein, high carbohydrate and high fat foods in humans. Euro J Clin Nutr, 1999;53:13-21.
22. Porrini M, Crovetti R, et al. Evaluation of satiety sensations and food intake after different preloads. Appetite, 1995;25:17-30.
23. Barkeling B, Rossner S, et al. Effects of a high protein meal and a high carbohydrate meal on satiety measured by automated computerized monitoring of subsequent food intake, motivation to eat and food preferences. Int J Obes, 1990;14:743-51.
24. Booth DA, Chase A, et al. Relative effectiveness of protein in the late stages of appetite suppression in man. Physiol Behav, 1970;5:1299-1302.
25. Farnsworth E, Luscombe ND, et al. Effect of a high protein energy restricted diet on body composition, glycemic control and lipid concentrations in overweight and obese hyperinsulinemic men and women. Am J Clin Nutr, 2003;78:31-9.
26. Parker B, Noakes M, et al. Effect of a high protein, high monounsaturated fat weight loss diet on glycemic control and lipid levels in type-2 diabetes. Diabetes Care, 2002;25:425-30.
27. Wolfe BM. Potential role of raising dietary protein intake for reducing risk of atherosclerosis. Can J Cardiol, 1995;11(Suppl G):127g - 31g.
28. Iso H, Stampfer MJ, et al. Prospective study of fat and protein intake and risk of intraparenchymal hemorrhage in women. Circulation, 2001;103:856-63.