Influence of carbohydrates on food intake
Food intake is regulated by the complex interaction of psychological and physiological events associated with ingestion. While the energy content of foods has an important role in determining the amount eaten, a number of other properties of foods also may be important. These include palatability, macronutrient composition, form of the food (solid vs. liquid), how it is prepared, and its energy density (calories per gram).
Of key concern is whether the varying physiological responses to carbohydrates are associated with distinctive effects on food intake. Ways in which carbohydrates could influence intake include taste, chewing time, stomach distension, digestibility, absorption rate, hormonal changes, and metabolic signals arising as a result of carbohydrate utilization by different tissues. The roles of these various influences and the way that they interact to affect food intake are not well-understood.
It is useful to distinguish between "satiation" and "satiety." Satiation refers to the processes involved in the termination of a meal, whereas satiety refers to the effects of a food (often referred to as a preload) or a meal after eating has ended (93). Foods that are readily overeaten (i.e. have relatively little impact on satiation) are usually highly palatable and have high energy density. Most studies of carbohydrates have examined the effects on satiety, that is, how fixed amounts of carbohydrate or carbohydrate-rich foods impact subsequent food intake.
Sugars and food intake
The literature on the effects of sugars on the regulation of food intake has been recently reviewed (94). Some sugars are of particular interest because of the sweet taste they provide. While sweetness increases the palatability of foods, particularly when combined with fat, and therefore may increase the probability that sweet foods will be selected for consumption (95), there is no indication that sugar is associated with excessive food intake. Intake of sweet foods or drinks is limited by changes in the hedonic response to sweetness during consumption (96). Thus, to a hungry individual a sweet food will be rated as extremely pleasant in taste, but as consumption proceeds this rating of pleasantness declines. Ratings of foods with different tastes, for example, salty foods, will be unaffected by consumption of sweet foods. This "sensory-specific satiety" limits consumption of one type of food and helps to ensure that a variety of foods is consumed (97).
Many people believe that sugar and other carbohydrates contribute to overeating and obesity. Despite this popular belief, there is little direct evidence that obese individuals eat excessive quantities of sweet foods. Indeed, a number of studies show an inverse relationship between reported sugar consumption and degree of overweight (98). In a recent survey of the 10 favorite foods of a large sample of obese men and women, it was found that obese men listed mainly protein/fat sources (meat dishes) among their favorite foods, while obese women listed predominantly carbohydrate/fat sources (doughnuts, cookies, cake) and foods that are sweet. Preference for carbohydrates was not a standard feature of obesity. Rather preferences for major food sources of fat as opposed to carbohydrate may be a primary characteristic of human obesity syndromes (95,99). Thus, although there is little evidence that any of the various sugars are associated with obesity, sugars are often associated with a high-fat content in foods and serve to increase the palatability of fat, and fat is associated with obesity.
Starch and food intake
Variations in the starch in foods could affect the amount consumed or hunger and satiety. For example, the preparation method, the food source, and the amylose/amylopectin ratio can all lead to different glucose/insulin responses and hormonal profiles. Starchy foods vary widely in their glycemic response (the effect on blood glucose) from lente, a slow sustained glycemic response, to rapid increases in blood glucose (73). Slow digestion and absorption of carbohydrates helps to maintain steady blood glucose levels which can be beneficial to diabetics. High consumption of lente foods can also reduce serum triglycerides and improve lipid metabolism (100).
Altering the amylose/amylopectin ratio changes physiologic responses which could influence satiety. High-amylose starches are associated with a lower glycemic response than low-amylose starches, and they may also empty more slowly from the stomach. As would be predicted from these physiologic effects, increasing the amylose/amylopectin ratio has consistently been found to be associated with high satiety.
Predictions about how resistant starch would affect satiety are not straightforward. If similar amounts of resistant and regular starch are consumed, the resistant starch will deliver only about half the energy as the regular starch and one would expect decreased satiety and compensatory food intake. On the other hand, resistant starch may act like soluble fibre in that it could delay gastric emptying and prolong absorption which in turn could prolong satiety. When resistant starch (50g raw potato starch) was compared to an equal weight of pregelatinized potato starch consumed in a drink, the resistant starch was associated with a low glycemic response and was less satiating. Ratings of satiety and fullness returned to baseline fasting levels much more rapidly than they did with digestible starch (101).
Dietary fibre and food intake
There are a number of reasons why dietary fibre can reduce food intake: high-fibre foods take longer to eat; fibre decreases the energy density of food; some fibres such as guar gum and pectin slow gastric emptying; fibre may reduce the digestibility of food; there may be increased faecal loss of energy on high-fibre diets; and fibre may affect some gastrointestinal hormones that influence food intake (102).
The literature on this topic is complex because of the different types and doses of fibre that have been tested, and the wide variety of experimental protocols. This is illustrated by the previous discussion of the effects of resistant starch which is a type of dietary fibre. Nevertheless, there are a number of studies that show that high-fibre foods consumed either at breakfast or lunch significantly reduce intake at the next meal compared to low-fibre foods. A recent well-controlled study in which the effects of soluble or insoluble fibre supplementation at breakfast were compared, found that fibre supplementation (20g rather than 3g) was associated with a significant reduction in lunch intake. Total daily energy intake, however, was not affected by the quantity or type of fibre in the breakfast (103).
Energy and macronutrient balance
Maintaining a stable body weight requires achieving energy balance, where the amount of energy ingested equals the amount of energy expended. While obesity can only develop when energy intake exceeds energy expenditure (104), efforts to attribute obesity solely to a high level of energy intake or to a low level of energy expenditure have been unsuccessful. Obesity could develop slowly from a small, sustained positive energy balance produced by some combination of increased energy intake and decreased physical activity or could result from periodic bouts of positive energy balance achieved by temporary increases in intake or decreases in physical activity.
Achieving body weight regulation requires more than achieving energy balance; it also requires that macronutrient balance be achieved. Macronutrient balance means that the intake of each macronutrient is equal to its oxidation. If this is not the case for a particular macronutrient, body stores of that macronutrient will change. For a weight-stable individual this means that the composition of fuel oxidized is equal to the composition of energy ingested. When the state of energy and macronutrient balance is disrupted (e.g. overfeeding, altering chronic level of physical activity), the body attempts to restore this state of homeostasis. In such cases, the differences in the rapidity with which balance of each macronutrient is restored has important implications for the role of diet composition in body weight regulation.
The hierarchy for substrate oxidation
The fuel for energy expenditure is supplied by protein, carbohydrate and fat. This fuel can be supplied by the diet or can come from body energy stores. There appears to be a hierarchy for substrate oxidation which is determined by the storage capability of the body for each macronutrient, the energy costs of converting a macronutrient to a form with greater storage capacity, and by specific fuel needs of certain tissues. Alcohol has highest priority for oxidation because there is no body storage pool and conversion of alcohol to fat is energetically expensive. Amino acids are next in the oxidative hierarchy. Again, there is not a specific storage pool for amino acids. Body proteins are functional in nature and do not serve as a storage depot for amino acids. Carbohydrates are third in the oxidative hierarchy. There is a limited capacity to store carbohydrate as glycogen (a typical adult male can store approximately 500 g of glycogen, predominantly in muscle and liver) and conversion of carbohydrate to fat is energetically expensive. Carbohydrate is also somewhat unique in that it is an obligatory fuel for the central nervous system and the formed blood elements (e.g. red blood cells). In contrast to the other macronutrients there a virtually unlimited storage capacity for fat (largely in adipose tissue). The efficiency of storage of dietary fat in adipose tissue is very high (96-98%). Unlike carbohydrate, fat is not a unique fuel source for any body tissue.
Because of their oxidative priority, the body has an exceptional ability to maintain alcohol and protein balance across a wide range of intake of each. Because carbohydrate stores represent a small proportion of daily carbohydrate intake and because net de novo lipogenesis from carbohydrate does not occur to an appreciable extent under normal circumstances (105,106), carbohydrate oxidation closely matches carbohydrate intake. Carbohydrate balance appears to be well maintained across a wide range of carbohydrate intake. Unlike other macronutrients, fat does not promote its own oxidation and the amount of fat which is oxidized is the difference between total energy needs and oxidation of the other priority fuels.
Obesity and nutrient balance
The body's ability to maintain energy and nutrient balance is dependent upon a complex regulatory system that allows the body to achieve and maintain a steady-state of energy and nutrient balance. Sustained increases in energy intake can lead to increased body weight and an accompanying increase in energy expenditure. Body weight will stabilize and energy balance will be achieved when energy expenditure is increased to the level of energy intake. Conversely, a decrease in energy intake will disrupt energy balance and produce a loss of body weight accompanied by a reduction in energy expenditure. Body weight will stabilize when energy expenditure declines to the level of energy intake.
It may be more useful in understanding body weight regulation to examine how the body achieves macronutrient balance. As discussed earlier, acute changes in intake of alcohol, protein, or carbohydrate are rapidly balanced by changes in oxidation of each. In contrast, fat oxidation is not tightly linked to fat intake. As a consequence, positive or negative energy balance are largely conditions of positive or negative fat balance. Thus, the point at which a stable body weight and body composition is reached and defended is that point at which fat balance is achieved.
The two major factors which influence fat balance are amount and composition of food eaten and the total amount of physical activity. Positive fat balance can be produced by overconsumption of energy or restriction of physical activity. Positive fat balance will occur when any type of diet is overconsumed. During carbohydrate overfeeding, for example, carbohydrate oxidation increases to maintain carbohydrate balance, but because carbohydrate is providing more fuel for oxidative needs, fat oxidation is providing less than usual, creating positive fat balance (107).
Negative fat balance can result from underconsumption of total energy or fat or by an increase in the level of physical activity. During underconsumption of energy, the supply of the priority metabolic fuels (carbohydrate and protein) are insufficient to meet the body's energy needs. Thus, the remaining energy needs are met by fat oxidation which comes largely from endogenous fat stores. An increase in the level of physical activity will increase total energy requirements with the additional energy needs being met by increased fat oxidation.
Fat balance and body weight stability
There are two mechanisms by which a new steady-state of body weight and body composition achieved following a positive or negative perturbation in fat balance. First, changes in behaviour can lead to adjustments in either intake or oxidation of fat (e.g. altering total energy or fat intake and altering physical activity). Second, in the absence of sufficient behaviour changes, fat oxidation will be altered following alterations in the body fat mass. As an example of behavioural adjustments, the negative fat balance produced by reducing energy intake could be eliminated totally by a compensatory reduction in physical activity. As an example of metabolic adjustments, overconsumption of total energy and fat will produce positive energy balance. If behavioural adjustments are absent or insufficient, increases in the body fat mass will result. Increased body fat mass is associated with increased levels of circulating free fatty acids which elevate total fat oxidation. Thus, a stable body weight will be reached at the point where the body fat mass has increased sufficiently so that fat oxidation equals fat intake.
Metabolic differences between carbohydrate and fat
Based on known differences in macronutrient metabolism, we can begin to predict how the composition of the diet, and specifically the carbohydrate to fat ratio of the diet, might impact upon body weight regulation. It must be realized that the pathways by which nutrients are metabolized (particularly carbohydrate) vary with the overall state of energy balance and this must be considered when predicting the impact of diet composition. For example, conversion of carbohydrate to fat would occur during situations of excess carbohydrate intake and not under situations of normal or below normal intake.
Changing diet composition with no energy intake change
Altering diet composition without a change in total energy intake should have relatively modest effects on body weight and body fat content. There are at least two ways that such a change in diet composition could affect body weight. First, the thermic effect of carbohydrate is greater than the thermic effect of fat. Changing to a lower fat diet (assuming total energy and protein intake remain constant) means changing to a higher carbohydrate diet, which will increase total energy expenditure. The magnitude of increase in energy expenditure depends on the magnitude of change of the carbohydrate/fat ratio, but is probably relatively small and of questionable importance in body weight regulation for reducing dietary fat from 35-40% to 20-25% of total energy intake. Second, altering the carbohydrate/fat ratio of the diet requires that substrate oxidation rates be readjusted to the new macronutrient intakes. If total energy expenditure is not changed, these changes occur relatively rapidly, with carbohydrate and protein balance being reachieved more quickly than fat balance (108,109). Negative fat balance and some loss of body fat will occur until fat balance is reachieved. It is difficult to predict the rapidity with which fat balance will be reachieved following a reduction in fat (and an accompanying increase in carbohydrate intake).
Effects of diet composition during positive energy balance
It is during periods of positive energy balance that differences in carbohydrate and fat have the greatest impact upon body weight regulation. This is because of differences in the efficiency of metabolic pathways involved in disposing of excess carbohydrate vs. fat. One study (107) demonstrated that while the majority of excess energy is stored regardless of its composition, a greater proportion of excess energy is stored when the excess is from fat as compared to when the excess is from carbohydrate. This is a clear example of a situation where fat intake leads to more body energy storage than the same amount of energy from carbohydrate.
Total energy expenditure increases more with carbohydrate overfeeding than with fat overfeeding. This is because carbohydrate oxidation increases to a greater extent than fat oxidation decreases during carbohydrate overfeeding. The difference between carbohydrate and fat in the proportion of excess energy stored is greatest during the first week of overfeeding. This suggests that the more sustained the overfeeding, the less the difference between carbohydrate and fat overfeeding. If obesity develops due to brief, periodic episodes of overeating, differences between fat and carbohydrate are likely to be more important than if obesity develops from sustained positive energy balance.
Carbohydrate type and body weight regulation
The effects of different types of carbohydrates on body weight regulation have been reviewed recently (110). While there are clear differences in metabolism of carbohydrates and fat that could affect body weight regulation, there do not appear to be such metabolic differences between types of carbohydrate. The majority of comparisons have been made between simple sugars and complex carbohydrates. There is little scientific support for the commonly held perception that consumption of high amounts of simple sugar contributes to obesity. There is no evidence that simple sugars are used with a different efficiency than complex carbohydrates (other than dietary fibre or resistant oligosaccharides). While there is substantial data suggesting that high levels of dietary fat intake are associated with high levels of obesity, at present there is no reason to believe that high intake of simple sugar is associated with high levels of obesity.
Does carbohydrate make you fat?
The idea that increased insulin concentrations subsequent to carbohydrate intake lead to conversion of significant amounts of carbohydrate to fat is misleading. First, it takes an extreme excess of carbohydrate to produce de novolipogenesis, and even under these conditions, very little net fat is produced from carbohydrate. Second, the idea that persons with insulin resistance are particularly prone to become obese when eating high carbohydrate diets is unsubstantiated by scientific evidence. In fact, low-fat, high-carbohydrate diets are commonly recommended to prevent further weight gain for these individuals who are at risk to develop non-insulin dependent diabetes and coronary heart disease. Finally, substantial data suggest that voluntary energy intake is higher in many people when the diet is high in fat content and low in carbohydrate content. Excess consumption of energy in any form leads to accumulation of body fat. There is no serious scientific evidence to suggest, however, that diets high in carbohydrate promote weight gain when consumed in amounts which do not exceed energy requirements.
Prevention of obesity
Because excess dietary fat is stored more efficiently than excess dietary carbohydrate, eating a low fat diet may be helpful in obesity prevention. If one assumes that everyone overeats occasionally, less of the excess energy will be stored as adipose tissue if a low fat diet is consumed than a high fat diet. It remains prudent to recommend a high carbohydrate diet for body weight maintenance. Diets high in fat are likely to promote excess energy consumption and excess dietary fat is stored as adipose tissue with extremely high efficiency. Eating a high carbohydrate diet reduces the likelihood of overeating and, if overeating occurs, results in slightly less of the excess energy being stored as adipose tissue.
Alternative sweeteners
Dietary carbohydrates responsible for sweet taste are often replaced or substituted to varying extents by alternative sweeteners. The main reasons are to reduce the energy content of the diet, to minimise postprandial blood glucose fluctuations, to reduce cariogenicity, and to reduce cost.
Alternative sweeteners are defined as sweeteners other than sucrose. The term sweetener is mostly used for the high-intensity sweeteners (174) or for "any substance other than a carbohydrate whose primary sensory characteristic is sweet"(175), but sometimes to also collectively describe nutritive and non-nutritive sweeteners. The nutritive sweeteners are the mono and disaccharide sugars and a large variety of carbohydrate sweeteners that occur naturally in foods or are added in purified form (174).
The two main groups of alternative sweeteners that are used as sucrose substitutes or replacers, and classified on the basis of their function in foods, are the high intensity "non-nutritive" sweeteners and the "nutritive" bulk sweeteners or "sugar bulking" agents.
Non-nutritive sweeteners
Alternative sweeteners which are non-nutritive, non-carbohydrate, very low in calories and with an intense sweet taste, have been further grouped into three classes (176). First, the naturally occurring compounds such as monellin, thaumatin, miraculin, stevioside, steviol, etc., of which more than 30 have been identified and described. The second group includes the synthetic compounds saccharin, cyclamate, acesulfame, and others. The third group has two semi-synthetic compounds, neohesperidin dihydrochalcone (NHDC) and the dipeptide aspartylphenylalanine, also known as aspartame.
Nutritive sweeteners
Other alternative sweeteners are low-energy, bulk, sugar (sucrose) substitutes which are used not only for their sweet taste, but also to replace intrinsic functions of sugar in baked products, ice cream, frozen desserts, and other processed foods. These sugar substitutes are carbohydrates and are usually classified as nutritive sweeteners. They include glucose (dextrose), liquid glucose, high fructose syrups, liquid fructose, crystalline fructose, corn syrup, corn syrup solids, concentrated grape juice, invert sugar, invert syrups (174,175), and polyols, which are polyhydric alcohols produced by the hydrogenation of the corresponding reducing sugars.
The benefits of carbohydrate loading before prolonged submaximal exercise have been shown mainly during cycling. A link was demonstrated between endurance performance during cycle ergometry and pre-exercise muscle glycogen concentration (184). The importance of muscle glycogen during prolonged exercise was confirmed in subsequent studies which showed that fatigue occurs when muscle glycogen concentrations are reduced to low values (185-187). Therefore, it is not surprising that attempts were made to find methods of increasing muscle glycogen stores in preparation for prolonged exercise. One study (188) examined the influence of different nutritional states on the resynthesis of glycogen during recovery from prolonged exhaustive exercise. It found that a diet low in carbohydrate, and high in fat and protein for 2 to 3 days after prolonged submaximal exercise, produced a delayed muscle glycogen resynthesis, but when this was followed by a high carbohydrate diet for the same period of time, glycogen supercompensation occurred (see Figure 7). This dietary manipulation not only increased the pre-exercise muscle glycogen concentration but also resulted in a significant improvement in endurance capacity (see Figure 8). Although this original method of carbohydrate-loading was recommended as part of the preparation for endurance competitions, the low carbohydrate, high fat and protein phase of the diet is an unpleasant experience. Therefore, alternative ways were explored to increase the pre-exercise glycogen stores without including a period on a diet high in fat and protein (189). It was found that a carbohydrate-rich diet consumed for 3 days prior to competition, accompanied by a decrease in training intensity, resulted in increased muscle glycogen concentrations of the same magnitude as those achieved with the traditional carbohydrate loading procedure.
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Food intake is regulated by the complex interaction of psychological and physiological events associated with ingestion. While the energy content of foods has an important role in determining the amount eaten, a number of other properties of foods also may be important. These include palatability, macronutrient composition, form of the food (solid vs. liquid), how it is prepared, and its energy density (calories per gram).
Of key concern is whether the varying physiological responses to carbohydrates are associated with distinctive effects on food intake. Ways in which carbohydrates could influence intake include taste, chewing time, stomach distension, digestibility, absorption rate, hormonal changes, and metabolic signals arising as a result of carbohydrate utilization by different tissues. The roles of these various influences and the way that they interact to affect food intake are not well-understood.
It is useful to distinguish between "satiation" and "satiety." Satiation refers to the processes involved in the termination of a meal, whereas satiety refers to the effects of a food (often referred to as a preload) or a meal after eating has ended (93). Foods that are readily overeaten (i.e. have relatively little impact on satiation) are usually highly palatable and have high energy density. Most studies of carbohydrates have examined the effects on satiety, that is, how fixed amounts of carbohydrate or carbohydrate-rich foods impact subsequent food intake.
Sugars and food intake
The literature on the effects of sugars on the regulation of food intake has been recently reviewed (94). Some sugars are of particular interest because of the sweet taste they provide. While sweetness increases the palatability of foods, particularly when combined with fat, and therefore may increase the probability that sweet foods will be selected for consumption (95), there is no indication that sugar is associated with excessive food intake. Intake of sweet foods or drinks is limited by changes in the hedonic response to sweetness during consumption (96). Thus, to a hungry individual a sweet food will be rated as extremely pleasant in taste, but as consumption proceeds this rating of pleasantness declines. Ratings of foods with different tastes, for example, salty foods, will be unaffected by consumption of sweet foods. This "sensory-specific satiety" limits consumption of one type of food and helps to ensure that a variety of foods is consumed (97).
Many people believe that sugar and other carbohydrates contribute to overeating and obesity. Despite this popular belief, there is little direct evidence that obese individuals eat excessive quantities of sweet foods. Indeed, a number of studies show an inverse relationship between reported sugar consumption and degree of overweight (98). In a recent survey of the 10 favorite foods of a large sample of obese men and women, it was found that obese men listed mainly protein/fat sources (meat dishes) among their favorite foods, while obese women listed predominantly carbohydrate/fat sources (doughnuts, cookies, cake) and foods that are sweet. Preference for carbohydrates was not a standard feature of obesity. Rather preferences for major food sources of fat as opposed to carbohydrate may be a primary characteristic of human obesity syndromes (95,99). Thus, although there is little evidence that any of the various sugars are associated with obesity, sugars are often associated with a high-fat content in foods and serve to increase the palatability of fat, and fat is associated with obesity.
Starch and food intake
Variations in the starch in foods could affect the amount consumed or hunger and satiety. For example, the preparation method, the food source, and the amylose/amylopectin ratio can all lead to different glucose/insulin responses and hormonal profiles. Starchy foods vary widely in their glycemic response (the effect on blood glucose) from lente, a slow sustained glycemic response, to rapid increases in blood glucose (73). Slow digestion and absorption of carbohydrates helps to maintain steady blood glucose levels which can be beneficial to diabetics. High consumption of lente foods can also reduce serum triglycerides and improve lipid metabolism (100).
Altering the amylose/amylopectin ratio changes physiologic responses which could influence satiety. High-amylose starches are associated with a lower glycemic response than low-amylose starches, and they may also empty more slowly from the stomach. As would be predicted from these physiologic effects, increasing the amylose/amylopectin ratio has consistently been found to be associated with high satiety.
Predictions about how resistant starch would affect satiety are not straightforward. If similar amounts of resistant and regular starch are consumed, the resistant starch will deliver only about half the energy as the regular starch and one would expect decreased satiety and compensatory food intake. On the other hand, resistant starch may act like soluble fibre in that it could delay gastric emptying and prolong absorption which in turn could prolong satiety. When resistant starch (50g raw potato starch) was compared to an equal weight of pregelatinized potato starch consumed in a drink, the resistant starch was associated with a low glycemic response and was less satiating. Ratings of satiety and fullness returned to baseline fasting levels much more rapidly than they did with digestible starch (101).
Dietary fibre and food intake
There are a number of reasons why dietary fibre can reduce food intake: high-fibre foods take longer to eat; fibre decreases the energy density of food; some fibres such as guar gum and pectin slow gastric emptying; fibre may reduce the digestibility of food; there may be increased faecal loss of energy on high-fibre diets; and fibre may affect some gastrointestinal hormones that influence food intake (102).
The literature on this topic is complex because of the different types and doses of fibre that have been tested, and the wide variety of experimental protocols. This is illustrated by the previous discussion of the effects of resistant starch which is a type of dietary fibre. Nevertheless, there are a number of studies that show that high-fibre foods consumed either at breakfast or lunch significantly reduce intake at the next meal compared to low-fibre foods. A recent well-controlled study in which the effects of soluble or insoluble fibre supplementation at breakfast were compared, found that fibre supplementation (20g rather than 3g) was associated with a significant reduction in lunch intake. Total daily energy intake, however, was not affected by the quantity or type of fibre in the breakfast (103).
Energy and macronutrient balance
Maintaining a stable body weight requires achieving energy balance, where the amount of energy ingested equals the amount of energy expended. While obesity can only develop when energy intake exceeds energy expenditure (104), efforts to attribute obesity solely to a high level of energy intake or to a low level of energy expenditure have been unsuccessful. Obesity could develop slowly from a small, sustained positive energy balance produced by some combination of increased energy intake and decreased physical activity or could result from periodic bouts of positive energy balance achieved by temporary increases in intake or decreases in physical activity.
Achieving body weight regulation requires more than achieving energy balance; it also requires that macronutrient balance be achieved. Macronutrient balance means that the intake of each macronutrient is equal to its oxidation. If this is not the case for a particular macronutrient, body stores of that macronutrient will change. For a weight-stable individual this means that the composition of fuel oxidized is equal to the composition of energy ingested. When the state of energy and macronutrient balance is disrupted (e.g. overfeeding, altering chronic level of physical activity), the body attempts to restore this state of homeostasis. In such cases, the differences in the rapidity with which balance of each macronutrient is restored has important implications for the role of diet composition in body weight regulation.
The hierarchy for substrate oxidation
The fuel for energy expenditure is supplied by protein, carbohydrate and fat. This fuel can be supplied by the diet or can come from body energy stores. There appears to be a hierarchy for substrate oxidation which is determined by the storage capability of the body for each macronutrient, the energy costs of converting a macronutrient to a form with greater storage capacity, and by specific fuel needs of certain tissues. Alcohol has highest priority for oxidation because there is no body storage pool and conversion of alcohol to fat is energetically expensive. Amino acids are next in the oxidative hierarchy. Again, there is not a specific storage pool for amino acids. Body proteins are functional in nature and do not serve as a storage depot for amino acids. Carbohydrates are third in the oxidative hierarchy. There is a limited capacity to store carbohydrate as glycogen (a typical adult male can store approximately 500 g of glycogen, predominantly in muscle and liver) and conversion of carbohydrate to fat is energetically expensive. Carbohydrate is also somewhat unique in that it is an obligatory fuel for the central nervous system and the formed blood elements (e.g. red blood cells). In contrast to the other macronutrients there a virtually unlimited storage capacity for fat (largely in adipose tissue). The efficiency of storage of dietary fat in adipose tissue is very high (96-98%). Unlike carbohydrate, fat is not a unique fuel source for any body tissue.
Because of their oxidative priority, the body has an exceptional ability to maintain alcohol and protein balance across a wide range of intake of each. Because carbohydrate stores represent a small proportion of daily carbohydrate intake and because net de novo lipogenesis from carbohydrate does not occur to an appreciable extent under normal circumstances (105,106), carbohydrate oxidation closely matches carbohydrate intake. Carbohydrate balance appears to be well maintained across a wide range of carbohydrate intake. Unlike other macronutrients, fat does not promote its own oxidation and the amount of fat which is oxidized is the difference between total energy needs and oxidation of the other priority fuels.
Obesity and nutrient balance
The body's ability to maintain energy and nutrient balance is dependent upon a complex regulatory system that allows the body to achieve and maintain a steady-state of energy and nutrient balance. Sustained increases in energy intake can lead to increased body weight and an accompanying increase in energy expenditure. Body weight will stabilize and energy balance will be achieved when energy expenditure is increased to the level of energy intake. Conversely, a decrease in energy intake will disrupt energy balance and produce a loss of body weight accompanied by a reduction in energy expenditure. Body weight will stabilize when energy expenditure declines to the level of energy intake.
It may be more useful in understanding body weight regulation to examine how the body achieves macronutrient balance. As discussed earlier, acute changes in intake of alcohol, protein, or carbohydrate are rapidly balanced by changes in oxidation of each. In contrast, fat oxidation is not tightly linked to fat intake. As a consequence, positive or negative energy balance are largely conditions of positive or negative fat balance. Thus, the point at which a stable body weight and body composition is reached and defended is that point at which fat balance is achieved.
The two major factors which influence fat balance are amount and composition of food eaten and the total amount of physical activity. Positive fat balance can be produced by overconsumption of energy or restriction of physical activity. Positive fat balance will occur when any type of diet is overconsumed. During carbohydrate overfeeding, for example, carbohydrate oxidation increases to maintain carbohydrate balance, but because carbohydrate is providing more fuel for oxidative needs, fat oxidation is providing less than usual, creating positive fat balance (107).
Negative fat balance can result from underconsumption of total energy or fat or by an increase in the level of physical activity. During underconsumption of energy, the supply of the priority metabolic fuels (carbohydrate and protein) are insufficient to meet the body's energy needs. Thus, the remaining energy needs are met by fat oxidation which comes largely from endogenous fat stores. An increase in the level of physical activity will increase total energy requirements with the additional energy needs being met by increased fat oxidation.
Fat balance and body weight stability
There are two mechanisms by which a new steady-state of body weight and body composition achieved following a positive or negative perturbation in fat balance. First, changes in behaviour can lead to adjustments in either intake or oxidation of fat (e.g. altering total energy or fat intake and altering physical activity). Second, in the absence of sufficient behaviour changes, fat oxidation will be altered following alterations in the body fat mass. As an example of behavioural adjustments, the negative fat balance produced by reducing energy intake could be eliminated totally by a compensatory reduction in physical activity. As an example of metabolic adjustments, overconsumption of total energy and fat will produce positive energy balance. If behavioural adjustments are absent or insufficient, increases in the body fat mass will result. Increased body fat mass is associated with increased levels of circulating free fatty acids which elevate total fat oxidation. Thus, a stable body weight will be reached at the point where the body fat mass has increased sufficiently so that fat oxidation equals fat intake.
Metabolic differences between carbohydrate and fat
Based on known differences in macronutrient metabolism, we can begin to predict how the composition of the diet, and specifically the carbohydrate to fat ratio of the diet, might impact upon body weight regulation. It must be realized that the pathways by which nutrients are metabolized (particularly carbohydrate) vary with the overall state of energy balance and this must be considered when predicting the impact of diet composition. For example, conversion of carbohydrate to fat would occur during situations of excess carbohydrate intake and not under situations of normal or below normal intake.
Changing diet composition with no energy intake change
Altering diet composition without a change in total energy intake should have relatively modest effects on body weight and body fat content. There are at least two ways that such a change in diet composition could affect body weight. First, the thermic effect of carbohydrate is greater than the thermic effect of fat. Changing to a lower fat diet (assuming total energy and protein intake remain constant) means changing to a higher carbohydrate diet, which will increase total energy expenditure. The magnitude of increase in energy expenditure depends on the magnitude of change of the carbohydrate/fat ratio, but is probably relatively small and of questionable importance in body weight regulation for reducing dietary fat from 35-40% to 20-25% of total energy intake. Second, altering the carbohydrate/fat ratio of the diet requires that substrate oxidation rates be readjusted to the new macronutrient intakes. If total energy expenditure is not changed, these changes occur relatively rapidly, with carbohydrate and protein balance being reachieved more quickly than fat balance (108,109). Negative fat balance and some loss of body fat will occur until fat balance is reachieved. It is difficult to predict the rapidity with which fat balance will be reachieved following a reduction in fat (and an accompanying increase in carbohydrate intake).
Effects of diet composition during positive energy balance
It is during periods of positive energy balance that differences in carbohydrate and fat have the greatest impact upon body weight regulation. This is because of differences in the efficiency of metabolic pathways involved in disposing of excess carbohydrate vs. fat. One study (107) demonstrated that while the majority of excess energy is stored regardless of its composition, a greater proportion of excess energy is stored when the excess is from fat as compared to when the excess is from carbohydrate. This is a clear example of a situation where fat intake leads to more body energy storage than the same amount of energy from carbohydrate.
Total energy expenditure increases more with carbohydrate overfeeding than with fat overfeeding. This is because carbohydrate oxidation increases to a greater extent than fat oxidation decreases during carbohydrate overfeeding. The difference between carbohydrate and fat in the proportion of excess energy stored is greatest during the first week of overfeeding. This suggests that the more sustained the overfeeding, the less the difference between carbohydrate and fat overfeeding. If obesity develops due to brief, periodic episodes of overeating, differences between fat and carbohydrate are likely to be more important than if obesity develops from sustained positive energy balance.
Carbohydrate type and body weight regulation
The effects of different types of carbohydrates on body weight regulation have been reviewed recently (110). While there are clear differences in metabolism of carbohydrates and fat that could affect body weight regulation, there do not appear to be such metabolic differences between types of carbohydrate. The majority of comparisons have been made between simple sugars and complex carbohydrates. There is little scientific support for the commonly held perception that consumption of high amounts of simple sugar contributes to obesity. There is no evidence that simple sugars are used with a different efficiency than complex carbohydrates (other than dietary fibre or resistant oligosaccharides). While there is substantial data suggesting that high levels of dietary fat intake are associated with high levels of obesity, at present there is no reason to believe that high intake of simple sugar is associated with high levels of obesity.
Does carbohydrate make you fat?
The idea that increased insulin concentrations subsequent to carbohydrate intake lead to conversion of significant amounts of carbohydrate to fat is misleading. First, it takes an extreme excess of carbohydrate to produce de novolipogenesis, and even under these conditions, very little net fat is produced from carbohydrate. Second, the idea that persons with insulin resistance are particularly prone to become obese when eating high carbohydrate diets is unsubstantiated by scientific evidence. In fact, low-fat, high-carbohydrate diets are commonly recommended to prevent further weight gain for these individuals who are at risk to develop non-insulin dependent diabetes and coronary heart disease. Finally, substantial data suggest that voluntary energy intake is higher in many people when the diet is high in fat content and low in carbohydrate content. Excess consumption of energy in any form leads to accumulation of body fat. There is no serious scientific evidence to suggest, however, that diets high in carbohydrate promote weight gain when consumed in amounts which do not exceed energy requirements.
Prevention of obesity
Because excess dietary fat is stored more efficiently than excess dietary carbohydrate, eating a low fat diet may be helpful in obesity prevention. If one assumes that everyone overeats occasionally, less of the excess energy will be stored as adipose tissue if a low fat diet is consumed than a high fat diet. It remains prudent to recommend a high carbohydrate diet for body weight maintenance. Diets high in fat are likely to promote excess energy consumption and excess dietary fat is stored as adipose tissue with extremely high efficiency. Eating a high carbohydrate diet reduces the likelihood of overeating and, if overeating occurs, results in slightly less of the excess energy being stored as adipose tissue.
Alternative sweeteners
Dietary carbohydrates responsible for sweet taste are often replaced or substituted to varying extents by alternative sweeteners. The main reasons are to reduce the energy content of the diet, to minimise postprandial blood glucose fluctuations, to reduce cariogenicity, and to reduce cost.
Alternative sweeteners are defined as sweeteners other than sucrose. The term sweetener is mostly used for the high-intensity sweeteners (174) or for "any substance other than a carbohydrate whose primary sensory characteristic is sweet"(175), but sometimes to also collectively describe nutritive and non-nutritive sweeteners. The nutritive sweeteners are the mono and disaccharide sugars and a large variety of carbohydrate sweeteners that occur naturally in foods or are added in purified form (174).
The two main groups of alternative sweeteners that are used as sucrose substitutes or replacers, and classified on the basis of their function in foods, are the high intensity "non-nutritive" sweeteners and the "nutritive" bulk sweeteners or "sugar bulking" agents.
Non-nutritive sweeteners
Alternative sweeteners which are non-nutritive, non-carbohydrate, very low in calories and with an intense sweet taste, have been further grouped into three classes (176). First, the naturally occurring compounds such as monellin, thaumatin, miraculin, stevioside, steviol, etc., of which more than 30 have been identified and described. The second group includes the synthetic compounds saccharin, cyclamate, acesulfame, and others. The third group has two semi-synthetic compounds, neohesperidin dihydrochalcone (NHDC) and the dipeptide aspartylphenylalanine, also known as aspartame.
Nutritive sweeteners
Other alternative sweeteners are low-energy, bulk, sugar (sucrose) substitutes which are used not only for their sweet taste, but also to replace intrinsic functions of sugar in baked products, ice cream, frozen desserts, and other processed foods. These sugar substitutes are carbohydrates and are usually classified as nutritive sweeteners. They include glucose (dextrose), liquid glucose, high fructose syrups, liquid fructose, crystalline fructose, corn syrup, corn syrup solids, concentrated grape juice, invert sugar, invert syrups (174,175), and polyols, which are polyhydric alcohols produced by the hydrogenation of the corresponding reducing sugars.
The benefits of carbohydrate loading before prolonged submaximal exercise have been shown mainly during cycling. A link was demonstrated between endurance performance during cycle ergometry and pre-exercise muscle glycogen concentration (184). The importance of muscle glycogen during prolonged exercise was confirmed in subsequent studies which showed that fatigue occurs when muscle glycogen concentrations are reduced to low values (185-187). Therefore, it is not surprising that attempts were made to find methods of increasing muscle glycogen stores in preparation for prolonged exercise. One study (188) examined the influence of different nutritional states on the resynthesis of glycogen during recovery from prolonged exhaustive exercise. It found that a diet low in carbohydrate, and high in fat and protein for 2 to 3 days after prolonged submaximal exercise, produced a delayed muscle glycogen resynthesis, but when this was followed by a high carbohydrate diet for the same period of time, glycogen supercompensation occurred (see Figure 7). This dietary manipulation not only increased the pre-exercise muscle glycogen concentration but also resulted in a significant improvement in endurance capacity (see Figure 8). Although this original method of carbohydrate-loading was recommended as part of the preparation for endurance competitions, the low carbohydrate, high fat and protein phase of the diet is an unpleasant experience. Therefore, alternative ways were explored to increase the pre-exercise glycogen stores without including a period on a diet high in fat and protein (189). It was found that a carbohydrate-rich diet consumed for 3 days prior to competition, accompanied by a decrease in training intensity, resulted in increased muscle glycogen concentrations of the same magnitude as those achieved with the traditional carbohydrate loading procedure.
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