The Role of Energy Density Adam Drewnowski* Nutritional Sciences Program, School of Public Health and Community Medicine, University of Washington, Seattle, Washington 98195
ABSTRACT: Dietary energy density (ED) appears to have a major influence on the regulation of food intake and body weight. If people consume a fixed weight of food each day, then high-ED diets should be associated with high energy intakes and with overweight. In contrast, low-ED diets should result in lower daily energy intakes and therefore weight loss. For this approach to work, low-ED foods must be as palatable as high-ED foods and, calorie for calorie, have a greater satiating power. Each of those assumptions is debatable. Dietary ED depends chiefly on the water content of foods. As a rule, high-ED foods are more palatable but less satiating, whereas low-ED foods are more satiating but less palatable. Consumer preferences for high-ED foods can be explained in terms of good taste, low cost, and convenience. Low-ED foods, such as fresh produce, provide less energy per unit cost than do high-ED foods, which often contain added sugars and fats. Poverty and obesity may well be linked through the habitual consumption of a low-cost, high-ED diet. Paper no. L9242 in Lipids 38, 109–115 (February 2003)
Dietary energy density (ED) is said to have a major effect on energy intakes (1–3) and on the long-term control of body weight (4–6). ED has replaced fat content as the principal dietary variable of interest in obesity research (5–8). The World Health Organization (WHO) recently identified high dietary ED as a principal contributor to the global obesity epidemic. High-ED foods and high-ED diets are increasingly held responsible for the rising prevalence of obesity and overweight (9). Any connection between dietary ED and obesity rests on the premise that people consume a constant weight of food each day, as opposed to a constant amount of energy (3,7,10). Selecting high-ED foods would then increase daily energy intakes and lead to weight gain. In contrast, bulky low-ED foods provide fewer calories per unit volume and deliver less energy per eating occasion (3,12). In principle then, low-ED food choices should result in lower daily energy intakes and therefore weight loss. High-ED diets have been associated with obesity, whereas lowering dietary ED may be a promising approach to weight reduction (11–13). For the ED approach to work, low-ED and high-ED foods should be equally palatable and have the same satiating power. The overall goal is to make the consumer feel full on *To whom correspondence should be addressed at 305 Raitt Hall #353410, University of Washington, Seattle, WA 98195. E-mail:
[email protected] Abbreviations: ED, energy density; FPC, food preference checklist; NHANES, National Health and Nutrition Examination Survey; SI, satiety index. Copyright © 2003 by AOCS Press
fewer calories (10,13). Raw vegetables and fruit, salad greens, soups, and beverages provide between 0.1 and 0.5 kcal/g (5) and have long been available for human consumption. Yet consumers often prefer high-ED sweet and high-fat foods, including snacks, confectionery, sweets, and other desserts (14–16). The ED approach makes a secondary assumption that low-ED foods, those with fewer calories per unit weight, are as satiating as high-ED foods (10,13). In other words, energy density, palatability, and satiety must be independent variables (17). Although ED and palatability have been separated under tightly controlled laboratory conditions (5,7,18,19), it is unclear whether they are separable in real life. High-ED foods tend to be more palatable than low-ED foods because they often contain fat, sugar, or both (15). Foods that are overconsumed are by definition less satiating than foods that are consumed in smaller amounts (5). As will be demonstrated below, palatability and satiety are inversely linked. As a rule, high-ED foods are palatable but not satiating, whereas lowED foods are more satiating but less palatable (5,17). To complicate matters, high dietary ED may be linked to lower food costs. Generally, packaged high-ED foods are less expensive than perishable fresh produce, when expressed in terms of dietary energy per unit cost (kcal/$) (20). Reducing the ED of the total diet may therefore involve certain tradeoffs with respect to palatability, satiety, and the economics of food choice. Interactions among these variables are the focus of this review. WHAT IS DIETARY ED? The ED of individual foods is a function of their water content. Although early studies emphasized the links between ED and the fat content of foods (1,4), water was, in fact, the determining variable (5). Table 1 shows that the highest-ED foods are those that contain the least water. Dietary energy is provided by fat, carbohydrates, and in some cases sugar (5). The extremes of the ED spectrum are represented by vegetable oil (9 kcal/g) and diet soft drinks (0 kcal/g). The relationships between ED and the nutrient composition of some common foods are summarized in Figures 1–5. These analyses are based on a 171-item food preference checklist (FPC) that listed a variety of meats, dairy products, grains, vegetables, and fruit as well as alcohol, sugars, oils, and fats (21–23). The food list was adapted from past analyses of National Health and Nutrition Examination Survey (NHANES) II data (24). Comparisons of the FPC with food
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TABLE 1 Energy Density and Water Content of Selected Common Foods Food item
Energy density (kJ/g) (kcal/g)
Safflower oil Peanuts, dry Candy, milk chocolate Cereal, granola type Doughnut, cake type Potatoes, french-fried Pizza, cheese Ice cream sundae Ham, lean Spaghetti with tomato sauce Potato, baked Yogurt, fruit-flavored Soup, split pea Yogurt, low-fat plain Orange, raw Soda, cola type Spinach, boiled Tomato juice Salad, green Soda, diet type
36.8 24.4 22.6 19.5 17.8 12.9 9.3 7.5 6.6 5.6 4.6 4.4 3.1 2.6 2.0 1.7 1.0 0.7 0.7 0.0
8.9 5.8 5.4 4.7 4.3 3.1 2.2 1.8 1.6 1.3 1.1 1.1 0.8 0.6 0.5 0.4 0.2 0.2 0.2 0.0
Water content (g/100 g) 0 1 1 5 20 40 48 60 66 70 71 85 86 85 87 89 91 94 96 100
frequency questionnaires have been published previously (21–23). High-ED foods contain less water per unit weight (Fig. 1). Low-ED foods were vegetables and fruit, whereas high-ED foods included spreads, oils, and fats. The fat content was also related to the ED of foods (Fig. 2). Multiple regression analysis showed that water content alone accounted for 85% of the variance in ED, whereas water and fat together accounted for 99%. Carbohydrate (including sugar), protein, and fiber content of foods played a decidedly lesser role, as indicated in Figures 3–5. Because of their high water content, raw vegetables and fruit rarely provide more energy than 0.5 kcal/g (2 kJ/g). High water content also keeps the ED of beverages, juices, and soups below 1.0 kcal/g (4.0 kJ/g). Yogurt, ice cream, and some meats are other foods with a relatively high water content. As an al-
FIG. 1. The relationship between energy density (kJ/g) and water content of foods.
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FIG. 2. The relationship between energy density (kJ/g) and fat content of foods.
FIG. 3. The relationship between energy density (kJ/g) and carbohydrate (CHO) content of foods.
ternative to adding water, the ED of foods can be lowered by replacing caloric sugar and fat with low-energy equivalents. Intense sweeteners reduce the ED of soft drinks to zero while maintaining their sweetness (16). To some extent, the ED of foods can also be lowered by incorporating dietary fiber or partially digestible starches, gels, and gums that mimic the texture and mouthfeel of dietary fat (15). The challenge is to reduce dietary ED while keeping palatability constant.
FIG. 4. The relationship between energy density (kJ/g) and protein content of foods.
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FIG. 5. The relationship between energy density (kJ/g) and fiber content of foods.
ED AND PALATABILITY Arguably, foods are palatable because they are energy dense (5,17). Sensory enjoyment of sugar and fat is directly related to the fact that both represent concentrated and readily available sources of dietary energy. Although concentrated energy is rewarding per se, there seems to be no physiologic drive to select bulky low-ED foods that provide a fraction of a calorie per gram. High-ED chocolate tastes better to most people than low-ED spinach, and is consumed with more pleasure and satisfaction. Given a choice, young children prefer high-ED foods to foods that deliver less energy per unit weight (25,26). The question is whether high-ED foods are indeed more palatable than low-ED foods. Chocolate cake, hamburgers, and french fries provide from 12 to 18 kJ/g. Chocolate candy and peanut butter provide 22–24 kJ/gram. In contrast, most salad greens are low-ED foods, providing <1 kJ/g. By definition, there are no high-ED beverages. ED values of regular cola, orange juice, and 1% milk are almost exactly the same at 2 kJ/g. Apart from anecdotal reports, the relationship between ED and food palatability is not well documented. Food preference studies tend to rely on self-reported preferences for food names, not for actual foods. The best such data were obtained from persons least subject to social desirability concerns or dietary restraint, in other words, children. A reanalysis of data obtained with 4-yr-old children in the United Kingdom (27) showed that their food preferences were related to the sweetness and ED of foods (Fig. 6). The best-liked foods were either energy dense or sweet. A positive relationship between ED and food preferences had also been observed in young and mostly male Army personnel (5,28). Food preference data obtained from college-age women are altogether different. Although children and young men prefer high-ED potato chips to yogurt and fruit, many young women report precisely the opposite. In a sample of 159 college women, raspberries were the most highly preferred food, outranking chocolate, french fries, and pizza. There was no significant correlation between ED and food preferences. In past studies, young women suffering from the eating disorder anorexia nervosa also reported higher preferences for salad
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FIG. 6. The relationship between energy density and self-reported food preferences for 4-yr-old children in the United Kingdom [based on data from Wardle et al. (27)].
greens than for ice cream or chocolate (29,30). Similarly, older women reported higher preferences for fresh vegetables and fruit than for higher-ED foods (21). The relationship between ED and food palatability, as measured by selfreported food preferences, is strongly influenced by age, gender, and diet-related attitudes and behaviors. Although observed among children and young men, it has not been observed consistently among women. DIETARY ED AND SATIETY Feeling full on fewer calories requires that satiety be influenced not only by dietary energy but also by the weight or volume of the foods consumed (10,13). Most laboratory studies on ED and satiety have addressed this issue using a study design known as the preload paradigm (17). In such studies, ingestion of a caloric preload was followed by repeated measures of hunger and satiety and by the eventual consumption of a test meal. Preload ED was manipulated by keeping preload energy constant while altering volume, or by keeping volume constant while altering energy. In most studies, preload volume was altered by using water. Preload energy was also altered by using fat, sugar, intense sweeteners, fat replacement products, and sometimes fiber (11,12,18,19). In fact, many studies in this area were focused not so much on ED but on the effect of intense sweeteners and fat replacements on hunger and satiety (31–34). Studies that provided subjects with preloads of constant volume but different energy yielded inconsistent results. Some did demonstrate differences in hunger and satiety between low-ED and high-ED conditions, whereas others did not. In our studies (18,19), participants consumed a breakfast consisting of large volume (500 g) of fromage blanc (a soft creamy white cheese) that was sweetened with sucrose (700 kcal) or aspartame (400 kcal). Although preload volume was constant, the ED varied from 2.5 to 5.8 kJ/g. Participants reported being equally satiated by high-ED and low-ED preloads in the first 30 min postingestion. However, it would be
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incorrect to assume that energy had no effect on satiety. Measurable differences in hunger, fullness, and satiety scores became apparent later, reaching a peak ~2 h postingestion. Studies in which the time interval between preload and the test meal is <20 min are liable to conclude, incorrectly, that preload energy has no effect on satiety. Although regular and diet soft drinks may have the same initial effect on hunger and satiety, the effect of calories does become apparent with time (35). Studies that kept preload energy constant and varied preload volume showed more agreement. Isoenergetic preloads with higher volume promoted satiety more effectively, at least in the short term (2,3). Those data are consistent with the notion that satiety is influenced primarily by dietary energy and that preload volume may have some additional effects that are observed shortly postingestion. Recently, studies of ED have gone beyond the standard manipulations of water, sugar, and fat. One study varied ED by altering the proportion of vegetables to pasta in a pasta salad (3). Study subjects given meals of varying ED consumed the same amount of food by weight so that energy intakes were a direct function of ED level (3). As a result, subjects in the low-ED condition consumed 30% less energy over a 2-d period without a major reported effect on hunger or satiety. Matching foods for palatability was a critical part of study design because reduced consumption of low-ED foods might be explained by their reduced appeal and lower palatability. As semiliquid preloads are replaced by real foods, the palatability issue becomes more of a problem. The satiety index (SI) of foods was an early attempt to map the relationship between ED and satiety. In that study (36), satiety ratings were measured every 15 min for 2 h after the consumption of 240-kcal portions of 38 common foods. The SI was calculated by dividing the area under the curve for each food by that for white bread and multiplying by 100%. SI values were correlated most highly with food weight, i.e., with ED. A ration of 240 kcal was provided by 38 g of peanuts or by 625 g of oranges (36). As might be expected, the more bulky and low-ED foods had the highest SI values, with potatoes, porridge, and fish proving to be more satiating than chocolate, cookies, and cakes. However, in that study, as in many others, the most satiating foods were also rated the least palatable (36). PALATABILITY AND SATIETY Researchers have struggled to explain why people overeat high-ED foods, especially those that contain sugar and fat. Some have argued that the high palatability of sweet and high-fat foods overrides normal satiety signals, thereby leading to overeating and overweight (37–40). The question was whether such foods were overeaten because of their high ED or their high fat content. Some researchers have argued that satiety effects were macronutrient specific, and that fat was less satiating than an isocaloric amount of carbohydrate or protein. Indeed, the phrase “passive overconsumption” was launched to account for the overeating of fat-rich foods (40). Lipids, Vol. 38, no. 2 (2003)
Other researchers believe that satiety is volume driven, such that bulky low-ED foods are more satiating, independent of their fat content. Palatability and satiety, or more properly satiation, have opposite effects on food intakes. Palatability increases appetite and therefore energy intakes, whereas satiation limits consumption by reducing meal size and satiety delays the time to the next meal (5,17). Palatability is the property of the food itself, coupled with the appetitive state of the consumer. Commonly used measures of palatability include the rated pleasantness of a given food, intent to eat, and the amount of food consumed (5). Satiation, defined as an internal state of energy repletion after a meal, has been measured in terms of fullness, reduced intent to eat, and reduced amount of food consumed (5,17). Satiety has also been measured in terms of reduced palatability. For example, sensory-specific satiety was defined in terms of reduced palatability of the just-consumed food relative to other foods (41). In other words, our measures of palatability and satiation are inversely linked (5,17). The most palatable foods are, by definition, the least satiating and vice versa. As shown by Holt et al. (36), the more palatable cake, cookies, and chocolate were less satiating than the less palatable porridge, potatoes, and boiled fish. If palatability and satiety are inversely linked, then the creation of highly palatable and yet satiating foods is a contradiction in terms. Laboratory studies on ED and satiety have tried to keep palatability constant. Their chief intent was to demonstrate that low ED foods could be just as palatable as high-ED foods and just as acceptable to the consumer. In some cases, reducing ED had no effect on palatability ratings. However, the ED of most test foods was already low (3-4 kJ/g) and was allowed to vary within only a narrow range, from 3 to 6 kJ/g (2,3,7). All test stimuli had a high water content and included yogurts, soups, and a semiliquid white cheese, fromage blanc (5). Maintaining good taste while varying ED over a broader range may present more of a challenge. ED OF THE DIET Most studies on ED have been based on individual foods, single dishes, or single meals (5,6), although a few have addressed the ED of the total diet (42–44). Dietary ED is difficult to establish because there is little consensus concerning whether water, noncaloric beverages, caloric beverages, soups, semiliquids, or semisolids ought to be included or excluded from analyses. Current research suggests that water consumed as a beverage and water incorporated into fruit, juices, or soups may have a differential effect on satiation and satiety (45). Diet structure may turn out to be the more important variable because different types of diets may have similar ED values. Whether people consume a fixed weight or volume of food and beverages each day is not always clear. Although this may be the case under laboratory conditions (3,5), epidemiologic surveys suggest that the weight of foods and beverages
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FIG. 7. Mean amounts of food (g) consumed by age group in the NHANES II data (1976–1980).
declines sharply with age. A reanalysis of 1976–1980 data from the NHANES II survey (46) showed that both energy intakes and the weight of foods and beverages declined with each advancing decade of life (47). Older adults in the NHANES II data set consumed progressively less food (Fig. 7). Energy intakes also declined as a function of age. The mean dietary ED was influenced by both sex and age (47) (Fig. 8). Dietary ED dropped from a peak of 1.2 kcal/g in childhood and adolescence to a low of 0.7 kcal/g for adult women 45–54 yr old. Given that intakes of vitamin C (mg/1000 kcal) increase steeply after the age of 35 yr, particularly for women, it seems likely that the reduction in dietary ED was achieved through increased consumption of vegetables and fruit. Age-associated increases in vegetable and fruit intakes, observed in other studies, are wholly consistent with that hypothesis. In fact, an argument has been made that varying the energy density of foods is the body’s prime mechanism for regulating energy intakes during the life cycle. Although children, adolescents, and young adults consume high-ED diets, older adults may reduce energy intake by reducing both food volume and dietary ED (48).
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Dietary ED is strongly affected by age. Aging is associated with lower energy intakes, lower intakes of fat and saturated fat, and higher intakes of dietary fiber, vegetables, and fruit (46,49). Older adults consume more whole grains, vegetables, more cruciferous vegetables, green leafy and other vegetables, and more fruit than do younger adults (49). Adults over the age of 59 yr are more likely to consume fruit, tomatoes, breakfast cereals, and whole-grain breads than those 18–59 yr old and less likely to consume sweets, snacks, and carbonated sugar-based beverages (50,51). Consumption of at least five servings of fruit and vegetables per day (50) also rises with age. Data obtained from 23,699 adults in 16 U.S. states, as part of the Behavioral Risk Factor Surveillance System, showed that twice as many women over the age of 65 yr (29%) complied with the five-a-day diet compared with women aged 18–24 yr (14%) (51). DIETARY ED AND FOOD COSTS The fact that dietary ED is primarily a function of the water content of foods has economic consequences. Packaged, dry, high-ED foods with a stable shelf life provide more energy per unit cost than perishable low-ED fresh produce with a high water content. As noted in Table 2, lower-ED foods typically provide fewer calories per unit cost than do high-ED foods. Consumers select foods on the basis of taste, cost, and convenience (52), with cost being of most concern to lowincome families. Not surprisingly, higher-income groups in both Britain and the United States tend to have higher-quality diets (53–55). Obesity, in turn, is associated with limited economic resources, and low levels of education and income. Compliance with dietary guidelines for health promotion is often poor, especially among low-income respondents. Studies on dietary compliance in weight loss have addressed a variety of metabolic and cognitive variables, from glycemic index to information about the fat content of foods. Yet concerns about the increased cost of low-ED diets have not become a part of mainstream obesity research. The possibility remains that food expenditures are a major barrier to dietary change. Simply put, palatable high-ED foods containing sugar and fat provide more energy per unit cost than any low-ED
TABLE 2 Energy Density and the Cost of Selected Foods (kcal/$) Food item
FIG. 8. Mean energy density of the diet (kcal/g) by age group in the NHANES II data (1976–1980).
Oil (1 tbs) Peanuts, roasted (1 oz) Chocolate bar, Hershey (1.5 oz) Cheese nachos (7 oz) Ice cream, Häagen Dazs (1 cup) Sirloin steak (8 oz) Fruit yogurt, low-fat (8 oz) Apple (1 fruit) Broccoli, cooked (1/2 cup) Spinach, raw (1 cup)
Energy density (kcal) (kcal/g) 120 180 230 810 540 390 230 90 20 10
8.8 5.9 5.3 4.0 2.5 1.6 1.0 0.6 0.3 0.2
(kcal/$) 3852 1147 460 967 332 260 291 270 170 90
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|alternatives. A relationship between ED and food costs for selected foods is outlined in Table 2. DIETARY ED AND BODY WEIGHT Higher-ED diets are linked to increased consumption of fast foods, sweets, and desserts. Lower-ED diets are associated with increased consumption of vegetables and fruit. Studies have linked obesity to fat consumption and to the percentage of fat energy in the total diet. Although dietary ED and dietary fat content are linked, there is no population-based evidence at this point that high-ED diets are associated with obesity in either women or men. It remains to be demonstrated that ED alone, independent of fat content, is the causal factor in promoting body weight gain. Reducing dietary ED can be accomplished by selecting more bulky and lower-ED foods that provide fewer calories in a larger volume. Laboratory studies suggest that such foods can be as palatable and as satisfying as high-ED foods. Real-life experience suggests otherwise. High-ED foods containing fat, sugar, and sometimes salt tend to be more palatable than lowerED options. Packaged high-ED foods are arguably more convenient to use, and eating away from home provides a variety of high-ED options. Perhaps most important, high-ED is often associated with lower food costs, expressed as calories per dollar. Lowering dietary ED may be a potent option for weight reduction and it is currently being promoted as such. However, consumers’ food choices are based largely on taste, cost, and convenience. For the purposes of obesity research, food costs and the economics of food choice merit a closer look.
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Lipids, Vol. 38, no. 2 (2003)