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(Journal of Nutrition. 2000;130:268S-271S.)
© 2000 The American Society for Nutritional Sciences


Supplement

The Role of Energy Density in the Overconsumption of Fat1 ,2

Barbara J. Rolls

Nutrition Department, Pennsylvania State University, University Park, PA 16802-6501


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
In recent years, research has focused on why fat is so readily overconsumed. Although the palatability of many high fat foods can encourage overconsumption, another possibility is that fat is not very satiating. A number of studies have compared the effects of fat and carbohydrate on both satiation (the amount eaten in a meal) and satiety (the effect on subsequent intake), but have found little difference between these macronutrients when the palatability and energy density were similar. On the other hand, the energy density of foods has been demonstrated to have a robust and significant effect on both satiety and satiation, independently of palatability and macronutrient content. It is likely that the high energy density of many high fat foods facilitates the overconsumption of fat. An understanding of the role that the energy density of foods plays in the regulation of food intake should lead to better dietary management of hunger and satiety in conditions associated with both over- and underconsumption of energy, such as obesity and anorexia.


KEY WORDS: • energy density • fat intake • human food intake • hunger • satiety


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
The energy density of foods (kJ/g) is a key determinant of energy intake. This is not a new suggestion, but it has gained considerable support recently. Studies aimed at understanding why dietary fat is overconsumed have indicated that the high energy density of fat plays an important role. In this review, we will discuss recent studies that have led to new understanding of the role of the energy density of foods in energy intake.

During the 1990s, studies of energy intake have tested the hypothesis that the macronutrients can have different effects. Of particular importance for this review is the suggestion that dietary fat is overeaten because it affects satiety and satiation less than carbohydrate and protein (Rolls and Hammer 1995Citation ). The methods used to study satiety (the effect on subsequent intake) and satiation (the amount eaten in a meal) differ; therefore, the results from these studies will be considered separately.


    Do macronutrients differ in their effects on satiety?
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
Satiety refers to the effects of a food or meal after eating has ended. To study satiety, a fixed amount of a defined food (a preload) is consumed; after an interval of time, the effect of the preload on subsequent intake is measured. In this review, only studies investigating early satiety, that is, satiety occurring within 30 min after the preload, will be considered. Although a number of studies have found a hierarchy of the effects of the macronutrients on early satiety such that protein had the greatest effect, followed by carbohydrates, with fat as the least effective, many of these studies did not adequately control for differences in the palatability or energy density of the test foods (Rolls and Hammer 1995Citation , Prentice 1998Citation ).

We have published several reviews of the studies comparing the effects of fat and carbohydrate on food intake (Rolls and Hammer 1995Citation , Rolls and Bell 1999Citation ). In studies of satiety, the fat and carbohydrate content of a preload had similar effects on subsequent food intake when the palatability and energy density were matched. This was seen when the foods were ingested orally or infused intravenously or intragastrically. In one study, however, fat ingested in yogurt preloads suppressed lunch intake slightly (but significantly) less than carbohydrate in some of the participants who were obese or concerned with their body weight (Rolls et al. 1994Citation ). Although the difference was small, even small differences could have an influence on energy balance over time.


    The role of the energy density of food in satiety
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
Because fat contains 37.6 kJ/g compared with 16.7 kJ/g for carbohydrate and protein, high fat foods are often high in energy density. If a food is high in fat, even small portions may have a high energy content. If the amount of food (weight or volume) plays a role in the regulation of food intake, a plausible hypothesis is that the energy density of a food can affect both satiety and satiation, and that this is at least part of the explanation for the excess consumption of fat.

To test the effect of the energy density of a food on satiety, the palatability and the macronutrient and energy content of a preload should be similar, whereas the energy density changes. For example, the addition of water will increase the weight or volume, thus decreasing the energy density. This was done in a recent study in which lean young men were served a milk-based preload that had varying amounts of water added to change the volume (300, 450 and 600 mL) but not macronutrient content or palatability (Rolls et al. 1998Citation ). Because the total energy content was held constant (2088 kJ), the preloads varied in energy density. The results showed that energy density of the preload affected energy intake at lunch 30 min later such that intake was significantly lower by 18% after the high volume, low energy density drink than after the low volume, high energy density drink. Furthermore, the men in the study did not compensate at dinner for the reduced intake at lunch. These results demonstrate that the weight or volume of food consumed, and thus the energy density, can affect satiety.

In general, the water content of foods is a critical determinant of energy density; it has a larger effect than other ingredients such as fat or fiber. We saw in the previous experiment that adding water to a food increased the effect of the food on satiety. It is of both practical and theoretical interest to determine whether the addition of water affects intake simply by increasing the volume in the stomach, or if an increased volume of food affects satiety through sensory and cognitive influences. For example, a food with added water will look bigger and will likely cause greater stimulation of oropharyngeal mechanisms. One way to separate these influences is to test subjects with the food and water consumed separately and to compare the effects with those when the food and water are mixed together. In a recent study, we developed a chicken, rice and vegetable casserole containing 1128 kJ and weighing 263 g (Rolls et al. 1999bCitation ). The base of this casserole was undiluted cream of chicken soup; thus water could be added to the casserole to make a soup. The casserole and soup had exactly the same ingredients except for the additional 356 g of water in the soup. In a third condition, the casserole was served with a glass of water equivalent to the amount of water that had been added to make the soup. When the women in the study ate lunch 5 min after finishing the preloads, the water affected how much was eaten, but only when it was incorporated into the casserole to make a soup. The women ate similar amounts when the casserole was served with and without a glass of water. When they consumed soup, however, they felt fuller and less hungry and consumed ~27% less energy compared with intake at lunch after the casserole. The subjects did not compensate at dinner for this reduction in lunch intake. This study showed that water had to be incorporated into a food, thereby increasing its weight or volume, to influence satiety.

The effects of the energy density of foods on satiety are robust and of a magnitude that implies that they are an important influence on the regulation of energy intake. When the macronutrient content of foods is varied, but the energy density is kept constant, the effects of fat and carbohydrate on satiety are similar. When the palatability of foods is similar, energy density is the major determinant of how foods affect satiety regardless of macronutrient content.


    Do macronutrients differ in their effects on satiation?
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
Satiation refers to the processes involved in the termination of a meal. It is studied by providing individuals with foods varying in composition and measuring the amount consumed when the food is freely available. In this review, the critical question is whether the fat content affects how much is eaten in a meal. In studies of satiation, it is important to match the palatability of the foods when they are compared. If it is not, the fact that one food tastes better than another could override any effects of the nutrient composition on amount consumed (Drewnowski 1998Citation ). In addition, to study the specific effects of macronutrients, they must be manipulated independently of energy density.

Most of the early studies on the effects of the fat content of foods on satiation varied the amount of fat in the available foods without concern for the confounding effects of differences in palatability and energy density (Rolls and Hammer 1995Citation , Rolls and Bell 1999Citation ). In these studies, which lasted from a single meal to 11 wk, the higher the fat content and the energy density, the greater the daily energy intake. When the participants in these studies were allowed free access to the manipulated foods, they ate a similar amount by weight of food regardless of the composition (Duncan et al. 1983Citation , Kendall et al. 1991Citation , Lissner et al. 1987Citation , Miller et al. 1998Citation , Stubbs et al. 1995Citation ). The results demonstrated consistently that the weight of food consumed daily was more constant than energy intake over periods as long as 11 wk (Kendall et al. 1991Citation ).

The tendency to consume a constant weight of food was confirmed by an analysis of 4-d weighed food records from 45 nonobese adults (Seagle et al. 1997Citation ). The weight of food consumed remained more constant over a day than either the intake of energy or fat. Similarly, an analysis of reported intakes in large community samples showed there was little adjustment in the amount of food consumed to compensate for variations in the energy density of the total diet (Poppitt and Prentice 1996Citation ). All of these studies showing that people eat a constant weight or volume of food imply that energy density will be a critical determinant of energy intake. Because high fat foods are often high in energy density, this could be at least part of the explanation for the high intake of fat. Of importance for the present discussion of the effects of dietary fat on intake is whether fat affects satiation independently of the effects on energy density.

Several studies have tested the effects of variations in the fat content of foods while holding the energy density constant. In one study, liquid diets varying in fat content (24 vs. 47%) but similar in energy density were compared (van Stratum et al. 1978Citation ). Most of the energy consumed by the Trappist nuns in this study was from the liquid diets that were offered ad libitum, with standardized snacks contributing 25% of energy intake. Over the 2 wk on each diet, the women consumed a constant weight of the manipulated liquid diet, and thus energy intake remained constant. This was the first study to demonstrate that the fat content of foods per se did not have an independent effect on satiation. This finding was confirmed in another study in which six men of normal weight were offered each of three 14-d diets varying in fat content (20, 40 or 60% of energy) but similar in energy density (Stubbs et al. 1996Citation ). Again, subjects ate a constant weight of food so that energy intake did not differ among conditions despite the large difference in fat content. More recently, Saltzman et al. (1997)Citation fed men diets containing foods varying in fat content (20 vs. 40%) but matched for energy density. The energy intakes when these diets were consumed were similar over the 9 d of each dietary condition, again suggesting that the level of fat per se did not affect intake. These three studies indicate that the amount of fat in the diet did not influence satiation when the energy density was held constant.


    Does the energy density of foods affect satiation?
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
Although fat has an effect on the energy density of foods, it is possible to vary energy density while holding the fat content constant by adding water or ingredients with high water content. In a recent study, women of normal weight consumed all of their meals in the laboratory over three 2-d periods (Bell et al. 1998aCitation ). The entrees, which were available ad libitum at lunch and dinner, were similar in fat content but varied in energy density. This was achieved by adding more high water content vegetables to lower the energy density. Entrees were rated as equally palatable. The energy densities of the three diets were as follows: low, 4.3 kJ/g; medium, 4.9 kJ/g; and high, 5.6 kJ/g. The women ate a similar weight of food across conditions so that daily energy intakes varied directly with the energy density of the diets. They consumed ~30% less energy daily with the diet of low energy density than with the diet of high energy density, but there were no differences in the ratings of hunger and fullness. These results provide clear evidence that the energy density of food can affect satiation independently of macronutrient content and palatability.


    Variations in the fat content or energy density of a portion of the diet
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
In the previous study, the energy density of the entire diet was manipulated, and energy density was shown to influence energy intake. It is likely, however, that when individuals attempt to modify their diets, they may alter the energy density or the fat content of some but not all foods. Thus, it is of interest to modify experimentally a portion of the diet to determine whether compensation is seen when the participants can choose whatever else they want to eat.

We manipulated the energy density and/or the fat content of part of the diets of lean and obese women over 4 d to determine the effect on energy intake (Rolls et al. 1999aCitation ). In three of these 4-d test periods, subjects were served compulsory entrees which represented 50% of their usual energy intake at breakfast, lunch and dinner. Additional foods could be consumed ad libitum during and between meals. The results showed that variations in the fat content (16.4 vs. 36.5% energy) had no effect on energy intake. In contrast, the energy density of the compulsory foods did affect energy intake over the 4 d in both the lean and obese women. Intake of self-selected foods at meals was reduced significantly by 16% in the low (4.4 kJ/g) compared with the high energy density (6.7 kJ/g) condition. Ratings of hunger did not differ between the diets. The results showed that when a portion of the diet was manipulated, energy density, but not the fat content, affected energy intake.


    How does energy density affect energy intake?
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
Studies are required to determine why energy density exerts such a powerful influence on energy intake. The studies we have reviewed imply that there is a tendency for people to eat a constant weight of food. It seems likely that through a lifetime of eating experiences, people learn how satiating various foods are, and they eat amounts that conform to this expectation. Foods, even of the same type, however, can vary widely in energy density. These variations in energy density will affect energy intake.

In addition to learned influences, the sensory cues associated with changes in the amount of food consumed are likely to be important. Seeing a large portion of food and then tasting, chewing and swallowing it are likely to enhance satiety. Sensory-specific satiety has been shown to be affected by the amount of food consumed rather than the energy content (Bell et al. 1998bCitation ). Gastric distension and stomach emptying can also be affected by the energy density of foods. The rate at which nutrients reach satiety receptors and release satiety hormones could be affected by the energy density of food. Future studies should determine how the behavioral and physiologic effects of the energy density of food together lead to satiety and satiation.


    Clinical implications
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 
An understanding of how the energy density of food affects energy intake and satiety will lead potentially to better management of any condition that is related to over- or underconsumption of energy. A recent example of the clinical utility of understanding the effect of energy density comes from a study of elderly hospitalized patients, a population in which anorexia is common (Olin et al. 1996Citation ). It was found that a significant increase in energy intake could be achieved by increasing the energy density of regular hospital food. Intake was affected more by the volume consumed than by the energy content. On the other hand, lowering the energy density of the core foods in a weight management plan has the potential to lower energy intake while maintaining a reduction in hunger and an increase in satiety (Hammer and Rolls 1997Citation ), but at present there are no long-term clinical studies of the effects of energy density independent of variations in fat content. There is a need for such clinical studies using interventions focused on lowering the energy density of the diet to determine whether the effects persist.

Because the critical importance of the energy density of foods has been demonstrated only recently, there are few data available on the typical energy densities of diets consumed by populations (Poppitt and Prentice 1996Citation ). In the future, community studies should include data on energy density. This will require weighed intakes and records of fluid consumption. Although laboratory studies did not show a critical effect of water as a beverage on energy intake, the effect of energy-containing beverages may be important (Rolls et al. 1999bCitation ). Assessment of diet records over several days indicates that obesity is associated with the consumption of foods high in energy density (McCrory et al. 1999Citation , Westerterp-Plantenga et al. 1996Citation ). Population studies are required to assess the energy densities of the total diet, not only in groups of different body weights, but also in other groups at nutritional risk such as the elderly.


    FOOTNOTES
 
1 Presented at the symposium entitled "Dietary Composition and Obesity: Do We Need to Look Beyond Dietary Fat?" as part of the Experimental Biology 99 meeting held April 17–21 in Washington, DC. This symposium was sponsored by the American Society for Nutritional Sciences and was supported in part by an educational grant from the ILSI Research Foundation. The proceedings of this symposium are published as a supplement to The Journal of Nutrition. Guest editors for this supplement were Susan R. Roberts, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, MA and Melvin B. Heyman, University of California, San Francisco, CA.

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2 Supported by the National Institute of Diabetes and Digestive and Kidney Diseases (grants DK-39177 and DK-50156).

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    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 Do macronutrients differ in...
 The role of the...
 Do macronutrients differ in...
 Does the energy density...
 Variations in the fat...
 How does energy density...
 Clinical implications
 REFERENCES
 

1. Bell E. A., Castellanos V. H., Pelkman C. L., Thorwart M. L., Rolls B. J. Energy density of foods affected energy intake in normal-weight women. Am. J. Clin. Nutr. 1998a;67:412-420[Abstract]

2. Bell E. A., Thorwart M. L., Rolls B. J. Effects of energy content and volume on sensory-specific satiety. FASEB 1998b;12:A347(abs.)

3. Drewnowski A. Energy density, palatability, and satiety: implications for weight control. Nutr. Rev. 1998;56:347-353[Medline]

4. Duncan K. H., Bacon J. A., Weinsier R. L. The effects of high and low energy density diets on satiety, energy intake, and eating time of obese and nonobese subjects. Am. J. Clin. Nutr 1983;37:763-767[Abstract/Free Full Text]

5. Hammer V. A., Rolls B. J. Diet composition and the regulation of food intake and body weight. Dalton S. eds. Obesity and Weight Management: The Health Professional’s Guide to Understanding and Treatment 1997:254-283 Aspen Publishers Gaithersberg, MD

6. Kendall A., Levitsky D. A., Strupp B. J., Lissner L. Weight loss on a low-fat diet: consequence of the imprecision of the control of food intake in humans. Am. J. Clin. Nutr. 1991;53:1124-1129[Abstract/Free Full Text]

7. Lissner L., Levitsky D. A., Strupp B. J., Kalkwarf H. J., Roe D. A. Dietary fat and the regulation of energy intake in human subjects. Am. J. Clin. Nutr. 1987;46:886-892[Abstract/Free Full Text]

8. McCrory M. A., Fuss P. J., McCallum J. E., Yao M., Vinken A. G., Hays N. P., Roberts S. B. Dietary variety within food groups: association with energy intake and body fatness in men and woman. Am. J. Clin. Nutr. 1999;69:440-447[Abstract/Free Full Text]

9. Miller D. L., Castellanos V. H., Shide D. J., Peters J. C., Rolls B. J. Effect of fat-free potato chips with and without nutrition labels on fat and energy intakes. Am. J. Clin. Nutr. 1998;68:282-290[Abstract]

10. Olin A. O., Osterberg P., Hadell K., Armyr I., Jerstrom S., Ljungqvist O. Energy-enriched hospital food to improve energy intake in elderly patients. J. Parent. Enteral Nutr. 1996;20(suppl. 2):93-97[Abstract/Free Full Text]

11. Poppitt S. D., Prentice A. M. Energy density and its role in the control of food intake: evidence from metabolic and community studies. Appetite 1996;26:153-174[Medline]

12. Prentice A. M. Manipulation of dietary fat and energy density and subsequent effects on substrate flux and food intake. Am. J. Clin. Nutr. 1998;67(suppl. 3):535S-541S[Abstract]

13. Rolls B. J., Bell E. A. Intake of fat and carbohydrate: role of energy density. Eur. J. Clin. Nutr. 1999;53(suppl. 1):S166-S173

14. Rolls B. J., Bell E. A., Castellanos V. H., Chow M., Pelkman C. L., Thorwart M. L. Energy density but not fat content of foods affected energy intake in lean and obese women. Am. J. Clin. Nutr. 1999a;69:863-871[Abstract/Free Full Text]

15. Rolls B. J., Bell E. A., Thorwart M. L. Water incorporated into a food but not served with a food decreases energy intake in lean women. Am. J. Clin. Nutr. 1999b;70:448-455[Abstract/Free Full Text]

16. Rolls B. J., Castellanos V. H., Halford J. C., Kilara A., Panyam D., Pelkman C. L., Smith G. P., Thorwart M. L. Volume of food consumed affects satiety in men. Am. J. Clin. Nutr. 1998;67:1170-1177[Abstract]

17. Rolls B. J., Hammer V. A. Fat, carbohydrate and the regulation of energy intake. Am. J. Clin. Nutr. 1995;62(suppl. 1):1086S-1095S[Abstract/Free Full Text]

18. Rolls B. J., Kim-Harris S., Fischman M. W., Foltin R. W., Moran T. H., Stoner S. A. Satiety after preloads with different amounts of fat and carbohydrate: implications for obesity. Am. J. Clin. Nutr. 1994;60:476-487[Abstract/Free Full Text]

19. Saltzman E., Dallal G. E., Roberts S. B. Effect of high-fat and low-fat diets on voluntary energy intake and substrate oxidation: studies in identical twins consuming diets matched for energy density, fiber and palatability. Am. J. Clin. Nutr. 1997;66:1332-1339[Abstract/Free Full Text]

20. Seagle H. M., Davy B. M., Grunwald G., Hill J. O. Energy density of self-reported food intake: variation and relationship to other food components. Obes. Res. 1997;5(suppl. 1):78S

21. Stubbs R. J., Harbron C. G., Prentice A. M. Covert manipulation of the dietary fat to carbohydrate ratio of isoenergetically dense diets: effect on food intake in feeding men ad libitum. Int. J. Obes. 1996;20:651-660

22. Stubbs R. J., Ritz P., Coward W. A., Prentice A. M. Covert manipulation of the ratio of dietary fat to carbohydrate and energy density: effect on food intake and energy balance in free-living men eating ad libitum. Am. J. Clin. Nutr. 1995;62:330-337[Abstract/Free Full Text]

23. van Stratum P., Lussenburg R. N., van Wezel L. A., Vergroesen A. J., Cremer H. D. The effect of dietary carbohydrate:fat ratio on energy intake by adult women. Am. J. Clin. Nutr. 1978;31:206-212[Abstract/Free Full Text]

24. Westerterp-Plantenga M. S., Pasman W. J., Yedema M.J.W., Wijckmans-Duijsens N.E.G. Energy intake adaptation of food intake to extreme energy densities of food by obese and non-obese women. Eur. J. Clin. Nutr. 1996;50:401-407[Medline]





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