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3 Universidade Federal de Pelotas, Departamento de Medicina Social, Pelotas, RS, Brazil; 4 Groningen University, Zoological Laboratory, Haren, The Netherlands; 5 Groningen University, Laboratory of Paediatrics, Groningen, The Netherlands; 6 MRC Human Nutrition Research, Elsie Widdowson Laboratory, Cambridge, UK; 7 Centre for Isotope Research, Groningen, The Netherlands; and 8 Institute of Child Health, MRC Childhood Nutrition Research Group, London, UK
* To whom correspondence should be addressed. E-mail: h.h.haisma{at}med.umcg.nl.
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ABSTRACT |
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 TOP ABSTRACT IntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Introduction |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Subjects and Methods |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Study design.
The study was conducted in Pelotas, a city of 
330,000 habitants and 6000 births/y in the extreme south of Brazil (32° S and 52° W). The study was designed as a cross-sectional study to compare TEE, minimal observable energy expenditure (MOEE), and activity energy expenditure (AEE) among infants 8 mo of age from middle and low socio-economic status (SES). Participation of each mother-infant pair was for a period of 3 wk. All measurements were done by qualified fieldworkers at the homes of the participating babies. During the first 14 d of data collection, breast-milk intake was measured using the dose-to-the-mother 2H2O turnover method. During 1 d in the second wk of the study, food intake was measured by food-weighing. On d 14, a dose of doubly labeled water (2H218O, DLW) was given to the baby, and urine samples were collected until d 21. During this last week, sleeping metabolic rate and child development were also assessed. Morbidity was monitored throughout the study period.
Subjects.
An electronic database (SINASC), including all birth registrations in Pelotas, was used for the random selection of mother-baby pairs. Mother-baby pairs were selected on the basis of maternal education: 
3 y, low education, low SES group; or maternal education 
8 y, middle education, or middle SES group. All babies were healthy at the beginning of the study.
Environmental factors, indicators of socio-economic status.
A standardized questionnaire was used to collect data on parental education, family income, employment, availability of water and sanitation, crowding, parity, and smoking behavior. Schooling of the father was categorized in the same way as for the mothers (3 y; 3.1–7.9 y; 8 y). Income was categorized using minimum wages for Brazil (at the time of the study this was R$180/mo, or $80/mo). Crowding was defined as:
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Prevalence of obesity.
The prevalence of obesity was assessed on the basis of BMI (kg/m2). At 8 mo of age, infants were classified as being overweight or obese using cut-off points corresponding to a BMI of 25 for overweight and 30 for obesity at age 18 y, as suggested by Cole et al. (23). Z-scores were calculated from the BMI data available from our population of infants:
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For girls Z-scores of 1.19 and 2.0 were used as cut-off points for overweight and obesity, respectively, and for boys these values were 1.30 and 2.0.
Intake of complementary foods, minimal observable energy expenditure, anthropometry, and morbidity. Intake of complementary foods was measured by 1-d food weighing using a mechanical scale calibrated against standard weights. SMR and MOEE were measured by respiration calorimetry using a Deltatrac MBM-100. SMR (kJ/min) was defined as the mean of energy expenditure during a period of 40 min to 1 h of sleep, and MOEE (kJ/min) was defined as the mean of the 5 consecutive lowest 1-min values for energy expenditure (kJ/d). Measurements were made at a time the infant would usually sleep. Weight and length were measured. Morbidity questionnaires were applied twice weekly. Details of these measurements can be found elsewhere (22).
Breast-milk intake and total energy expenditure. The dose-to-the-mother 2H2O turnover method was used to measure breast-milk intake, but this was combined with the subsequent measurement of TEE using 2H218O. Details of the basic breast-milk measurements have been described elsewhere (22,24), but, in short, the method involves the administration of 0.5 mol/L (10 g) of 99.8% deuterium to the mother, and collection of saliva samples from the mother immediately before dose administration on d 0 (predose), and subsequently on d 1, 3, 13, and 14. Urine samples were collected from the baby on d 0 (predose), and on d 1, 2, 3, 13, and 14. For the measurement of TEE an oral dose of 0.18 g/kg H218O and 0.10 g/kg 2H2O was administered to the infant on d 14 shortly after the collection of the d 14 sample for the breast-milk estimates. The dose was slowly fed into the baby's mouth using a nasogastric tube attached to a syringe. Any spillage was collected using preweighed tissues. The exact dose administered was calculated from the difference in weight of the dosing vial, syringe, nasogastric tube, and tissues pre- and postdosing, and was, on average, 84% of the dose prepared. Subsequently, urine samples were collected from the baby on d 15, 16, 17, 20, and 21. During the field work, samples were stored on ice, and thereafter at –20°C. Samples were shipped unfrozen to Cambridge, for analysis.
Calculations.
For the measurement of 2H2O kinetic parameters, 2H enrichment above d 0 baseline, measured at the defined times in the period from d 0 to d 14 for the mother and d 0 to 21 for the baby, were fitted to the basic lactation model described by Haisma et al. (24) but including the additional 2H isotopic dose at d 14. In this way residual 2H reaching the baby from the mother could be accounted for during the TEE measurement phase (d 14–21). For the mother,
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where Em(0) is 2H isotopic enrichment above background (ppm) immediately after the first isotope dose, Em(t) is subsequent enrichment, t is time after the isotopic dose (d) and Kmm is water turnover in the mother (d–1).
For the infant, data for 2H was fitted to:
when t < tD2,
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 | (Eq. 2) |
where Eb(D2) is the initial 2H isotopic enrichment (ppm) appearing as a consequence of the second isotopic dose given at time tD2 (d) after the first dose. Eb(D2) was used to calculate Vb (the 2H distribution space, mol) at this time and values at other times (Eb(t)) were assumed to be in the same proportion of body weight changing linearly over the measurement period. Fbm is the transfer of water from the mother to the baby via breast milk (mol/d) and Fbb is total water loss in the baby (mol/d).
For the infant 18O data were fitted to:
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where E'b(D2) is the initial 18O enrichment following the second isotopic dose. E'b(D2) was used to calculate V'b (the 18O distribution space, mol) at this time and values at other times (E'b(t)) were assumed to be in the same proportion of body weight changing linearly over the measurement period. F'bb is total water plus water equivalents of CO2 loss in the baby (mol/d).
Experimental data were simultaneously fitted to equations 1, 2, and separately to 3 using the "Solver" function in Excel to minimize the sum of the squares of the differences between observed and fitted values for mother and baby data combined. Parameters fitted were Em(0), Eb(D2), E'b(D2), Fbm, Kmm, Fbb, and F'bb.
Calculation of the parameters of breast-milk and other water intake was performed from the fitted data as described by Haisma et al. (24). For TEE, CO2 production (
, mol/d) was first calculated assuming that a constant proportion of the infants' water turnover was fractionated (25):
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where rate constants for isotope disappearance are: 
for 2H and 
for 18O; normalized isotope distribution spaces (N, based on 2H dilution, mol) are:
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and (N', based on 18O dilution, mol) 
; fractionation factors are: 
, 
, and f3 = 1.037; proportion of water losses fractionated (x) is assumed to be 0.2 (26).
was then converted to TEE (kJ/d) from the equation:
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RQ was estimated from the mean food quotient calculated from the composition of the total diet of the infants per study group (27). This was 0.87 in this study. AEE was calculated from the difference between TEE and MOEE.
Total body water and body composition.
Infant total body water was calculated as the mean of the isotope distribution spaces of 2H and 18O corrected for nonaqueous isotope exchange:
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Fat free mass (FFM, kg), fat mass (FM, kg), fat free mass index (FFMI, kg/m2), and fat mass index (FMI, kg/m2) were calculated from total body water as described elsewhere (22) using a hydration coefficient of 79.7% for the infant (28) and 73% for the mother (25).
Sample size. The main study outcome was TEE. The only data available from 8-mo-old breast-fed infants were from Dutch infants, and these data were used for sample size calculations. The TEE of these infants at 8 mo was 347 ± 40.4 kJ/(kg · d) (11). The same authors found an 8% difference in TEE at 8 mo of age between breast-fed and formula-fed infants. To detect a significant difference of the same magnitude in TEE between middle and low SES infants, assuming a standard deviation of 40.4 kJ/(kg · d), the study required 35 infants in each group. These calculations assume a Type I error (alpha) of 5%, 2-tailed, and a Type II error (beta) of 20%, that is, a statistical power of 80%.
To allow for any unforeseen reduction in sample size, we increased the total sample size by 8 (4 middle SES, 4 low SES infants), i.e., 39 middle SES and 39 low SES mother-infant pairs were enrolled.
Figure 1 shows how the participating mother-infant pairs were obtained. Of the 78 infants enrolled, TEE was measured successfully in 65 infants. This sample was used as the basis of analysis. SMR and MOEE data were available from 52 of 65 infants. Food intake data were available from 60 of 65 infants. Breast-milk intake, child development and behavior, and morbidity were evaluated in all 65 infants included.
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Ethics. The study was approved by the Ethical Committee of the Universidade Federal de Pelotas, affiliated with the National Commission on Research Ethics or the Brazilian Ministry of Health, and signed informed consent was provided by the mother.
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Results |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Refusals and drop-outs. Socio-economic, environmental, and anthropometric characteristics did not differ between mother-infant pairs who completed the study and those who refused before or during the study, or were lost due to problems at the stage of isotope analysis.
Confounding factors. Gender was not a confounder of the association between TEE and SES. Normalized to weight, TEE was 284 ± 65.7 in boys vs. 291 ± 79.1 kJ/(kg · d) in girls (P = 0.672). In contrast, ethnicity differed between SES groups (see Subjects section), and TEE [kJ/d, kJ/(kg · d), kJ/(kg FFM · d)] differed between white and nonwhite infants. Normalized to weight, TEE was 272 ± 76.4 kJ/(kg · d) in white infants as compared with 316 ± 56.8 kJ/(kg · d) in nonwhite infants (P = 0.019). Further analysis (see below) showed that the inclusion of ethnicity in the regression model resulted in a 10% decrease in the crude difference of TEE between study groups (middle vs. low SES). Ethnicity was therefore treated as a confounder in subsequent analyses of TEE, and all analyses concerning TEE were adjusted for ethnicity.
Indicators of socio-economic status and environmental characteristics. All indicators of SES and environmental characteristics included in the questionnaire differed between SES groups (Table 2).
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Activity energy expenditure. AEE [TEE-MOEE, kJ/d, kJ/(kg · d), kJ/(kg FFM · d)] differed between study groups. Unadjusted means were 394 ± 616 kJ/d in middle SES infants and 927 ± 583 kJ/d in low SES infants (P = 0.002). Normalized to weight, these values were 46.3 ± 70.8 kJ/(kg · d) for middle SES infants and 117 ± 70.4 kJ/(kg · d) for low SES infants (P = 0.001); and normalized by FFM, AEE was 66.2 ± 100.5 kJ/(kg FFM · d) in middle SES infants and 159 ± 97.6 kJ/(kg FFM · d) in low SES infants (P = 0.001). AEE did not differ between sexes. Ethnicity was a confounding factor in the association of AEE and SES, but differences remained significant even after adjustment for this variable (Table 4). Comparisons based on AEE calculated as the difference between TEE and SMR gave similar results.
Energy and macronutrient intake. Breast milk provided 55.7 ± 28.1% of the infants' energy intake; cow's milk, 10.4 ± 17.3%, and solids, 33.9 ± 18.7%. In terms of nutrients, 51.9 ± 6.7% of the energy was from carbohydrates, 39.8 ± 9.3% from fat, and 10.5 ± 3.1% from protein. There were no differences between middle and low SES infants.
Breast milk intake did not differ between the middle SES (689 ± 334 mL/d) and low SES, (638 ± 325 mL/d, P = 0.535), but intake of cow's milk tended to be higher in low SES (162 ± 224 mL/d) compared with middle SES (69.1 ± 174 mL/d, P = 0.079) infants. The percentage of infants receiving breast milk as the only source of milk (i.e., not receiving any cow's milk) did not differ between groups (middle SES, 53.1% vs. low SES, 51.5%; P = 0.897). Energy and macronutrient intakes did not differ between middle SES [367 ± 89.0 kJ/(kg · d)] and low SES [404 ± 114 kJ/(kg · d); P = 0.163] infants (Supplemental Table 1), and were not correlated with weight, FFM, or FM. Ethnicity and sex were not confounding factors in the association of energy intake and SES.
Morbidity. There were n o differences in morbidity between middle and high SES infants (Supplemental Table 2).
Mediating factors for TEE. Of the potential mediating factors, TEE (kJ/d) was positively correlated with intake of cow's milk (mL/d, r = 0.272, P = 0.037). TEE tended to be correlated with weight (r = 0.200, P = 0.130) and FFM (kg, r = 0.200, P = 0.129), but not with FM (r = 0.07, P = 0.575). TEE (kJ/d) tended to be negatively correlated with breast-milk intake (mL/d, r = –0.230, P = 0.068). Health status was not associated with TEE (kJ/d), nor were the number of days an infant presented diarrhea, fever, running nose, or cough correlated with TEE [kJ/d or kJ/(kg · d)].
Inclusion of the intake of breast milk or cow's milk into the model had no effect on the difference in TEE between groups.
Crowding as a mediating factor of AEE. AEE (kJ/d) (adjusted for ethnicity) was not correlated with any of the indicators of nutritional status and morbidity. AEE (kJ/d) tended to be positively correlated (P < 0.10) with crowding, and maternal weight. Adjustment for crowding reduced the difference in AEE between groups by >10%, to an extent that it was no longer significant; the unadjusted difference between SES groups was –460 (95% CI –856 to –64.7) kJ/d (P = 0.024); adjusted for crowding, the difference was reduced to –352 (95% CI –867 to 184) kJ/d (P = 0.177). Inclusion of maternal weight into the model had no effect on the difference in AEE between groups.
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Discussion |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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The study has both limitations and strengths. A strength of the study was the large sample size per study group. Post hoc power calculations, using means and SD of TEE observed, showed a statistical power of 96%. The large sample size also allowed an investigation of associations between components of TEE and ER and environmental, maternal, and infant characteristics. The cross-sectional study design could be considered a limitation, but for the purpose of the study (i.e., to compare TEE and ER between different socio-economic groups), adequate power at a fixed age was considered more important than having smaller samples at various ages.
The DLW methodology used in this study was modified from the usual procedure in that a dose of DLW was administered after first applying a dose-to-the-mother 2H2O dilution method for measuring breast-milk intake. The reason for administering the DLW dose after completing the breast-milk intake measurement was to avoid the possibility that expensive H218O would be given to infants who would subsequently drop out of the study. The consequence of this procedure was that there was 2H2O influx from breast milk during the DLW experiment. Ample consideration has been given to this issue in the analysis. The model applied to the isotopic data accounted for the 2H2O influx but because it is more complex than that normally used, the larger population CV of TEE [kJ/(kg · d)] observed in this study [25% compared with the 19% observed by Butte et al. (10) in 9-mo–old infants] is not unexpected. Isotope dilution spaces and fractional turnover rates indicate no methodological difficulties. The difference in TEE between SES groups was found in all terciles of the breast-milk intake distribution (results available from the author). Thus, the modified method may have been the origin of the larger population CV of TEE [kJ/(kg · d)] observed in this study but is unlikely to have contributed to a general or group-specific bias.
A priori, we hypothesized that TEE and ER could possibly be higher in low SES infants due to the strain of the environment, thereby increasing basal metabolic needs, for example, as the result of infections or for catch-up growth. However, although TEE was higher in low SES infants, we did not find a difference in MOEE or SMR, and therefore our a priori hypothesis was not confirmed. Rather, the low TEE in middle SES infants was the result of low AEE in those infants. Weight and height were higher in middle SES infants, as was the prevalence of overweight. Although energy intake did not differ between groups in this sample of infants, in the larger sample of 78 infants that were initially enrolled, energy intake tended to be lower in the high SES infants (P = 0.08). The differences in body composition and weight gain did not reach statistical significance, but were in the expected direction, and may well become significant in a larger sample, with adequate power. This may be a lesson for planning of future studies.
MOEE and AEE were available only from 52 of 65 infants. To maximize statistical power, 65 infants were included in the analysis for comparison of TEE and anthropometric variables. Results of these variables were similar in the subgroup of 52 infants from whom MOEE and AEE were available.
Analysis of covariance showed that the difference in AEE was mediated by crowding. Its inclusion into a multivariate model reduced the difference between groups to an extent that it was no longer significant. Crowding was the only environmental variable that had a significant impact on the difference in AEE between groups. Whether crowding refers just to the number of people per bedroom, or whether it should be considered in a broader sense, including other living or housing conditions, cannot be concluded from this study simply because of the limited number of socio-environmental factors included. The Brazilian Institute for Geography and Statistics uses crowding as an indicator of quality of life (32). We expect crowding to be inversely related to time spent sleeping. Infants from low SES live in small houses, sometimes sleep with 8 people in one room, and it is likely that they sleep or rest less and thus spend more energy on activity. Crowding is also likely to be related to housing facilities such as ventilation and heating but the real significance of the "crowding factor" remains to be unraveled.
Ethnicity was a confounder in the association of SES and TEE and AEE, and analyses were therefore adjusted for this factor. However, this does not imply that there is a genetic origin for the differences in TEE between white and nonwhite infants. Rather, if a regression model is used to explain differences between ethnic groups, SES appears as a highly significant mediator (results not shown). We should therefore conclude that the difference between ethnic groups is mediated through SES, and is phenotypic rather than genetic.
Comparison of mean TEE observed in this study (288 ± 72.8 kJ/(kg · d)) with findings from others at this age (see Table 5, 10,11,15,17,26,33–35) showed that it is slightly lower than usual found, though within the 95% CI of values published by Butte (10), and is approximately on the 25th percentile as published by Reichman et al. (35).
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In conclusion, energy expenditure was found to be 24% higher in breast-fed infants from low SES compared with breast-fed infants from middle SES at 8 mo of age. The difference in TEE between middle and low SES infants is attributed to AEE, and reflects the difference in lifestyle between the categories of SES. Prevalence of overweight was also higher in middle SES infants, and although the longer-term implication of these findings is not known, it may be a matter of concern in relation to the development of obesity later in life. Furthermore, the findings question the extent to which TEE data, based on middle SES infants, should be considered normative for the age group.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supplemental Tables 1 and 2 are available with the online posting of this paper at jn.nutrition.org.
9 Abbreviations used: AEE, activity energy expenditure (kJ/d); DLW, doubly labeled water (2H218O); ER, energy requirements (kJ/d); FFM, fat free mass (kg); FFMI, fat free mass index (kg/m2); FM, fat mass (kg); FMI, fat mass index (kg/m2); MOEE, minimal observable energy expenditure (kJ/d); SES, socio-economic status; SMR, sleeping metabolic rate (kJ/d); TEE, total energy expenditure (kJ/d).
Manuscript received 7 April 2006. Initial review completed 14 May 2006. Revision accepted 1 September 2006.
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LITERATURE CITED |
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