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1 From the US Department of Agriculture, Agricultural Research Service, Children's Nutrition Research Center, the Department of Pediatrics, Baylor College of Medicine, Houston.
2 Presented at the symposium Fat Intake During Childhood, held in Houston, June 8–9, 1998. 3 The contents of this publication do not necessarily reflect the views or policies of the UDSA, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government. 4 Supported in part by the USDA, ARS under Cooperative Agreement 58-6250-6-001. 5 Address reprint requests to NF Butte, USDA/ARS, Children's Nutrition Research Center, 1100 Bates, Houston, TX 77030. E-mail: nbutte{at}bcm.tmc.edu.
ABSTRACT
The optimal fat intake for children is discussed in light of their energy requirements. Total energy requirements were estimated from doubly labeled water studies of total energy expenditure (TEE) and the energy cost of growth. Basal metabolic rates (BMRs) were calculated from weight by using the equations of Schofield et al or by indirect calorimetry. Activity energy expenditure and physical activity levels were calculated as TEE - BMR and TEE/BMR, respectively. Weight-specific energy requirements for maintenance and growth changed inversely to the increased energy needed for physical activity in healthy, active children. The total energy requirements of infants increased from 1.4 MJ/d at 1 mo to 4.0 MJ/d at 24 mo. The energy cost of growth decreased sharply from 37–38% to 2% of the total requirement during the first 24 mo of life. Energy requirements increased from 4 MJ/d at 2 y to 11 MJ/d at 18 y in girls and from 5 to 15 MJ/d in boys. The energy cost of growth varied between 1% and 4% of total energy requirements in childhood and adolescence. The current recommendation of 30% of energy from dietary fat for children aged >2 y is sufficient for adequate growth. Lower fat intakes may be associated with inadequate vitamin and mineral intakes and increased risk of poor growth. Diets higher in fat may lead to higher energy intakes and higher body fat, although available data for children are conflicting. Beyond infancy, children can meet their energy needs for maintenance, physical activity, and growth from a diet providing 30% of energy from fat.
Key Words: Energy requirements • fat intake • basal metabolic rate • physical activity • energy expenditure • infants • children
INTRODUCTION
The role of dietary fat in mammalian species extends beyond the absolute requirement for essential fatty acids. The high energy density of fat allows the young of many species to meet their high energy requirements. Weight-specific metabolic rates and growth rates peak during infancy (1). Blaxter (2) correctly predicted that the energy density of mammalian milks varies with newborn weight raised to the power of -0.25 to -0.27. Smaller species need to ingest more energy per unit of body size than do larger species to meet their energy requirements, which are higher per unit of body weight. Although body size and growth rate are key variables affecting milk composition, species-specific factors such as the duration of gestation and lactation, physical constraints such as gastrointestinal capacity, and behavioral factors such as feeding frequency also affect the optimal energy density of milk. The lipid content across species varies widely, ranging from 36% to 91% of energy (3). Human milk provides 50% of infants' requirements for energy at a time of maximal metabolic rate and growth. Dietary fat also plays an important role in neural development, immune defense, and possibly maturation. Attainment of puberty in mammals is delayed by undernutrition, usually accompanied by low dietary fat consumption. As in other species, the optimal amount of dietary fat for infants and children depends not only on energy and essential fatty acid needs (2–4% of dietary energy), but also on physiologic and behavioral factors.
ENERGY REQUIREMENTS OF INFANTS AND CHILDREN
Energy requirements of infants and children may be derived from total energy expenditure (TEE) with an allowance for growth. TEE estimated by doubly labeled water (DLW) encompasses the basal metabolic rate (BMR), thermoregulation, and the synthetic cost of growth and physical activity. The energy deposited in newly accrued tissues is added to TEE to get the total energy requirement.
DLW studies published through 1993 on the TEE of infants during the first year of life were compiled in a previous publication (4). In this article, the TEE database was expanded to include children through 2 y of age by using published (5–7) and unpublished data (NF Butte, unpublished observations, 1999). The BMR was estimated from weight by using equations published by Schofield et al (1). Activity energy expenditure (AEE) was calculated as the difference between TEE and BMR. BMR, AEE, and TEE are displayed graphically in Figure 1 (MJ/d) and Figure 2 (MJ•kg body wt -1•d-1). For children <2 y of age, the rates of weight gain and the proportion of fat to protein deposition published by Fomon et al (8) were used to compute energy deposition. Total energy requirements increased from 1.4 MJ/d at 1 mo to 4.0 MJ/d at 24 mo (Table 1, Figure 3). The energy cost of growth decreased sharply from 37–38% to 2% of the total requirement during the first 24 mo of life.
FIGURE 1. . The basal metabolic rate (BMR), activity energy expenditure (AEE), and total energy expenditure (TEE) of girls and boys from birth to 18 y of age.
FIGURE 2. . The weight-specific basal metabolic rate (BMR), activity energy expenditure (AEE), and total energy expenditure (TEE) of girls and boys from birth to 18 y of age.
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TABLE 1. Energy requirements of infants and young children 0–24 mo of age1
FIGURE 3. . Energy requirements of girls and boys from birth to 18 y of age, partitioned into basal metabolic rate (BMR), activity energy expenditure (AEE), and energy cost of growth (ECG).
For older children, the compilation of DLW studies by Black et al (9) was modified to include only TEE results of normal-weight children and additional publications that presented subjects by sex and weight (Table 2) (7, 10–17). The BMR was measured by indirect calorimetry or estimated from weight by using the Schofield equations (1). AEE was calculated as TEE - BMR. BMR, AEE, and TEE are displayed in Figures 1 and 2. Weight-specific energy requirements for maintenance and growth changed inversely to the increased energy needed for physical activity in healthy, active children. To derive the total energy requirements, TEE was added to the energy deposition, based on Tanner weight velocities (18) and an energy content of 20 kJ/g tissue deposited. The readily available DLW studies for children >9 y of age are limited, precluding a detailed tabulation of energy requirements; however, tentative energy requirements are depicted in Figure 3. Energy requirements in girls increased from 4 MJ/d at 2 y to 11 MJ/d at 18 y. The increase was greater in boys, ranging from 5 to 15 MJ/d. The energy cost of growth varied between 1% and 4% of total energy requirements in childhood and adolescence. The energy content of newly synthesized tissues varies in childhood, particularly during the childhood adiposity rebound and adolescent growth spurt, but these variations minimally affect the total energy requirements of children. Consistent with the prolonged juvenile phase in humans, the energy cost of growth as a percentage of total requirements drops dramatically during the first 2 y of life and remains low thereafter.
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TABLE 2. Mean total energy expenditure (TEE), basal metabolic rate (BMR), activity energy expenditure (AEE), and physical activity level (PAL) measured by doubly labeled water and respiration calorimetry
An index of physical activity level (PAL) can be derived by dividing TEE by BMR. PAL values derived from DLW studies of infants and children are displayed in Figure 4; the large scatter reflects differences in lifestyle, geographic habitat, and socioeconomic conditions. Torun et al (19) reviewed PALs estimated by DLW, heart rate monitoring, and time-motion records in children. The mean PAL was between 1.3 and 1.5 for children <5 y of age and between 1.5 and 1.9 for children 6–18 y of age living in urban settings in industrialized countries. There is a lack of information on TEE in children living in rural areas in developing countries.
FIGURE 4. . The physical activity level (PAL) of girls and boys from birth to 18 y of age, calculated by dividing the total energy expenditure (TEE) by the basal metabolic rate (BMR).
The energy requirements of infants and children vary markedly because of variations in growth rate and physical activity (20). Energy needs for growth are highest in infancy. The growth rate slows in toddlers, but activity levels are high and appetite and food intake tend to be erratic. Energy-dense foods enable toddlers to meet their energy needs. In older children, growth is more constant, but energy needs still vary within and between individuals. Fluctuation in appetite is common; fatigue, excitement, and vigorous activity can interfere with or augment appetite. In adolescents, changes in growth, maturation, and occupational and recreational activities impinge on energy requirements. Physiologic and behavioral factors influence the optimal macronutrient composition of the diet needed to meet the energy needs of infants and children.
RECOMMENDED AND OBSERVED DIETARY FAT INTAKES OF INFANTS AND CHILDREN
The American Academy of Pediatrics (21) and the American Heart Association (22) recommend that children >2 y of age derive 30% of energy from fat. No restrictions in dietary fat were recommended for children <2 y of age. The World Health Organization recommends that during weaning and at least until 2 y of age, a child's diet should contain 30–40% of energy from fat and provide an amount of essential fatty acids similar to that found in human milk (23). Infants in developing countries are traditionally weaned onto cereal or tuber-based diets with a low energy density. The use of fat, especially vegetable oils, is encouraged in weaning preparations for infants and toddlers to maintain the energy density of the diet. Beyond 2 y of age, the World Health Organization recommends 15% of energy from dietary fat.
Dietary fat during the first 6 mo of life is controlled in infants fed human milk and infant formulas, which both provide 50% of energy as fat. A review of studies from Europe and North America, however, indicated wide variation in the fat content of diets of children 6–36 mo of age; mean dietary fat ranged from 27% to 42% of energy, with several diets containing <30% of energy (24). In the Copenhagen Cohort Study on Infant Nutrition and Growth, dietary intake was assessed at 2, 4, and 6 mo of age in 87 infants (25). At 2 and 4 mo of age, mean dietary fat was 51–52%, 45–48%, and 44–47% of energy in infants exclusively breast-fed, partially breast-fed, and formula-fed, respectively. By 9 mo of age, the dietary fat content declined to 32% and 31% in infants partially breast-fed or weaned and formula-fed, respectively. The energy density of the diet was 2.8 kJ/g at 4–5 mo and increased as weaning foods (3.1 kJ/g) were introduced.
Studies conducted at the Children's Nutrition Research Center (CNRC) in Houston confirm low fat intakes in some children during the first 2 y of life. In a longitudinal study of 76 breast-fed and formula-fed infants, dietary fat averaged 48%, 41%, 35%, and 30% at 3, 6, 12, and 24 mo of age, respectively (NF Butte, J Hopkinson, unpublished observations, 1999).
The third National Health and Nutrition Examination Survey provided representative data on the dietary intake of American children. This latest survey indicated that children 1–19 y of age consumed on average 34% of energy as dietary fat (26). Similar results were found in the US Department of Agriculture 1989–1991 Continuing Surveys of Food Intakes by Individuals (27): the total fat intake was 35% of energy and the discretionary fat intake was 25% of energy in children 2–19 y of age.
Although complex carbohydrates ideally should substitute for the displaced fat in low-fat diets, fat was replaced with sugar in the Bogalusa Heart Study (28) and in the Oslo Study (29). In Oslo, the mean fat intake of children 8–12 y of age was 31% of energy; 44% of children reported consuming <30% of energy as fat.
ROLE OF DIETARY FAT IN MEETING THE ENERGY REQUIREMENTS TO MAINTAIN ADEQUATE GROWTH IN INFANTS AND CHILDREN
Even though the energy cost of growth is a minor component of total energy requirements, growth rate is a sensitive indicator of overall diet adequacy. There is no convincing evidence that a dietary fat intake of 30% of energy adversely affects the growth and development of healthy children, whose diet supplies adequate energy and essential nutrients.
A review of studies from Europe and North America found little evidence of adverse effects of a diet low in fat on the growth of children 6–36 mo of age (24). The percentage of energy as fat in the diet was not correlated with energy intake, growth velocity, or the energy density of the diet between 6 and 12 mo of age, whereas energy density was positively associated with energy intake and weight gain. Energy density, nutrient density, and feeding frequency may be more important than is the dietary fat content in influencing the energy intake and growth of young children. No association between fat intake and growth was detected in 7–13-mo-old infants (30), 2–5-y-old children (31), or 3–5-y-old children (32). In the Special Turku Coronary Risk Factor Intervention Project (STRIP) baby trial, moderately restricted fat intake (25–30% of energy) was not associated with compromised infant growth between 7 and 36 mo (33). A similar intervention with a fat intake of 30–35% of energy in 7-mo-old French infants also did not result in impaired growth between 7 and 13 mo of age (34). Many studies found lower energy intakes with low-fat diets, but no differences in growth. If the diet records accurately reflect habitual intake, these findings raise the possibility of decreased physical activity in infants and young toddlers adapted to low-fat diets.
Some studies of secular trends, migration, and vegetarian diets link dietary fat restriction to slower growth, but these studies are confounded by inadequacies in total energy intake and intakes of other nutrients (35). Some investigators (28, 36), but not others (37), reported unsatisfactory intakes of vitamins and minerals with low-fat diets. A cohort of 500 Canadian preschoolers was stratified according to fat intake: <30%, 30–40%, or 40% of energy from fat between 3 and 6 y of life (36). A low fat intake was associated with inadequate intake of fat-soluble vitamins. For children habitually consuming low-fat diets, the odds ratio of being below the 50th percentile of weight-for-age was 2.3 at 6 y.
The role of dietary fat in the development of obesity in children is not clear. In growing animals, the proportion of fat deposited increases as the amount of food consumed increases and as the amount of fat in the diet increases (2). Rats offered a high-fat diet consumed the same amount of energy as did controls, but gained more weight with the diet containing more fat (88% compared with 56%). Dietary fat has a high efficiency for promoting energy retention. On the basis of biochemical stoichiometry and empirical evidence from animal experiments, the efficiency of fat synthesis when dietary fat is the source of energy is 96% (2).
The relation between dietary fat intake and body fat in children was examined in many studies. Unfortunately, the commonly used method, skinfold-thickness measurement, is not the most sensitive predictor of body fat. The effect of dietary fat on the growth of 140 children in New Zealand was examined from infancy to 8 y of age (38). The median percentage of dietary fat intake fell from 44% at 3 mo to 36% at 6 mo and remained at a similar level until 8 y, except for a slight increase to 38% at 2 y. At each age interval, no significant differences in height, weight, or skinfold-thickness measurements were observed among children consuming <30%, 30–34.9%, or >34.9% of dietary energy as fat.
Maffeis et al (39) recorded a diet history and measured the skinfold thicknesses of 82 prepubertal Italian children. The mean fat intake was 36.6% in obese children and 33.8% in nonobese children. The percentage of dietary fat was weakly correlated with the percentage body fat mass (r = 0.28, P = 0.01). Gazzaniga and Burns (40) studied 48 lean and obese American children and reported that the obese children consumed higher proportions of total energy as fat. The percentage body fat mass was positively correlated with dietary fat intake (r = 0.55, P = 0.0001), independent of total energy intake.
Fisher and Birch (41) found that children who preferred high-fat snacks consumed a high percentage of total energy as fat and had high triceps skinfold-thickness measurements. Ricketts (42) obtained the diet records, preference ratings of high- and low-fat snack foods, and skinfold-thickness measurements of 88 US children aged 9–12 y. Their mean fat intake was 34% of energy. Children who preferred the high-fat snacks had high dietary fat intakes. A preference for high-fat food was associated with higher body mass indexes and triceps skinfold-thickness measurements.
OTHER CONSIDERATIONS OF THE ROLE OF FAT IN DIETS OF CHILDREN
The present recommendations of the American Academy of Pediatrics (21) and of the American Heart Association (22) to consume 30% of energy as fat apply to the entire population >2 y of age, irrespective of age and sex. Even though epidemiologic data do not suggest problems associated with a fat intake of 30% of energy, the metabolism and metabolic consequences of varying the fat content in the diets of infants and children have not been studied thoroughly.
A small study of children 5–10 y of age suggested that children may preferentially oxidize dietary fat (43). Oxidation of [1-13C]palmitic acid, estimated as the percentage of the administered dose excreted as breath 13CO2, was significantly higher in children (44.7% in girls and 48.1% in boys) than in adults (22.2% in men and 26.5% in women).
Molnár and Schutz (44) compared rates of fat oxidation in 159 obese and 235 nonobese (control) adolescent boys and girls. The postabsorptive respiratory quotient (RQ) was lower in the obese than in the nonobese children, indicating higher fat oxidation (42.3%) than in the control subjects (28.7%), even after adjustment for fat-free mass. Fat oxidation (g/24 h) was positively correlated with fat-free mass and fat mass. Fat oxidation (g/24 h; %TEE) rose during puberty in both groups and was explained by differences in body composition. The postabsorptive RQ was also significantly lower in obese than in nonobese prepubertal children (39).
In studies conducted at the CNRC, 24-h respiratory calorimetry was performed in numerous children fed a diet providing 30% of energy as fat. The mean 24-h RQ was 0.89. Fat oxidation represented 30% of TEE, as expected, but high variability was observed among individuals (CV: 30%). A CNRC study currently underway is examining metabolic adaptation to high-fat (55%) and low-fat (25%) diets in prepubertal and adolescent children. Preliminary results suggest considerable metabolic flexibility in children's ability to oxidize different amounts of dietary fat, but again the variable response observed in children strongly suggests that there are additional factors that modulate fat utilization (M Haymond, A Sunehag, M Treuth, NF Butte, D Bier, unpublished observations, 1999).
CONCLUSIONS
Current recommendations for persons 2 y of age to consume 30% of energy as fat are sufficient to ensure adequate growth. Lower fat intakes (<30% of energy as fat) may be associated with inadequate intakes of vitamins and minerals and increased risk of poor growth. Diets higher in fat may lead to higher energy intakes and higher body fat. The functional consequences of low-fat diets for infants and children should be evaluated in terms of maturation, immune defense, and neural development. Evidence delineating the role of dietary fat in the development of childhood obesity is conflicting and it is uncertain whether dietary fat recommendations should differ for obese children. A more thorough understanding of the factors that modulate fat metabolism in children would provide a sounder basis on which to determine the optimal fat content in the diets of children.
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