Total energy expenditure and physical activity level in healthy young ...

European Journal of Clinical Nutrition (2003) 57, 647–653 ß 2003 Nature Publishing Group All rights reserved 0954–3007/03 $25.00 www.nature.com/ejcn

ORIGINAL COMMUNICATION Total energy expenditure and physical activity level in healthy young Swedish children 9 or 14 months of age C Tennefors1,2, WA Coward3, O Hernell4, A Wright3 and E Forsum2* 1 Semper AB, Stockholm, Sweden; 2Department of Biomedicine and Surgery, University of Linko¨ping, Sweden; 3MRC, Human Nutrition Research, Cambridge, UK; and 4Department of Clinical Sciences, Pediatrics, Umea˚ University, Sweden

Objectives: To measure total energy expenditure (TEE) and total body water (TBW) in healthy Swedish children 9 or 14 months of age. To compare their TEE with current recommendations for energy intake. To define their body composition and relate this to energy expenditure. Design: Children were investigated at 9 or 14 months. The following variables were measured: TEE and TBW (by the doubly labelled water method), weight and length. Total body fat (TBF), sleeping metabolic rate, activity energy expenditure and physical activity level (PAL) were calculated. Subjects: Thirty infants 9 months of age and 29 children 14 months of age. Results: TEE was 323 38, 322 29, 313 23 and 331 28 kJ=kg=day in 9-month-old girls, 9-month-old boys, 14-month-old girls and 14-month-old boys, respectively. At 9 months of age girls and boys contained 29.6 4.8 and 29.7 4.5% TBF, respectively. At 14 months the corresponding figures were 29.1 4.3 and 28.2 4.3%. There was a significant negative relationship between PAL and %TBF (r ¼ 70.81, P < 0.001, n ¼ 59). Conclusions: Measured TEE plus calculated energy cost of growth confirm previous estimates that the physiological energy requirements of children 9 and 14 months of age are 15 – 20% lower than current recommendations for energy intake. One possible interpretation of the relationship between PAL and %TBF is that children with a high TBF content are less physically active than children with less TBF. However, this relationship needs further studies. European Journal of Clinical Nutrition (2003) 57, 647 – 653. doi:10.1038/sj.ejcn.1601591 Keywords: body composition; children; doubly labelled water; energy expenditure; physical activity level

Introduction Knowledge about dietary needs for energy during early life is required for appropriate planning and evaluation of diets for infants and children. Estimates of energy requirements were previously based on energy intake data obtained in dietary surveys. However, in 1985 it was declared that ‘estimates of

*Correspondence: C Tennefors, Semper AB, SE-105 46 Stockholm, Sweden. Guarantor: C Tennefors. Contributors: CT, OH and EF designed the study together. OH was responsible for the larger survey from which the infants were recruited to this study. WAC and AW conducted the isotopic analyses and calculated the doubly labelled water results. CT was responsible for data collection and prepared the manuscript together with EF. All contributors reviewed the paper. Accepted 15 July 2002

requirements should be based on measurements of energy expenditure’ (FAO=WHO=UNU, 1985). Nevertheless, this expert consultation group based its estimates of energy requirements for children up to 10 y of age on the observed intakes of healthy children with normal growth. During the 1980s the doubly labelled water (DLW) method became a practical technique for human use. This noninvasive technique makes it possible to measure the total energy expenditure (TEE) of human subjects during freeliving conditions (Speakman, 1997). The method, which assesses carbon dioxide production rate from the disappearance rate of the stable isotopes deuterium (2H) and oxygen-18 (18O) from the body water pool after an oral administration of these isotopes, has been validated in infants against respiratory gas exchange measurements (Roberts et al, 1986; Jones et al, 1987). Another aspect is that the DLW method also

Total energy expenditure and PAL C Tennefors et al

648 provides estimates of total body water (TBW), an important variable in body composition studies. During recent years this method has been extensively applied in studies on human subjects of all ages. Butte (1996) and Davies (1998) have reviewed studies reporting available data on TEE of infants as assessed by the DLW method. In the compilation made by Butte (1996) the estimated energy requirements were 9 – 39% lower than current recommendations for infants below 12 months of age. Butte (1996) as well as Davies (1998) concluded that estimated energy requirements of infants based on measurements of TEE and growth are lower than the 1985 FAO=WHO=UNU recommendations, providing strong evidence that these are too high and ought to be revised. Furthermore, Prentice et al (1988) have compiled data showing that a similar statement can be made for children during the first part of the second year of life. In the case of young children implementation of new dietary recommendations is associated with several practical and ethical considerations and it is necessary that the scientific foundation for such new recommendations is firm. Further studies of the TEE of children from populations not previously studied by the DLW method are therefore required. Another important reason to study energy metabolism and body composition of young children is the fact that the prevalence and severity of obesity in children and adults are increasing at alarming rates world wide (Koletzko et al, 2000). This health problem is of great concern since obesity is associated with increased morbidity and mortality and contributes to the increasing costs of the health sector. Thus there is a need to develop strategies for prevention and treatment; this requires a better understanding of the specific mechanisms involved when obesity is being established. Studies of the interaction between energy metabolism and body composition during infancy and childhood are therefore needed. During the period 1996 – 1999 a survey of health, nutrition and dietary habits of 300 infants and young children was conducted in northern Sweden. About 60 children from that group were randomly selected to take part in the present study in which energy metabolism and body composition were studied at the ages of 9 or 14 months.

Subjects and methods Subjects All 300 children who participated in the survey were healthy, born at term and lived in the Umea˚ area. Their parents belonged to a middle class population. All had completed 9 y of compulsory education while 35% had a college or university degree. The infants were enrolled in the survey at the age of 5 months. Out of the 300 children, 31 (14 girls, 17 boys) and 34 (15 girls, 19 boys) were randomly selected to take part in the present study at 9 or 14 months of age, respectively. Six of these 65 children were excluded from the study due to minor illnesses (n ¼ 2) or poor parent compliance (n ¼ 4). The study was approved by the ethics committee of the faculty of medicine and odontology at Umea˚ University. European Journal of Clinical Nutrition

Study design Anthropometric and DLW measurements were made when the children were 9 or 14 months old. Anthropometric measurements were taken on the same day as the dose of doubly labelled water was given.

Anthropometric measurements Body weight (naked) and recumbent length were measured during home visits. Body weight was measured to the nearest 0.02 kg (weighing scale for babies – adults 0 – 136 kg, CMS weighing equipment Ltd, London, UK). Length was measured to the nearest 0.1 cm (Rollameter baby measure mat, CMS weighing equipment Ltd, London, UK).

Energy expenditure and body composition Doubly labelled water method. For determination of background abundance of 2H and 18O two urine samples were collected from each child prior to dosing. An accurately weighed dose containing 0.29 0.02 g H218O (Enritech Enrichment Technologies, Ltd, Israel) and 0.09 0.01 g D2O (Sigma-Aldrich, USA) per kg body weight was mixed in an appropriate container with strained fruit or fruit juice at room temperature and fed to the child. A dough scraper was used to completely empty the container. The container was rinsed with juice or tap water and these washings were also given to the child. The dose was completely consumed by all children in the study. Four post-dose urine samples were taken during an 11-day period by the parents using selfadhesive plastic bags (Coloplast AB). The first urine sample was taken on the day after dosing and the second, third and fourth samples on days 4, 7 and 11 after dosing, respectively. The urine samples were transferred to glass vials with an internal aluminium-lined screw-cap seal and kept at þ4 C until sample collection was finished, after which they were stored at 718 C until analysis. Isotope enrichment in dose and urine samples was analysed using a Sira dual inlet mass spectrometer (Hoffman et al, 2000). Carbon dioxide production was calculated according to Davies et al (1994), assuming that 20% of total water losses were fractionated. Isotope dilution spaces were calculated from the zero-time enrichments obtained from the exponential isotope disappearance curves that provided estimates for the rate constants, kd and ko, for 2H and 18O, respectively. Carbon dioxide production was converted to TEE assuming an RQ of 0.85 (Black et al, 1986) using the Weir equation (de Weir, 1949). Body composition. Total body water was calculated as the average of the isotope dilution spaces (Nd and No for 2H and 18 O, respectively) corrected for isotope sequestration of non-water pools in the body, ie Nd=1.04 and No=1.01. Fat-free mass (FFM) was calculated assuming a water content of 79% (girls) and 79.3% (boys) at 9 months of age, and 78.7% (girls) and 78.8% (boys) at 14 months of age. These figures are from the reference data for normal infants


1.05 0.24 1.13 0.22 1.15 0.44 a

Calculated using the National Center for Health Statistics (NCHS-1977) growth reference data (WHO, 1983).

1.07 70.10 0.99 0.26 0.99 1.02 0.25

0.26

0.78 0.69 0.93 0.66 1.13 0.64 0.57 0.70 0.62 0.72 0.54 0.66 0.93

0.54

1.34 0.04 1.00 10.21 0.76 0.52 1.37 0.03 1.12 10.89 0.80 0.42 1.52 0.03 1.32 11.34 0.80 0.56 0.81 0.02 0.77 10.24 0.79 0.23 0.92 0.02 0.88 9.55 0.73 0.62 0.88 0.01 0.83 9.74 0.74 0.52 0.95 0.02 0.95 9.33 0.73 0.73

Weight (kg) Length (m) Weight-for-age Z-scorea Length-for-age Z-scorea Weight-for-length a Z-score

s.d. Mean s.d. Mean s.d. Mean s.d. Mean s.d. Mean s.d. Mean s.d.

All (n ¼ 29) Boys (n ¼ 17) Girls (n ¼ 14)

Boys (n ¼ 16)

All (n ¼ 30)

Girls (n ¼ 12)

14 months 9 months

Table 1 shows anthropometric data for the 59 children in the study including Z-scores (WHO, 1995) for weight-for-age, length-for-age and weight-for-length calculated using the National Center for Health Statistics growth reference data (WHO, 1983). The children in our study were slightly heavier and taller than those in the reference population and with the exception of 14-month-old girls our children tended to be heavy for their length. Almost all (98%) children in the study were breastfed during the first weeks of life and 82% were still partially or exclusively breastfed at 4 months of age. At 9 months of age 40% still received some breast milk. Five percent of the 14-month-old children were being partially breastfed when studied. With respect to the prevalence and duration of breastfeeding, figures for our children were comparable to data obtained for Swedish children in general (Marknadsbyra˚ n, unpublished, 1996 – 1999; Ivarsson et al, 2000). Table 2 presents results obtained using the DLW-method. For all children the mean value for the ratio Nd=No was 1.026 with an s.d. of 0.010. This ratio was not significantly affected by age or sex. The corresponding value for the kd=ko ratio was 0.793 0.016. This ratio was significantly lower for children at 14 months of age than for those at 9 months. TBW as a percentage of weight was similar in the four subgroups. At 9 months of age girls and boys contained 29.6 4.8 and 29.7 4.5% TBF, respectively. At 14 months the corresponding figures were 29.1 4.3 and 28.2 4.3%. Neither age nor sex had any significant effect on the %TBF. Energy expenditure results are shown in Table 3. When expressed per day, boys had significantly higher TEE and SMR than girls, and values at 14 months were higher than those at 9 months. However, when expressed per kg body weight, no significant effects were found for sex or age. On a daily basis AEE was also higher at 14 months than at 9 months of age, but when expressed per kg body weight

Weight, length, weight-for-age Z-score, length-for-age Z-score and weight-for length Z-score for the children in the study

Results

Table 1

Statistical analyses Linear regression and correlation analysis were carried out according to Altman (1999). Significant effects of age and sex were detected using two-way-analysis of variance (Armitage, 1971). The statistical computation was performed using StatWorksTM, Cricket Software Inc. (Philadelphia, PA, USA). Values are expressed as mean s.d.

Mean

9 þ 14 months

Components of energy expenditure. Sleeping metabolic rate (SMR) was calculated from body weight using sexspecific equations developed by Wells et al (1996). Activity energy expenditure (AEE) was calculated by subtracting SMR from TEE. Physical activity level (PAL) was calculated as TEE=SMR.

All (n ¼ 59)

649 described by Fomon et al (1982). Total body fat (TBF) was calculated as body weight minus FFM.

European Journal of Clinical Nutrition


297.4 289.5 1.027 0.193 0.241 0.801 5.62 5.16 55.6 2.80 29.6

20.0 18.7 0.009 0.022 0.023 0.018 0.48 0.34 3.8 0.72 4.8

s.d. 311.5 304.6 1.023 0.181 0.227 0.796 5.86 5.42 55.8 2.92 29.7

Mean 22.2 22.2 0.011 0.020 0.022 0.011 0.48 0.39 3.6 0.62 4.5

s.d.

Boys (n ¼ 16)

304.9 297.6 1.025 0.187 0.234 0.798 5.82 5.30 55.7 2.86 29.7

Mean 22.0 21.7 0.010 0.021 0.023 0.014 0.48 0.38 3.6 0.66 4.6

s.d.

All (n ¼ 30)

329.2 319.8 1.030 0.175 0.221 0.790 6.00 5.70 55.8 3.00 29.1

Mean 21.6 22.5 0.009 0.017 0.018 0.012 0.42 0.39 3.4 0.61 4.3

s.d.

Girls (n ¼ 12)

38.6 36.6 0.009 0.023 0.025 0.018 0.53 0.66 3.4 0.84 4.3

s.d. 351.8 342.3 1.028 0.176 0.222 0.788 6.58 6.10 56.2 3.14 28.6

Mean 37.6 36.5 0.009 0.021 0.022 0.016 0.68 0.65 3.3 0.75 4.2

s.d.

All (n ¼ 29)

2.99 323 1.99 1.00 109 1.51

0.26 38 0.17 0.28 36 0.16

s.d. 3.12 322 2.19 0.93 97 1.43

Mean 0.25 29 0.18 0.23 28 0.12

s.d.

Boys (n ¼ 16)

3.06 322 2.10 0.96 103 1.47

Mean

0.26 33 0.20 0.25 32 0.15

s.d.

All (n ¼ 30)

3.19 313 2.15 1.04 102 1.48

Mean

0.22 23 0.14 0.19 21 0.10

s.d.

Girls (n ¼ 12)

3.72 331 2.52 1.19 108 1.48

Mean

0.28 28 0.32 0.19 27 0.12

s.d.

Boys (n ¼ 17)

14 months

3.50 323 2.37 1.13 106 1.48

Mean

0.36 27 0.32 0.20 24 0.11

s.d.

All (n ¼ 29)

3.27 323 2.23 1.04 104 1.48

Mean

0.38 30 0.30 0.24 28 0.13

s.d.

All (n ¼ 59)

9 þ 14 months

38.5 37.2 0.010 0.022 0.023 0.016 0.72 0.66 3.5 0.71 4.4

s.d.

b

Values for children 14 months of age were significantly different (P < 0.001) from values for children 9 months of age, and values for boys were significantly different (P < 0.001) from values for girls. No significant difference between 9- and 14-month-old children or between boys and girls. c Values for children 14 months of age were significantly different (P ¼ 0.007) from values for children 9 months of age, while values for boys and girls were not significantly different.

a

TEE (MJ=day)a b TEE (kJ=kg=day) a SMR (MJ=day) c AEE (MJ=day) AEE (kJ=kg=day)b PALb

Mean

Girls (n ¼ 14)

9 months

Mean

All (n ¼ 59)

9 þ 14 months

327.9 319.6 1.026 0.181 0.228 0.793 6.16 5.69 56.0 3.00 29.1

Table 3 Total energy expenditure (TEE), sleeping metabolic rate (SMR), activity energy expenditure (AEE) and physical activity level (PAL) for the children in the study

b

Mean

Boys (n ¼ 17)

14 months

367.7 358.2 1.026 0.176 0.224 0.786 6.98 6.38 56.5 3.24 28.2

No significant difference between 9- and 14-month-old children or between boys and girls. Significant difference between 9- and 14-month-old children (P ¼ 0.014), but no significant difference between boys and girls.

a

Nd (mol) No (mol) a Nd=No 71 kd (day ) ko (day71) kd=kob rCO2 (mol=day) TBW (kg) a TBW (%) TBF (kg) a TBF (%)

Mean

Girls (n ¼ 14)

9 months

Table 2 Deuterium and oxygen-18-dilution spaces (Nd and No), Nd=No, disappearance rates for 2H (kd) and 18O (ko), kd=ko, carbon dioxide production rate (rCO2), total body water (TBW) and total body fat (TBF) for the children in the study


650


651

Figure 1 Regression of physical activity level (PAL) on percentage total body fat (%TBF) for all children in the study (n ¼ 59). Regression equation: PAL ¼ 70.024 %TBF þ 2.16 (r ¼ 70.81, P < 0.001).

no effect of age was observed. There were no significant age or sex effects with respect to PAL. Taking into account all the children (n ¼ 59), there was a significant inverse linear relationship between PAL and %TBF (Figure 1). The corresponding relationships were: PAL ¼ 70.032 %TBF þ 2.45 (r ¼ 70.93, P < 0.001) for 9-month-old girls, PAL ¼ 70.025 %TBF þ 2.18 (r ¼ 70.93, P < 0.001) for 9-month-old boys, PAL ¼ 70.015 %TBF þ 1.92 (r ¼ 70.66, P ¼ 0.019) for 14-month-old girls, and PAL ¼ 70.020 %TBF þ 2.05 (r ¼ 70.73, P < 0.001) for 14-month-old boys. Furthermore, when all children (n ¼ 59) were included, PAL was found to correlate significantly with the following variables: TBF (in kg; r ¼ 70.76, P < 0.001) and TBF in relation to body length (in kg=m; r ¼ 70.79, P < 0.001 and in kg=m2; r ¼ 70.78, P < 0.001), while no such significant correlations were found between PAL and the following variables: FFM (in kg) and FFM in relation to body length (in kg=m or in kg=m2).

Discussion There are several available equations by which CO2 production can be calculated when the DLW method is used. We applied the equation published by Davies et al (1994) with the assumption that 20% of total water losses are fractionated. However, inaccurate assumptions regarding the proportion of fractionated water losses have only minor effects on results obtained by the DLW method (Vasquez-Velasquez, 1988). To calculate the body fat content of infants and children from estimates of TBW, an assumption about the degree of hydration of the fat free mass (hydration factor) is needed.

We used the hydration factors of Fomon et al (1982) since these are commonly used. However, Butte et al (2000a) recently presented slightly different hydration factors. Applying these factors to our children resulted in slightly higher %TBF in all groups except in 14-month-old girls, where a 0.1% lower figure was obtained. True estimates of the basal metabolic rate (BMR) are difficult to obtain in young children. We used the equations of Wells et al (1996) to calculate SMR. Using the equations for predicting BMR that were published by Schofield et al (1985) did not affect the results and conclusions of this study. Application of the DLW method to young children is difficult, since this requires that the labelled water is given to the child without spillage or other losses. In the present study we kept the dose volumes relatively small (about 15 g) by using 20% rather than 10% H218O. In addition, the food item in which the dose was mixed was selected together with the parents in order to find something the child really liked. Time was spent together with the child and the rest of the family before dosing, which was started only if the atmosphere was calm, positive and the child was slightly hungry. These precautions helped to assure the successful administration of the dose to each child, and the advantages of taking such precautions are reflected in the internal consistency of our data. When compared with the National Center for Health Statistics growth reference data (WHO, 1983), the children in our study tended to be heavy and tall for their age. On average, %TBF in the 9-month-old infants is similar to the corresponding figure presented by Davies et al (1997), but higher than that reported by Butte et al (2000a). Percentage TBF in the 14-month-old children is higher than corresponding figures presented by others for 12-month-old children (Davies et al, 1997; de Bruin et al, 1998; Butte et al, 2000a). Several authors have reported data indicating that current recommendations for dietary energy intake during infancy and childhood are overestimations of the true physiological requirements. The TEE of our children was 323 30 kJ=kg=day. This is similar to figures reported by Butte et al (2000b), which were 320 40 and 340 50 kJ=kg=day for 9-month-old girls and boys, respectively, and 330 50 and 340 40 kJ=kg=day for 12-month-old girls and boys, respectively. Corresponding figures reported by de Bruin et al (1998) were 320 35 and 343 42 kJ=kg=day for 8-month-old girls and boys, respectively, and 323 27 and 341 35 kJ= kg=day for 12-monthold girls and boys, respectively. Davies et al (1997) presented slightly lower average figures, ie 306 62, 308 55, 325 64 and 322 56 kJ=kg=day for 9-month-old girls, 9-month-old boys, 12-month-old girls and 12-month-old boys, respectively. Recommendations for dietary energy intake consist of an allowance for energy expenditure plus an allowance for the cost of tissue synthesis compatible with normal growth. Assuming that the amounts of protein and fat deposited by the infants studied by Butte et al (2000a) represent normal growth, and using the energy costs for deposition of protein European Journal of Clinical Nutrition


652 and fat of 23.6 and 38.7 kJ=g, respectively, would result in the following energy requirements for the children in the present study: 332 39, 332 30, 320 23 and 339 29 kJ= kg=day for 9-month-old girls and boys and 14-month-old girls and boys, respectively. This in turn would result in energy requirements for the groups that are 17% (9-monthold girls and boys), 20% (14-month-old girls) and 15% (14-month-old boys) lower than current recommendations for dietary energy intake (FAO=WHO=UNU, 1985). Several investigators have identified a significant relationship between indices of physical activity and %TBF in humans. Rising et al (1994) who studied Pima Indians found a significant negative relationship between PAL and %TBF. There are also several relevant studies in paediatric populations. For example, Li et al (1995) found this kind of significant relationship in infants at 6, 9 and 12 months of age in a study where physical activity was measured from observation records and body fat was estimated using dual-energy X-ray absorptiometry (DEXA). In a crosssectional study of children 1.5 – 4.5 y of age a significant inverse linear relationship between PAL and %TBF was found (Davies et al, 1995). Ball et al (2001) also found such a relationship in boys aged 6 – 9 y but not in girls of the same age. However, Butte et al (2000b), who studied 72 children at 3, 6, 9, 12, 18 and 24 months of age, found no significant relationship between PAL and %TBF at any age. This may be related to the facts that, in this study, body composition assessment was based on a multicompartment model rather than on body water determinations only or that SMR of the infants was measured rather than calculated on the basis of body weight. Using the data obtained in the present study we were able to identify a significant inverse linear relationship between PAL and %TBF. This finding may be interpreted in at least two different ways. It is conceivable that a high %TBF tends to discourage physical activity because moving a fat body requires a comparatively large amount of energy. It is also conceivable that a low %FFM, which is bound to be associated with a high %TBF, may be present, since the muscles of the child are poorly developed. This may be the consequence as well as the cause of physical inactivity. In this study PAL was correlated with TBF but not with FFM, indicating that the former rather than the latter interpretation is likely to be correct. One may even speculate that children with a high %TBF and a low PAL are more likely to be in a state of positive energy balance than more active lean children. This would favour fat retention possibly establishing a vicious cycle. Considering that the presence of a significant relationship between PAL and %TBF may have such important implications it should be pointed out that the data used to establish this relationship are derived from variables that themselves to some extent are correlated. Consequently, the interpretation of this relationship that ‘children tend to be less physically active when their body fat content increases’ could be questioned. Nevertheless, since this potentially important relationship has been identified in several studies its true nature needs to be elucidated. ThereEuropean Journal of Clinical Nutrition

fore, more studies are needed of interactions between body composition, physical activity and energy metabolism in children using the DLW method in combination with methods able to provide unrelated estimates of body fat and physical activity. It is not known to what extent overfeeding during early life contributes to the development of obesity later in life. In this context observations published by Stunkard et al (1999) are of interest. These authors presented evidence for the contention that during infancy an excessive energy intake, rather than deficits in energy expenditure, contributes to the fat content of the body at one year of age. Should this be the case, our observation that a relationship between %TBF and PAL may already be present early in life becomes of obvious interest. Taken together, these observations could indicate that an inappropriate feeding regimen as early as during the first year of life may precipitate a vicious cycle leading to accumulation of body fat as suggested above. These aspects of possible interactions between energy metabolism and body composition during early life emphasise the need to establish adequate guidelines for energy intake during infancy and early childhood.

Acknowledgements The authors wish to thank all children and parents who participated in the study. We are also grateful to Margareta Henriksson, RN, for skilful assistance throughout this study. Financial support was received from Semper AB, Sweden, and the Swedish Medical Research Council, project number 12172.

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