Energy Density of the Diet, Food Volume and Energy Intake by Age and Sex in a Healthy Population

Home , Energy density, Volume (thermodynamics)

Energy density of the diet, food volume and energy intake by age and sex in a healthy population

C MartõÂ-Henneberg1*, F Capdevila1, V Arija2,SPeÂrez1, G CucoÂ2, B Vizmanos1 and J FernaÂndez-Ballart2

1Unitat de Pediatria i 2Unitat de Medicina Preventiva, Facultat de Medicina, Universitat Rovira i Virgili, Reus, Spain

Objective: To assess the changes in energy intake (EI), food intake volume (FV) and energy density (ED) related to age and gender in a population in the Mediterranean area of Spain, and to determine the different role of FV and ED on the consecution of the adequate EI throughout lifespan. Subjects: One thousand and eighty-eight individuals (1 ± 65 y) randomly selected from the population census. Design: Cross-sectional study in which food intake was quanti®ed by 24 h dietary recall, three non-consecutive days. Height and weight measurements were taken in 885 individuals. Results: EI, FV and ED increased progressively (P < 0.001) between 1 ± 2 y and 10 ± 12 y of age in both sexes. At 1 ± 2 y the EI is 5.8 Æ 1.5 MJ=d, FV 1195 Æ 275 g=d and ED 4.8 Æ 0.9 kJ=g. Between 1 ± 2 and 3 ± 4 y, coinciding with an EI that increased up to 7.2 Æ 1.5 MJ=d, there was an increase in ED up to 6.1 Æ 0.8 kJ=g (P < 0.001), while the FV did not vary signi®cantly. At the start of puberty, between 7 ± 9 and 10 ± 12 y, when the EI increased to 9.7 Æ 0.9 MJ=d(P < 0.001) in males, the ED rose to 7.1 Æ 0.9 kJ=g(P < 0.001) while the FV did not vary signi®cantly. At this age, a signi®cant difference between the genders was observed in the EI (P 0.04), and in the ED (P 0.02) but not, as yet, in the FV. During adulthood, a signi®cant trend towards decrease (P < 0.001 in both sexes) was observed in EI and ED. However, FV decreased signi®cantly only in females. Conclusions: The changes in energy intake that were observed with respect to age and gender were accommodated-for by changes in the ED of the diet rather than by variations in food volume intake. Auto- regulation of the ED of the diet, suf®cient for energy intake requirement changes, appears to be an essential human capacity for ef®cient nutrition. Sponsorship: This study was funded, in part, by a grant for B Vizmanos from DANONE, Spain. Descriptors: energy density; food volume; energy intake; age; gender; BMI

Introduction development of discriminatory taste in the individual (Cabanac, 1971; Rozin & Vollmecke, 1986; Bellisle, Energy requirements undergo variations over the long term 1992) such that one learns to recognize the energy content changes in life and this implies an adaptation of energy of foodstuffs from their organoleptic qualities (Kissilef & intake to meet the changing requirements. This is especially van Itallie, 1982; Birch, 1992); as a result of this one not so during growth, a period in which energy intake increases only regulates the energy intake by varying the volume of up to puberty so as to meet increased requirements (Butte et food but also one learns to make changes in the ED of one's al, 1995). These trends are reversed with advancing age diet so as to meet changing energy needs. (Roberts et al, 1995). Infancy is the period when the inter-relation between FV One of the factors affecting energy intake is the food intake and ED of the diet to cover the energy requirements volume. This factor increases during the growth phase but is initially appreciated (Fomon et al, 1977; Michaelsen & food volume being conditioned by gastric capacity and Jorgensen, 1995). As has been observed in developing time-course of feeding means that it can become, under countries, an adequate ED of the diet during food-item certain conditions, a limiting factor (Jones et al, 1997; diversi®cation in the course of weaning is essential if risk Kissilef & van Itallie, 1982). of inadequate nutrition is to be avoided (Michaelsen & Energy density (ED) is another regulatory mechanism of Jorgensen, 1995; Stephenson et al, 1994). Similarly, in the energy intake. The capacity to vary the ED of the diet so as case of the malnourished, the importance of ED in a re- to adapt it to changing energy requirements depends on the nutrition regimen is well documented (SaÂnchez-GrinÄaÂn et al, 1992; Brown et al, 1995). Dietary manipulation in experimental animals indicate a clear relationship between FV and ED (Booth, 1972) and it *Correspondence: C MartõÂ-Henneberg, Facultat de Medicina, C=Sant LlorencË 21, 43201 Reus, Spain. would seem that the ability to vary these two factors so as Guarantor: Carlos MartõÂ-Henneberg, MD PhD. to modify energy intake is a capacity of certain species, Contributors: C MartõÂ-Henneberg, V Arija and F Capdevila designed the such as humans, whose omnivorous diet facilitates a wide study, coordinated the ®eld work and wrote the paper. B Vizmanos, S choice of food items of differing nutritional and energy PeÂrez and G CucoÂ did the ®eld work and J FernaÂndez-Ballart did the contents (Rozin & Vollmecke, 1986). statistical analysis and contributed to the realization of the study. Received 9 October 1998; revised 23 December 1998; accepted 1 January Using various experimental diets, several studies in man 1999 have been conducted to investigate the importance of Energy density of the diet C MartõÂ-Henneberg et al 422 variations in ED of the diet (Duncan et al, 1983; Lissner et (1) Meats: including meat, offal, ®sh, shell®sh and eggs al, 1987; Stubbs et al, 1995; Prentice & Poppitt, 1996) but, (2) Cereals: including bread, pasta, pastry, rice etc. and to-date, there is a paucity of information on changes in also including tubers volume and ED of the diet under normal, everyday condi- (3) Vegetables tions (Poppitt & Prentice, 1996). (4) Fruits Our study attempts to describe, using an extensive (5) Milk and dairy products: including yoghourt, cheese, analysis of food intake of a population in the Mediterranean milk-derived sweets, etc area of Spain, the various changes in the energy intake, (6) Oil: including all types of cooking oils, butter, margar- food volume and ED in relation to age and gender and, as ine. In our food preparation, however, almost all the well, to identify those food items of our diet most closely intake of this group corresponds to olive oil related to volume of intake and energy density of this diet. (7) Sugar: table sugar, chocolates, sweets, sweetened We have also studied the relationship between ED and drinks, etc. BMI. In the 885 individuals height and weight measurements were available and the BMI was calculated as weight= height2 (kg=m2). Weight was measured on a portable scale Methods to a precision of 0.1 kg and height with a portable stadi- ometer (Harpenden). This study (Arija et al, 1996) was conducted in Reus, a city All analyses were conducted using the SPSS=PC on the Mediterranean coast of Spain and which contains package. All results are expressed as mean (standard approximately 91 000 inhabitants.. The study sample was deviation). The Student t-test was used to assess differences randomly selected from the population census. The central between consecutive age groups and between the sexes. unit was the family and the number of families selected Simple linear regression analyses were performed in which were representative of all the sectors of the city and of the the dependent variables were EI, ED and FV and the distinct socio-economic levels. The participation rate was independent variable was age expressed in years. Multiple of about 70% and the study sample eventually consisted of regression analyses were also performed in which the 1088 individuals with an age range from 1 ± 65 y. dependent variable was ED and the independent variables Food intake was quanti®ed by the 24 h dietary recall were the different groups of foodstuffs. Simple correlations method. This method, because of its characteristics (its were performed to assess the relationships between BMI realization does not need too much time, fact which favours and ED of the diet in the different age and gender groups. high participation rates; it has a relatively cheap cost; it does not modify the usual dietary habits; and the estimation of the foods consumed is good, as the interval of time Results between the intake and the interview is short), appears to be one of the most appropriate to provide estimates for Energy intake population groups (Cubeau, 1982; Stuff et al, 1983). In a linear regression made taking the sample from 1 ± 15 y Each individual was interviewed on three non-consecu- of age, the analysis showed, in both genders, a signi®cant tive days, one of which being a holiday or weekend. (P < 0.001), progressive increase in EI from the age of 1 ± Present at the interview of the selected individual was 2 y up to the age of puberty (13 ± 15 y). The mean increase the person responsible for the food preparation for the was 0.44 MJ=y in males and 0.38 MJ=y in females. In family or, in the case of small children, the person in another linear regression analysis made for the population charge of the child during the meals (mother, grandmother, older than 15 y of age, the trend was signi®cant (P < 0.001) babysitter ...). An extensive photographic album of stan- but reversed: intake decreased by 0.04 MJ=y in males and dard dishes of the area, food items and portion sizes was by 0.03 MJ=y in females. used to help the subject's memory recall. To evaluate the As shown in Table 1 and in Figure 1, the increase in EI, quantity of some of the food items such as cooking-oils relative to the preceding age-group, was signi®cant at 3 ± used in food preparation, a table-of-contents of quantities 4 y (7.2 Æ 1.5 MJ; P < 0.001) and at 10 ± 12 y (9.7 Æ 2.2 MJ used in certain standard dishes of the area was used as a in males; P < 0.001 and 8.7 Æ 1.9 MJ in females; P < 0.05). reference value. In adulthood a stabilization, followed by a slight decrease, To convert the food items into nutrient values, the TEC was observed in men; the decrease was signi®cant between & DOC Lavoisier-INRA Food Composition Table (Favier the groups of 41 ± 50 and 51 ± 65 y (P < 0.01). The differ- et al, 1997) was used. Originally, the distinct food items ence between sexes with respect to EI starts to become had been grouped and coded in 252 classes. These were, evident in the 10 ± 12 y old age group (P 0.035) and subsequently, re-classi®ed into 66 groups for ease of remains so for all of the rest of the age groups studied. application. To quantify the food volume, the weight of all of the Food volume and energy density food items consumed (both liquid and solid) that contained With respect to FV the linear progression analysis made for energy was summed, except in the case of sweetened drinks the population under 15 y old, indicated that this parameter which were quanti®ed only with respect to the weight of the progressively increased (P < 0.001) with age up to the age carbohydrate content of the sweetener. Certain of the of 13 ± 15 y (mean increase of 26.6 g=y in males and foodstuffs such as cereals and vegetables, whose cooked 26.0 g=y in females). In adulthood, the linear regression and raw volumes differ considerably, had a correction showed that there was a signi®cant diminution in the factor applied for volume. The energy density (ED) was volume consumed by women (P < 0.05) while, in men, calculated as the energy (kJ) divided by the food volume the decrease was not statistically signi®cant. (g). In all the analyses, alcohol consumption was excluded. In the analysis of the differences between the age groups The food items were grouped as the following: (Table 2), the only signi®cant variation appeared in the Energy density of the diet C MartõÂ-Henneberg et al 423 Table 1 Changes in the energy intake (MJ=d)

Energy intake Age n males/females Males Females P between sexes

1±2y,n 38 5.81 (1.5) 3±4y,n 32 7.2 (1.5)*** 5±6y,n 41 7.75 (1.8) 7±9y,n 63 7.95 (1.6) 10 ± 12 y, n 34/42 9.7 (2.2)*** 8.7 (1.9)* 0.035 13 ± 15 y, n 44/22 10.29 (2.6) 8.67 (1.4) 0.008 16 ± 20 y, n 60/63 10.02 (2.6) 7.68 (2.1)* 0.001 21 ± 30 y, n 69/84 9.71 (2.5) 7.39 (2.4) 0.001 31 ± 40 y, n 91/116 9.68 (2.6) 7.50 (2.4) 0.001 41 ± 50 y, n 80/83 9.36 (2.3) 6.93 (1.7) 0.001 51 ± 65 y, n 64/62 8.2 (2.2)** 6.38 (2.0) 0.001

Mean (s.d.).*P < 0.05; **P < 0.01; ***P < 0.001 with respect to the preceding age-group studied.

Figure 1 Energy intake of the diet (MJ/d) with respect to age and gender.

Table 2 Changes in the ED (kJ/g) and food volume (g/d)

Energy density Food volume Age n males/females Males Females P between sexes Males Females P between sexes

1±2y,n 38 4.8 (0.9) 1194.7 (275.0) 3±4y,n 32 6.1 (0.8)*** 1197.2 (303.7) 5±6y,n 41 6.4 (1.1) 1228.4 (304.9) 7±9y,n 63 6.3 (1.1) 1284.4 (249.7) 10 ± 12 y,n 34/42 7.1 (0.9)*** 6.6 (1.0) 0.026 1385.1 (295.7) 1344.2 (285.0) 0.540 13 ± 15 y,n 44/22 6.89 (1.0) 6.4 (0.9) 0.050 1495.6 (324.9) 1380.8 (301.2) 0.171 16 ± 20 y,n 60/63 7.1 (1.3) 5.97 (1.0) 0.001 1427.7 (335.6) 1299.1 (295.0) 0.026 21 ± 30 y,n 69/84 6.5 (1.0)** 5.98 (1.2) 0.005 1520.0 (438.2) 1264.3 (403.3) 0.001 31 ± 40 y,n 91/116 6.2 (1.0) 5.71 (1.2) 0.002 1601.3 (503.1) 1328.4 (372.6) 0.001 41 ± 50 y,n 80/83 6.2 (1.2) 5.34 (1.1)* 0.001 1555.2 (426.4) 1320.3 (302.8) 0.001 51 ± 65 y,n 64/62 5.95 (0.9) 5.41 (1.3) 0.008 1389.1 (307.9)** 1201.0 (315.6)** 0.001

Mean (s.d.).*P < 0.05; **P < 0.01; ***P < 0.001 with respect to the preceding age group. Energy density of the diet C MartõÂ-Henneberg et al 424 group of 51 ± 65 y olds in which a signi®cant decrease very different: on a gram-for-gram basis for example, olive (P < 0.01) in the FV with respect to the preceding age oil explained the maximum change in the proportion of group was observed, both in males and in females. Gender- dietary energy in all the age groups (data not shown). There based differences began at 16 ± 20 y (P 0.026) and were were, conversely, various groups of food items that espe- maintained for the rest of the age-groups studied. cially contributed to the food volume: these were the meats, For the ED, also, two different linear regression analyses cereals, fruits, milk products, and vegetables; the last of were performed. A signi®cant (P < 0.001) trend towards these components beginning to make this contribution at increase in ED of the diet was observed in both sexes from the age of 10 ± 12 y while the others had begun earlier. the 1 ± 2 y old groups through to puberty (up to the age of In relation to the ED, the contribution to the diet of olive 13 ± 15 y; mean increase of 0.24 kJ=g=y in boys and oil and visible sugars are the more determinant elements, 0.22 kJ=g=y in girls) and, subsequently, a signi®cant although cereals, as well, had a positive contribution (P < 0.001) diminution with age was observed (mean (Figure 5). The presence of milk products, fruit and decrease of 0.02 kJ=g=y in men and 0.01 kJ=g=y in women). vegetables decreased the ED of the diet. Figure 2 shows the long-term ED changes. The increase in the ED (Table 2) was signi®cant between 1 ± 2 and 3 ± 4 y of age (P < 0.001). In males there was also a major Correlation analyses between ED and BMI increase in ED between the 7 ± 9 y old and the 10 ± 12 y old When we analyzed the correlations between BMI and ED groups (P < 0.001). Subsequently the ED stabilized and, in for each age-group, we observed signi®cant positive corre- the 21 ± 30 y olds, diminished signi®cantly (P < 0.01). In lations between these two variables in males of 16 ± 20 y of women, there was no signi®cant increase in ED during age (n 45, r 0.44, P < 0.01), of 21 ± 30 (n 53, puberty. In adulthood, as well, a stabilization and a sub- r 0.43, P < 0.001) and of 41 ± 50 y of age (n 65, sequent decrease occurred, similar to that which occurred r 0.29, P < 0.05). No correlations were found between in men except that this diminution in the females was not ED and BMI in women. signi®cant until the 41 ± 50 y old age group (P < 0.05). The differences between genders began to be signi®cant (P 0.026) in the 10 ± 12 y old age group and continued Discussion to be so for the rest of the age-groups studied. Figures 3 and 4 show, one for males and the other for Energy requirements vary throughout life. These variations females, the percentage differences in ED, EI and FV imply an adaptation of energy intake to meet the require- observed between consecutive age-groups. ments; an adaptation involving variation in food volume intake and in the energy density of the food ingested. The results that we obtained in the analysis of the energy Contributions of the different groups of foodstuffs intake are in agreement with the data of other studies All the groups of foodstuffs, except vegetables, contributed conducted in our country (Aranceta et al, 1990; Serra- statistically signi®cantly to the variation in dietary energy Majem et al, 1995). These results obtained from our study in each age group. However, the relative contributions were (one which encompasses a large age range) indicate that,

Figure 2 Energy density of the diet (kJ/g) with respect to age and gender. Energy density of the diet C MartõÂ-Henneberg et al 425

Figure 3 Percentage differences in energy, intake, energy density and food volume between consecutive age-groups in males. The graphic also shows the values of the con®dence semi-intervals which are nearest to zero.

Figure 4 Percentage differences in energy, intake, energy density and food volume between consecutive age-groups in females. The graphic also shows the values of the con®dence semi-intervals which are nearest to zero. Energy density of the diet C MartõÂ-Henneberg et al 426

Figure 5 Foodstuffs and energy density. Multiple regression analysis for each age group, showing the change in energy density (kJ/g) occurred with the variation of the intake of each foodstuff (g).

within the overall long-term variation in energy intake with obtaining an adequate energy intake is observed already in age, certain well-de®ned stages are apparent. very small children. When babies are nourished with semi- The ®rst period, starting within the ®rst year of life skimmed milk, the volume of milk ingested is increased so (Capdevila et al, 1998) and up to puberty, sees a trend as to compensate for the low ED of this milk (Fomon et al, towards a progressive increase in energy intake (77% 1977). As such, specially during infancy, the ED of a diet is increase in boys and 50% in girls; from 1 ± 2 y to 13 ± seen to be an essential factor in maintaining an adequate 15 y). The variations observed in the energy intake during energy intake (Susheela & Narasinga-Rao, 1983). This is childhood are closely related to the physiological phenom- also well demonstrated in the case of the malnourished enon of growth. child in whom it is frequently suf®cient to slightly increase From the ®rst year of life up to 15 y of age, the food the ED of the re-nutrition diet for there to be a substantial volume intake shows a tendency to increase progressively improvement in the nutritional status of the patient (SaÂn- but slowly (25% increase in boys and 16% in girls). chez-GrinÄaÂn et al, 1992; Brown et al, 1995). The changes in ED, in general, show a trend towards a In our study, during the second stage, in adulthood, a signi®cant increase and this parameter seems to follow stabilization of the EI occurs followed by a diminution. The more closely in parallel with the changes in the energy differences between the sexes established at the onset of intake than the food volume parameter. Between 1 ± 2 y and puberty, however, are maintained throughout the succeed- 13 ± 15 y of age, an increase in the ED of 47% in boys and ing age-groups. of 33% in girls is observed. During the ®rst year of life this Paralleling the energy intake, a tendency towards dimin- relationship between the increase in ED and the variation in ished ED of the diet starting with early adulthood is evident EI is even more evident (Capdevila et al, 1998). And the (Table 2 and Figure 2). In the male, slightly after the end of relationship between the increase of the EI and DE between puberty and its anabolic peak, a signi®cant diminution of the groups of 1 ± 2 y and 3 ± 4 y of age, without a signi®cant ED is already observed; especially in the 21 ± 30 y age change in the FV parallel to those, is also very important. group with respect to the previous age group. Conversely, Between the ages of 5 and 9 y, the increase in ED slows- in the oldest age group studied there was no signi®cant down and becomes signi®cantly increased again at puberty; difference compared to the preceding one. Only in the a tendency very much related to that observed in the growth females was there a signi®cant decrease in ED in the group curve. Of note is that this signi®cant increase occurs only in of 41 ± 50 y olds with respect to the previous age group. the boys while it is much lower in the girls so that, by the In adulthood, the FV showed only a slight tendency age of 10 ± 12 y, a signi®cant difference in the ED is towards diminution in the females (13%), similar to the established between the sexes and which is parallel to diminution in ED. In the males the trend was less marked that which occurs in energy intake. (7%). Only in the oldest age-group studies was there an With respect to the relationship between FV and ED, the indication of a signi®cant decrease with respect to the capacity to regulate these two factors with the objective of preceding group. The difference between the sexes in Energy density of the diet C MartõÂ-Henneberg et al 427 food volume intake in adulthood probably re¯ects a greater Food volume, which also changes as a function of age social concern of females about their dietary control. and gender, showed, nevertheless, a less marked relation- The ED of a diet is very closely related to its macro- ship with changes in ingested energy. nutrient composition, especially to its lipid content. Fat The foodstuffs that had a major in¯uence of the ED confers on foodstuffs certain organoleptic qualities that changes were olive oil and visible sugar. Those that had the make them more attractive and contribute strongly to the major in¯uence on food volume were fruit, milk products palatability of the diet (Drewnowski, 1992, 1997). These and vegetables. Cereals and meats play an equilibrating factors ensure that children rapidly learn to prefer those role in density and volume. food items with a high lipid content (Birch, 1992; Kern et In males between 16 and 50 y there was a signi®cant al, 1993), and this preference does not decline with age. relationship between ED and BMI, but which was not The lipid content of foodstuffs is, of course, the main factor signi®cant during growth phase. that in¯uences ED in our society. As such, a high ED diet contains an elevated proportion of lipids, However the autocontrol of lipid ingestion appears less developed than that of the intake of sugars or proteins (Blundell et al, Acknowledgements ÐWe wish to thank Dr Drewnowski for his critical 1996); hence, a diet with high ED could be a factor in advice. We also wish to thank JoseÂ MarõÂa Barroso and Gerard AlbaigeÂs for their help in subject recruitment. Translation, orthography and editorial obesity. Several studies, experimental as well as observa- assistance were by Dr Peter R. Turner of t-SciMed (Reus, Spain). tional, demonstrate the relationship between the lipid content in the diet, its effect on ED and obesity (Blundell et al, 1996; Bolton-Smith & Woodward, 1994; Poppitt, 1995). We explored this relationship and found that, in adult males, there was a signi®cant positive correlation between References ED and BMI. 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